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In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa (1996)

Chapter: 10 Tropical Infectious Diseases

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Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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10

Tropical Infectious Diseases

Despite the growing importance of the chronic diseases in the developing world, the infectious and parasitic diseases are still paramount, and the high proportion of deaths in all age groups in the Sub-Saharan African region attributed to them is striking. These diseases account for one-quarter to one-third of the deaths of young adults in the region and figure prominently in Sub-Saharan Africa's persistently high levels of adult mortality, as well as its large burdens of disability. A number of these infections also play a crucial direct or indirect etiologic role in the genesis of some cancers that are of substantial epidemiologic significance in the Sub-Sahara, as well as in the etiology of rheumatic heart disease, hypertension, and diabetes (Feachem and Jamison, 1991; Ofosu-Amaah, 1991; these associations are discussed in Chapter 7).

There were several sets of criteria that might have been used to select, categorize, and prioritize the diseases addressed in this chapter. Among these were other institutional priorities—for instance, the priorities of the WHO Special Programme for Research and Training in Tropical Diseases (TDR), etiologic similarities, and quantitative or qualitative differences in the effects of given diseases on females as compared with males. The final decision was to use the information generated by the WHO/World Bank assessment of the Global Burden of Disease (GBD) and to select and prioritize the diseases addressed here according to the size of their burden as measured in Disability-Adjusted Life Years (DALYs) (Murray and Lopez, 1994). The GBD estimates are based on an extensive analysis of disease-specific epidemiologic studies and all known population studies of mortality and disability available to the authors. As a consequence, the DALY provides a measure of comparability among these diseases that is particularly useful for this chapter.

The chapter discusses the selected diseases in the following order: malaria, schistosomiasis, African trypanosomiasis; trachoma; dracunculiasis; onchocerciasis and lymphatic filariasis; leishmaniasis and leprosy. Although dracunculiasis (Guinea worm disease) was not among the tropical diseases included in the GBD analysis, we considered it a disease of special programmatic interest for this study because it has a particularly deleterious impact on women, and has been targeted for global eradication by the end of 1995.

Table 10-1 presents the burden of infectious and parasitic diseases in males and females in Sub-Saharan Africa compared with males and females in the rest of the world. Diseases are listed in descending order of the size of the burden as measured in DALYs lost. Table 10-2 presents the burden of disease measured in DALYs for Sub-Saharan Africa by sex and age.

Of the tropical infectious diseases discussed in this chapter, five are life-threatening: malaria, schistosomiasis,

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-1 Burden of Infectious and Parasitic Disease in Males and Females, Worldwide and in Sub-Saharan Africa, by Cause, 1990 (in hundreds of thousands of DALYs lost)

 

Sub-Saharan Africa

Worldwide

Disease

 

M

F

M

F

Malaria

''Tropical cluster"a

Schistosomiasis

Trypanosomiasis

Onchocerciasis

Trachoma

Leishmaniasis

Leprosy

Lymphatic filariasis

161.0

39.0

23.1

9.0

3.7

2.1

1.9

1.2

1.3

154.

25.8

11.8

8.8

2.7

6.9

2.0

1.1

0.5

182.3

75.0

29.9

9.0

3.7

9.3

12.0

5.1

5.6

175.0

51.0

15.4

8.8

2.7

23.7

8.6

5.1

2.9

a Defined as including: trypanosomiasis, Chagas' disease, schistosomiasis, leishmaniasis, lymphatic filariasis, and onchocerciasis (Murray and Lopez, 1994). Malaria, leprosy, and trachoma are addressed separately in the Global Burden of Disease categorization.

SOURCE: Murray and Lope, 1994.

African trypanosomiasis, onchocerciasis, and leishmaniasis. Even when episodes of these diseases do not proceed to mortality, they tend to generate considerable morbidity. This is also true for the other four, nonlethal, diseases addressed in this chapter. Thus, it is morbidity, or disability, that has the greatest weight in the total burden of these diseases as a group. Tables 10-3 and 10-4 desegregate that burden, first in mortality, and second in disability (morbidity).

Finally, Table 10-5 summarizes the gender burden of the tropical infectious diseases in the same fashion as other topics have been presented in each of the chapters of this report: that is, subcategorized by the degree to which the burden of each disease is distinctive for females. Contemplated as a group, the tables indicate that, with little exception, males in Sub-Saharan Africa have higher overall burdens of tropical disease, with higher rates of both mortality and disability, than females experience in the region, although there is significant internal variation.

This general conclusion coincides with several perspectives in the literature that have become almost standard. The first is that the overall worldwide burden of premature mortality and morbidity is higher in males than it is in females, and male life expectancy is correspondingly lower.

The second perspective is that the only noteworthy distinctions between males and females in disease susceptibility and expression lie in their relationship with female reproductive function. One consequence of this viewpoint is that biomedical research on sex differences in infectious disease has focused mainly on that relationship, with emphasis on pregnancy and pregnancy outcomes, placental transmission, and maternally induced protection. Because of these emphases, research into the longitudinal impact of infectious diseases across the female life span, as well as the simultaneous and progressive interactions of those diseases with other maladies and conditions, has been deficient (Feldmeier and Krantz, 1992; Feldmeier et al., 1992; Vlassoff and Bonita, 1994). Table 10-6, which present a detailed analysis of the sequelae of the tropical infectious diseases across the female life span, makes it abundantly clear that such a narrow focus does not fit the facts.

The third perspective is that, with the exception of the role of the reproductive factor, any other differences in male/female mortality and disability rates are caused by variations in the nature and degree of exposure and in the social, economic, cultural, and personal factors that influence both exposure and the impact of a given disease (Brain and Brain, 1992; Bunny and Medley, 1992).

The present state of the scientific literature offers little justification for disagreeing with any of these perspectives, nor has it offered much basis for expecting either sex to be genetically more predisposed to communicable disease infection. Nevertheless, there is reason begin questioning this assumption. Analysis of the influence of

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-2 Burden of Disease Measured in Disability-Adjusted Life Years, by Sex and Age, Sub-Saharan Africa, 1990 (Dallies, in thousands)

   

Males (age group)

 

Females (age group)

 

Differential in Size of Burden, by Gender (%)

Cause

Both Sexes, All Ages

0–4

5–14

15–44

45–59

60+

All Ages

0–4

5–14

15–44

45–59

60+

All Ages

 

Malaria

31,504

12,346

2,372

1,277

78

24

16,096

11,388

2,466

1,428

95

30

15,407

.3

Schistosomiasis

3,490

163

1,675

444

28

6

2,312

79

833

245

17

5

1,178

49.1

Dracunculiasis

a

 

Lymphatic filariasis

90

40

3

132

45

7

51

61.4

Onchocerciasis

641

4

176

124

66

370

3

128

94

47

272

26.5

African trypanosomiasis

1,782

51

395

362

82

9

899

94

356

371

57

5

883

1.8

Leprosy

227

9

93

9

2

3

116

9

86

10

3

4

111

 

Trachoma

901

168

29

14

210

558

 

79

53

690

Leishmaniasis

583

13

186

90

1

219

12

188

91

2

292

 

a No data.

SOURCE: Murray and Lopez, 1994.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-3 Estimated Deaths in Sub-Saharan Africa, by Sex and Age, 1990

   

Males (age group)

   

Females (age group)

 

Cause

Both Sexes

0–4

5–14

15–29

30–44

45–59

60–69

70+

All Ages

Both Sexes

0–4

5–14

15–29

30–44

45–59

60–69

70+

All Ages

Malaria 391.7

805.3

323.5

55.1

19.6

10.0

3.3

1.3

a

413.6

213.2

57.5

20.9

13.6

4.1

1.5

1.5

 

Schistosomiasis

21.0

45.0

4.2

2.1

1.4

13.6

1.9

2.3

1.5

7.4

Trypanosomiasis

55.1

1.5

10.2

7.2

3.6

4.8

28.2

2.7

9.1

6.8

4.4

3.2

26.8

Trachoma

Onchocerciasis

29.1

2.7

1.4

6.1

4.8

2.4

17.3

1.9

1.2

4.6

2.1

1.7

12.4

Leishmaniasis

10.4

3.1

1.0

5.0

3.3

1.1

5.4

Leprosy

Lymphatic filariasis

a No data.

SOURCE: Murray and Lopez, 1994.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-4 Years Lived with a Disability in Sub-Saharan Africa, by Sex and Age, 1990 (YLDs in thousands)

   

Males (age group)

Females (age group)

Cause

Both Sexes, All Ages

0–4

5–14

15–44

45–59

60+

All Ages

0–4

5–14

15–44

45–59

60+

All Ages

Malaria

4,708

1,576

350

391

29

10

2,356

1,561

347

400

32

13

2,353

Schistosomiasis

2,887

148

1,510

255

2

a

1,916

75

762

133

1

971

Dracunculiasis

Onchocerciasis

182

3

55

34

16

108

2

37

23

11

74

African trypanosomiasis

147

2

22

42

12

2

79

3

19

38

7

68

Leprosy

209

8

91

7

107

8

85

7

102

Trachoma

901

168

29

14

210

588

79

53

690

Leishmaniasis

228

2

72

45

119

2

68

39

a

109

a No data

SOURCE: Murray and Lopez, 1994.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-5 Tropical Infectious Diseases Adversely Influencing Health in Sub-Saharan Africa: Gender-Related Burden

Problem

Exclusive to Females

Greater for Females

Burden for Females and Males Comparable, but of Particular Significance for Females

Burkitt's lymphoma

 

X

 

Dracunculiasis

 

X (pelvic infection)

X

Leishmaniasis

   

X (stigmatization)

Leprosy

 

X (in pregnancy)

X (stigmatization)

Malaria

 

X (in pregnancy)

X

Onchocerciasis

   

X (stigmatization)

Schistosomiasis

 

X (ages 15–44)

X

Trachoma

X (neonatal vulvovaginitis)

 

X

Trypanosomiasis

 

X (ages 0–4)

X

NOTE: "Significance" is defined here as having an impact on health that, for any reason—biological, reproductive, sociocultural, or economic—is different in its implications for females than for males.

cross-sex disease transmission on mortality suggests that tantalizing possibility that there may be differentials in susceptibility and disease intensity that are biologically based (Aaby, 1992), and not purely derivative of reproductive function.

Exploration of this possibility will demand a much more expansive research framework, since the questions it raises cover broad areas. For example: Are there are genetic, physiologic, or morphologic traits associated with gender that either exacerbate or attenuate disease in males or females? What might those be? How do any such differences vary by disease, and what mechanisms are involved (Aaby, 1992; Michelson, 1992)? Secondary questions would have to do with the ways those fundamental traits play out in mortality, morbidity, and chronic disability throughout either the male or female life span (Mosley and Gray, 1993). Another set of questions—very complicated questions—would have to do with the causal, synergistic, and cumulative roles of comorbidities, an area where research has just begun.

MALARIA

Malaria remains the most important and widespread of the tropical diseases, and levels of malaria transmission are higher in Sub-Saharan Africa than anywhere in the world (Bradley, 1991). The region accounts for over 80 percent of the 110 million clinical cases worldwide each year, 90 percent of the estimated 275 million people in the world who are infected carriers of the parasite, and most of the estimated one to two million deaths that malaria causes annually (Najera et al., 1993; WHO/TDR, 1991a). Yet, although there has been a vast amount of malariological research over the past century, the true magnitude of mortality and morbidity from the disease is still uncertain (Bradley, 1991). Since reporting from tropical Africa has been irregular and fragmentary, reported cases of malaria may represent only 2 to 20 percent of actual cases (Najera et al., 1993).

The disease is transmitted by four species of the parasitic protozoa Plasmodium: P. falciparum, P. vivax, P. ovale, and P. malariae, each with its own morphology, biology, and clinical characteristics (Miller, 1984). Of

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-6 Biological Consequences of Tropical Infectious Diseases for Women a

Disease

Infancy/Childhood

Adolescence

Adulthood

Pregnancy

Malaria

Infancy: Females are disadvantaged. Fever, weakness, anemia, jaundice, splenomegaly, convulsion, vomiting, diarrhea.

Scant data, only available for pregnant adolescent girls. Clinical signs are similar to signs in childhood.

Anemia, weakness, splenomegaly. Other clinical signs appear to be similar to those in adolescence (more data available for pregnancy).

Hemolytic anemia, cerebral malaria, hypoglycemia, abortion, low birthweight babies, pulmonary edema, placental malaria.

Schistosomiasis

S. haematobium

S. mansoni

Infancy: Scant data. Childhood: Fever, hematuria, weakness, anemia, fatigue, weight loss, muscular pain. In addition, there is lower genital tract disease.

Hematuria, anemia, liver cirrhosis, obstructive uropathy, abortions, delayed menarche, poor growth, delayed puberty, decreased work capacity.

S. haematobium: Genital tract involvement, anemia, liver cirrhosis, obstructive uropathy, abortions S. mansoni: Portal hypertension, obstruction, ascots, gastro-intestinal disruption, granolas

Genital tract involvement (GTI): bladder, ureter S. mansoni (no report on GTI in Africa, intestinal polyposis). S. haematobium: Cancer of the genital tract, bladder and liver; infertility.

Dracunculiasis

Infancy: No signs because of length of incubation period. Childhood : Blister, itching, severe incapacitation from blisters, Guinea worm ulcer and lesions, tetanus death (from secondary infection).

Blister, fever, localized pain, urticaria. Other symptoms similar to symptoms in childhood.

Severe incapacitation from blisters, depending on location. Tetanus, chronic arthritis (common in women).

Bleeding in pregnancy (rare).

Onchocerciasis

Severe and incessant pruritus, lack of sleep, presence of nodules. Lack of data on the impact of these on the health of the girl child.

Severe and incessant pruritus, loss of restful sleep, presbydermia (premature aging of the skin), ocular lesions, dermal atrophy (lizard skin), severe popular eruption (irreverible and disfiguring lesion).

Blindness (common in savanna), weight loss, poor nutrition status, joint and muscular pains and abscesses, severe dermal atrophy (lizard skin), leopard skin, severe and incessant pruritus, loss of restful sleep, presbydermia (premature aging of the skin).

Exacerbation of skin lesions. Other symptoms in nonpregnant adult women persist and are often exacerbated in pregnancy.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

Trypanosomiasis

T. gambiense: Infancy: Low birthweight, somnolence, fever, hepatosplenomegaly, fetal wastage. Childhood: Fever, headache, normochromic anaemia, skin rash, neurologic symptoms, severe mental retardation, death.

Scant data on adolescent females for both types of trypanosomiasis.

T. gambiense: Organic dementia, tremors, hypertension T. rhodesiense : Early stage fever tremor, hepatocellular jaundice, debility, mild-severe anemia, myocardial involvement.

T. gambiense: Increased susceptibility to intrauterine infection, abortion, or sleep and depression, generalized immune depression, cerebral edema.

Trachoma

Maximum active disease.

Repeated infections.

Scarring, disfigurement, blindness.

Pneumonitis, neonatal vulvovaginitis, inclusion conjunctivitis, ophthalmia.

Leishmaniasis

High rate of acquisition.

High rate of acquisition.

High rate of acquisition, severe disfigurement.

 

Leprosy

Low birthweight, poor growth, increased susceptibility to infection.

Poor growth, increased susceptibility to infection.

Loss of asymptomatic status/reactivation/relapse/in pregnancy; nerve damage, blindness.

Reactivation/relapse/nerve damage in pregnancy; impaired placental function.

a There are few data on the biological and social consequences of these tropical diseases for postmenopausal and elderly women in Sub-Saharan Africa. For this reason, no separate column has been created for these life span stages.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

these, it is P. falciparum, the most dangerous, that predominates in Sub-Saharan Africa, followed in frequency by P. malariae and P. ovale (Miller, 1984). The disease is transmitted through the bite of certain species of mosquitoes of the genus Anopheles, which, in Sub-Saharan Africa, includes An. gambiae and An. funestus, two of the three most efficient malaria vectors in the world. The bite of the female anopheline starts a process of inoculation, proliferation, and red blood cell invasion that, in the case of P. falciparum, generates a distinctive pattern of clinical symptoms. It is the high parasitemia of P. falciparum that leads to the splenomegaly, severe anemia, renal failure, and cerebral malaria that produce the severe morbidity and mortality associated with this form of the disease.

Malaria in Children

Mortality and morbidity from malaria are highest in infants and in children under age 5. Malaria morbidity accounts for 10 to 80 percent of childhood fevers, for approximately 30 to 35 percent of all presenting cases recorded at the rural dispensaries in the savanna areas of Sub-Saharan Africa (Bradley, 1991), and from 10 to 30 percent of all infant and child deaths in the region (Najera et al., 1993).

Very few malaria studies present data disaggregated by gender, and this has certainly not been done in any extensive or reliable way. This is largely true for all the tropical diseases, and results from the lack of sensitivity to the possibility of gender-specific differences in disease outcomes mentioned above (Vlassoff and Bonilla, 1994) and, in the case of malaria, from overall methodological confusion (Bradley, 1991).

Malaria studies that have produced gender-specific data present a somewhat blurred picture of gender variation in childhood. Two such studies report higher parasite prevalence and densities in infant girls and female children under age 4 (Hendrickse et al., 1971; McGregor, 1964). A third study, from the well-documented and well-executed Garki project in Nigeria, reported prevalence and parasite density rates in male and female children under age 4 that were approximately the same, and rates in females from age 5 years onward that were lower than rates for males of the same ages (Molineaux and Gramiccia, 1980). The more recent GBD data report a DALY burden for males from birth through age 4 that is higher than it is in females, a difference that arises primarily from higher mortality in infant males than in females of the same cohort. Still, the male burden is only about 10 percent higher than the burden for females, and it is succeeded by a shift to a greater burden in females in all subsequent age cohorts (Murray and Lopez, 1994). On the basis of the Garki data, Reubin (1992) has concluded that females are not intrinsically more susceptible to malaria than males, and may actually mount a stronger antibody response. Apart from pregnancy, Reubin attributes any gender differences in malaria infection to a simple differential in exposure. Because the sex difference among all children ages 0 to 4 years is not dramatically large, however, and the female burden overtakes that of males beginning at age 5, well before pregnancy is a factor, any hypothesized female advantage is at least open to question.

Some of the best longitudinal data on malaria prevalence during childhood come from a series of studies in The Gambia, where the disease is hyperendemic and prevalence of falciparum malaria is close to 100 percent throughout childhood, declining gradually through adolescence into adulthood (McGregor and Smith, 1952). Longitudinal mortality data from the same study series show acute malaria exerting its maximum impact during the first and second years of life, when the transient passive placental immunity and levels of antibody titers against falciparum malaria have diminished; the sequelae of the disease during this period are disrupted growth patterns and anemia (McGregor et al., 1956). Morbidity over the longer period from birth to age 5 includes severe anemia; cerebral malaria; and damage to liver, spleen, and kidney, all of which have potential for progressing to mortality. For survivors, the disease appears to have negative effects on growth rates and on mental and motor development. Study of the sequelae of malaria for child development and performance does not seem to be extensive (Pollitt, 1990; UNESCO, 1989), but preschoolers with iron-deficiency anemia, a known sequela of malaria, repeatedly record lower test scores (Levinger, 1992).

Malaria in Adolescent and Adult Females

If females do have any relative advantage in parasite clearance during early childhood, it surely disappears

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-7 Prevalence of Malaria (Placental Infection or Parasitemia) among Women in Africa, by Parity at Delivery

Area

Prevalence PGa

Percentage MGb

Number Examined

West Nigeria

20.2

11.2

451

Nigeria (Ilesha)

62.5

25.3

392

East Nigeria

36.4

16.3

575

Uganda (Kampala)

21.7

14.7

570

Tanzania (Muheza)

37.0

33.0

413

Côte d'Ivoire (Abidjan)

55.0

36.2

192

Gambia, The (rural)

59.1

35.2

1,000c

Gambia, The (Banjul)

15.7

8.8

2,765

(Provinces)

46.7

20.4

3,194

Gambia, The (Keneba)

64.0

26.3

532

Nigeria (Lagos)

40.0

8.0

230

Zaire (urban and rural)

38.0

15.0

291

NOTE: All data were collected in hospitals and health clinics. Details on antimalarial therapies/prophylaxis were generally not reported.

a PG = Primigravidas.

b MG = Multigravidas.

c Antenatal parasite prevalence.

SOURCE: Brabin, 1991.

with the onset of the reproductive years, when the changes in immune status that accompany pregnancy dramatically increase female susceptibility to malaria, notably falciparum malaria (McGregor, 1983). A recent study in Nigeria of the prevention and treatment of malaria among 45 pregnant adolescents (mean age, 17.5 years) and a control group of 47 nonpregnant girls of comparable ages found the incidence of malaria parasitemia, anemia, and fever episodes in the study group to be significantly higher (Okonofua et al., 1992). This vulnerability can be especially unfortunate in this early reproductive age group, whose members display low rates of utilization of hospital-level treatment services and health center antenatal care programs.

It is because of this heightened maternal susceptibility, as well as the threat malaria represents for fetal development and survival, that research emphasis on malaria in Sub-Saharan African females has concentrated on its effects on reproductive status, processes, and outcomes. This has provided a window to a better understanding of the functioning of the disease in general, as well as gender-specific understanding that is atypical of most tropical disease research. Nevertheless, questions around differential female burden rates in the nonreproductive years remain unanswered. Because of the behavior of the vector and its complex epidemiology, there is no immediately obvious explanation for these gender differences.

The risks of complications of malaria in pregnancy vary in individual women and appear to be dependent on two factors: parity and maternal immune status. Recrudescence of preexisting malarial infection, placental infection, and frequency of low birthweight infants are all more common in primigravidae than in multigravidae (Hendrickse, 1987), and rates of low birthweights brought about by malaria among primigravidae are particularly high, ranging from 9 to 40 percent (Brabin, 1985; see Tables 10-7 and 10-8). The marked effect of malaria in primiparous women is thought to be the result of "evasion" of host immunity by the parasite (McGregor, 1983) or depressed maternal immunity during the first pregnancy (Brabin, 1985; Oaks et al., 1991).

Of the two factors, it is immune function that appears to be pivotal in the evolution and impact of malaria during pregnancy, and in the higher parasite rates and densities in pregnant women in general. Because of the suppression of cellular immunity in pregnancy, latent malaria has the tendency to develop into acute, overt attacks in pregnant women, with more serious complications than is the case in nonpregnant women. Mortality from

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-8 Incidence of Malaria Infection among 570 African Women

Group

Number

Positive

Percentage

Mothers

Placentas

Neonates

579

570

569a

32

92

1

5.6

16.1

0.2

a One died one hour after birth.

SOURCE: Jelliffe, 1992.

TABLE 10-9 Weights of Female Neonates with Infected and Noninfected Placentas, by Birth Rank (in grams)

Birth Rank

Infected

Noninfected

Difference

1

2

3

4

5

6

2,497 (10)

2,869 (12)

3,074 (11)

2,790 (8)

2,978 (3)

2,721 (7)

2,843 (39)

2,933 (33)

3,039 (52)

3,142 (42)

3,061 (31)

3,210 (36)

345

64

35

352

83

489

NOTE: Values in parentheses represent the number of subjects in each group.

SOURCE: Jelliffe, 1992.

cerebral malaria during pregnancy has been estimated at 40 percent, and rates of hypoglycemia and pulmonary edema are as high or higher (White and Darrell, 1988). In a study of cellular immune responses to plasmodium falciparum antigens in adults in The Gambia, Riley and colleagues (1988) found women of reproductive age (18–45 years) to be less immunologically responsive than men in the same age group, a phenomenon attributed in other studies to suppression of lymphoproliferative responses to the falciparum antigen.

In sum, the nature of the involvement of pregnancy in immunosuppression related to malaria infection remains at the level of theory, and its pathophysiology is still puzzling. Results of studies of Plasmodium berghei immunity in pregnant mice (Van Zon et al., 1982) and the higher serum cortisol levels encountered in Tanzanian women with patent malaria infection during pregnancy (Vleugels et al., 1987) have suggested that loss of cell-mediated immunity during pregnancy might be cortisol-related. What is also puzzling is that massive malarial infection can be present in placental blood, even when only a few parasites can be found in the peripheral blood of the mother. The human placenta appears to offer a particularly suitable environment for malaria parasites (Bray and Anderson, 1979; Covell, 1950), with peak frequency and severity of parasitemia at between weeks 13 and 16 of gestation (Brabin, 1985) (see Table 10-9).

The widely held view among Sub-Saharan African women that is responsible for spontaneous abortions, stillbirths, and miscarriages, as well as many other health problems during pregnancy (Kaseje, et al., 1987), is correct. Several studies from Africa have found maternal malaria during pregnancy to be associated with low birthweight (Brabin, 1991; Jelliffe, 1992) and a recent set of hospital and community studies in central Sudan by Taha, Gray, and colleagues (Taha et al., 1993) found significant associations between a maternal history of malaria and low birthweight, a higher risk of low birthweight among primiparous women compared with multiparous

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

women, and increased risk of neonatal mortality associated with malaria during pregnancy. The study also suggests that maternal malaria significantly increases the risk of stillbirth, at least for infections during the first two trimesters. Because malaria treatment, chemoprophylaxis, and use of insecticides are known to decrease the risk of low birthweight, the study authors recommend them as appropriate interventions that should target primigravid women and be initiated early in pregnancy (Taha et al., 1993).

Malaria leads to low birthweight either by premature delivery or by impaired growth in utero, because it provides the opportunity for parasites (especially P. falciparum) to invade the fetus itself or to impair placental function (McGregor, 1983). Birthweights of female babies born to mothers with infected placentas tend to be significantly lower than birthweights of female babies of noninfected controls. Maternal hematocrits of less than 50 percent are known to be highly correlated with retardation of fetal growth (Harrison, 1976; Harrison and Ibeziako, 1973), and malaria heads a list of causes of anemia in pregnancy, which also includes iron and folate deficiencies, sickle-cell disease, and HIV/AIDS (Fleming, 1989). A likely scenario is that there are synergies among these conditions, as well as between each of them and other parasitic infections (such as schistosomiasis). Anemia in women of reproductive age in Sub-Saharan Africa tends to be multifactorial, reflecting interaction among different causal variables, including comorbidities, malnutrition and malabsorption, and depressed immunity.

Another element of interaction with malaria that could have special programmatic relevance is seasonality. Brain (1991) has observed seasonal variations in parasite rates in pregnant women, citing six studies from four African countries that reported higher parasite rates in the wet season than in the dry season (see Table 10-10). Her analysis is that since parasitemia persists through the dry season, primigravidas delivering in the late part of the wet season or the early part of the dry season would be at greatest risk for low birthweight, not only because they are primigravidae, but also because they have been, in effect, at risk for malaria throughout most of their pregnancy. Requirements for folate are higher in pregnancy, especially during the last trimester; when hemolysis from malaria stimulates erythroid hyperplasia, demand for folate mounts. When this demand is unmet, the result is the megaloblastic erythropoiesis that is seen in up to 75 percent of severely anemic pregnant women in West Africa.

TABLE 10-10 Parasite Rates in Pregnant Women in the Wet and Dry Seasons (percent)

 

Parasite Rate

   

Area

Wet

Dry

Comment

Number

Sierra Leone

38.7

22.2

First attendance

1,345

Nigeria (Zaire)

29.8

20.1

First attendance < 24 wks gestation

228

(Asexual forms)

19.2

9.7

(Gametocytes)

 

Nigeria (Ibadan)

10.2

8.6

Adego State Hospital and Osegor Health Centre (Placenta)

1,085

Gambia, The (rural)

27.6

26.4

Placental blood

3,500

Senegal

48.8

7.3

First attendance Urban Dakar

866

Senegal

24.1

8.8

Urban Thies (Blood)

444

 

7.2

5.2

(Placenta)

443

SOURCE: Brabin, 1991.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

Megaloblastic anemia is common at the end of the dry season and during the rainy season because of the heightened prevalence and severity of malaria and consequent iron and folate deficiencies (Fleming et al., 1968). Thus, it would appear that the principal morbidity deriving from malaria during pregnancy may not be from parasite densities per se, but rather from the combined effect of persistent parasitemia coupled with the iron and folate deficiencies that are common during the dry season. If this conclusion is correct, it has useful implications for program interventions.

There are interactions of malaria with other conditions that might also merit research attention. Malaria infection has been implicated in three disease syndromes common in Sub-Saharan Africa: Burkitt's lymphoma, quartan malarial nephrotic syndrome, and hyperreactive tropical malarious splenomegaly. There may be some gender-specific differences in the role of malaria in the etiology of Burkitt's lymphoma, a tumor that occurs in areas of Africa that are hyperendemic for P. falciparum, and is believed to be an atypical response to Epstein-Barr virus infection. An epidemiologic study in Uganda over the 10-year period between 1959 and 1968 showed median age of onset of lymphoma for both sexes to be under 8 years, but found higher incidence in females under age 5. This may simply be an artifact of differences in prevalence of malaria in the same population, because by the age of 15, the incidence of lymphoma had become higher in males than in females of the same age. Nonetheless, the association has been interesting enough to have evoked research activity that could throw some light on malaria pathology and epidemiology. Hints of some gender differentials in the experience of these syndromes also come from literature outside Africa: Brabin and Brabin (1988) found higher spleen rates in women than in men in Papua New Guinea, where moderate to severe cases of hyperreactive malarious splenomegaly have been reported. There is also some evidence that HIV infection may diminish female capacity, particularly in pregnancy, to control falciparum parasitemia, notably placental infection, with resulting poor fetal growth (Brabin and Brabin, 1992).

SCHISTOSOMIASIS (BILHARZIASIS)

Often referred to as ''blood flukes," worms of the genus Schistosoma comprise several blood parasites of humans and other animals, of which the three most important are S. hematobium, S. mansoni, and S. japonicum. Each has a slightly different pathway through the human body, and thus produces different patterns of morbidity and mortality. In the case of S. hematobium, the pathway is skin, to lungs, to bladder/ureters, with associated hematuria, dysuria, renal failure, and increased risk of cancer of the bladder. The final destination for S. japonicum and S. mansoni is the human liver, and the sequelae are hepatomegaly, splenomegaly, bleeding esophageal varices, and cor pulmonale.

The global area endemic for the three major human schistosomes includes 79 countries with an estimated total population of 3 billion, or approximately 90 percent of the estimated 1980 population of the developing countries (Mahmoud, 1984). Using a prevalence estimate of 21 percent (Iarotski and Davis, 1981), the population at risk in the endemic countries totals approximately 600 million. Current morbidity is estimated at 200 million individuals infected worldwide. Unlike other helminthic infections, which generate mild to severe disability, schistosomiasis produces a substantial burden of mortality, with over 200,000 deaths annually (CDC, 1993; WHO/TDR, 1991a; Walsh, 1990). S. mansoni is endemic in much of West and East Africa, overlapping throughout most of that area with S. hematobium, whose range extends further to the northeast and southwest. The distribution of both parasites encompasses the limited foci of another schistosome, S. intercalatum, in Central and West Africa (Warren et al., 1993).

Schistosomal infection and the patterns of its transmission in endemic communities are powerfully influenced by ecological factors. Thus, there can be considerable variation in disease prevalence and intensity over quite short distances, and the sizes of transmission foci can be quite small (Warren, 1973). The relatively limited sizes of transmission sites, their individual characteristics as habitats for the snail intermediate host, and their proximity to homesteads affect not only the distribution of disease, but also the magnitude of the role of gender in the acquisition and spread of infection. In addition, certain seasons encourage formation of new foci of transmission, and ecological change produced by human activity is a common cause of these new foci.

There are several factors that govern the outcome of the transmission process in endemic areas: a small proportion of snails are infected at any one time, they shed at specific times of the day, cercariae (the infective

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

stage of the parasite) are dispersed in huge bodies of water, and they have limited effective duration of infectivity. Human exposure, susceptibility, and resulting parasite densities respond in some degree to patterns of contact that fit those transmission characteristics (Mahmoud, 1984).

Prevalence and intensity of infection in areas where schistosomiasis is endemic show a characteristic relationship to age and sex (Chandiwana and Christensen, 1988). In most circumstances, both prevalence and intensity (measured by egg count) increase gradually to peak at approximately 10 to 19 years of age, with females in some endemic communities showing slightly less prevalence and intensity than males (Mahmoud, 1984). A cross-sectional study in Machakos, Kenya, identified the pattern of variation more precisely: peak prevalence (98 percent) was found in the age group 10–19 years, with a diminution to 70 percent in older cohorts, and highest egg densities (1,026 eggs/g) were identified in females ages 10–14 and in males ages 20–24 (1,019 eggs/g) (Arap Siongok et al., 1976). Prevalence decreases only moderately by the beginning of the third decade of life, but egg counts decrease dramatically, so that the diagnostic pattern alters with increasing age. Some researchers see this an evidence for accrued immunity, others see changes in patterns of water contact as an equally logical explanation.

The epidemiology and morbidity of schistosomal infection depend on several factors: timing and duration of water contact and exposure, penetration of cercariae, and nutritional status. Of these, it is water contact that heads the list of human activities that determine the intensity of schistosomal infection (Jordan, 1972; Okafor, 1990; Warren, 1973). Although water contact studies have been relatively few in number, and very few of those have disaggregated their data by gender, the studies that have been carried out have discerned clear patterns: infection rates vary by age and gender in ways that are directly related to water contact. Brabin and Brabin summarize the results of these studies in a recent review (1992) and find two distinct patterns: for males, activities requiring water contact taper off as they get older; for females, those requirements remain constant from early adolescence onward.

Schistosomiasis in Children

The burden of schistosomiasis begins early, because children born to and breastfed by S. haemotobium-infected mothers are already at risk of exposure to a circulating schistosome antigen (Camus et al., 1976; Mahmoud, 1984). Risk in communities endemic for S. mansoni is especially high. The presence of a thermostable parasite antigen —the "M" antigen—in the milk of mothers with S. mansoni infection and its possible transfer to nursing infants may mean that children born to mothers infected with S. mansoni will lose their capacity to respond to certain idiotype-induced regulatory stimuli, will be prone to develop hepatosplenic complications, and will be likely to have lower titers of anti-hepatitis B antigens after vaccination (Ghaffar et al., 1989; Santoro et al., 1977).

The role of protective immunity in the epidemiology of urinary schistosome infection is inconclusive (Warren, 1982; Wilkins et al., 1984), so that studies to examine tolerance or sensitization in uninfected children born to infected mothers could be important. Prenatal sensitization would seem to be especially important because it may modify hypersensitivity to both the worm and egg stages of the parasite, and that sensitivity will in turn determine the nature and extent of the morbidity produced by the infection (Warren, 1972).

The two main nutritional consequences of schistosomal infection for very young children are growth faltering and anemia, although other micronutrient deficiencies have been noted. Three channels lead from infection to growth faltering—anorexia, nutrient losses through malabsorption, and decreased nutrient use from impaired liver and spleen function.

Whatever the mechanism, a large and growing literature documents the substantial growth impairment from schistosomiasis (Warren et al., 1993). Given the young age at which the schistosomiasis burden begins to accrue, growth velocities are affected quickly and early. Studies in Kenya, Liberia, Nigeria, Tanzania, and Zimbabwe provide substantial case material to document a frank connection between S. haematobium infection and protein-energy malnutrition in children (cf. Burki et al., 1986).

Perhaps because gender roles are not yet as sharply delineated in childhood as they will be later in life, there is no clear picture of gender-related differences in prevalence and intensity of schistosomiasis infection in the early years. In two studies, prevalence was greater in males than in females (El Malatawy et al., 1992; Pugh and Gilles,

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

1976); in the latter, a study of urinary schistosomiasis, prevalence was four times greater in boys ages 5 to 15 than in girls of those same ages. Studies in Ethiopia also found prevalence declining with age and, again, peaking in the second decade of life, in this case between ages 10 and 14 (Teklehaimanot and Fletcher, 1990). Other studies in Ethiopia also reported increased susceptibility in young boys, adolescent girls, and women ages 15 to 34, and found a clear correlation with the amount of water contact (Hiatt, 1976; Polderman, 1974). Nonetheless, later studies in Mali and The Gambia found that infection rates in males and females were similar, despite apparent differences in exposure patterns (Brinkmann, et al., 1988; Wilkins et al., 1984).

To obscure the picture further, studies carried out in Nigeria found prevalence and intensity of S. haemotobium infection to be higher in females, with highest prevalence in the late teen years (Anya and Okafor, 1986). A more recent study in Zanzibar, which measured schistosome-related morbidity in children, found the highest incidences of uropathy and hematuria in girls between birth and age 4; boys had the lowest incidences at those same ages (Hatz et al., 1990). Limited data on seasonal variation in the prevalence and intensity of infection with S. haematobium among Gambian children under age 10 (Wilkins and Scott, 1978) suggest that seasonality might be a good place to look for more precise and consistent patterns of etiology.

Schistosomiasis and some other helminthic infections generate very high levels of morbidity in school-age children, but carry relatively low direct consequences for mortality. In the age group 5 to 14 years, the disease has been associated with growth retardation and decreased work capacity (Berkley and Jamison, 1991). Infected children often complain of abdominal pain and other manifestations of infection, including fever, weakness, lassitude, muscular pain, nausea, vomiting, diarrhea, and fatigue (Pollitt, 1990). Research on the effects of schistosomiasis on schooling is scant, but it is extremely likely that such school-related outcomes as academic achievement and school attendance are negatively influenced by schistosomiasis and that girls bear the most severe consequences (Levinger, 1992).

Similar factors—age of exposure, concurrent nutritional deficits, greater prevalence of malaria infection, and longer duration of schistosomal infection —are implicated in schistosomiasis-related morbidity in both school-age children and adolescents. In a study in Kenya, lack of reinfection in 30 percent of 119 school children one year after treatment was classified as resistance to reinfection rather than lack of exposure. Resistance to infection, the authors argued, was an acquired and age-dependent trait, not related to previous egg-induced pathology (Butterworth et al., 1985).

Schistosomiasis and the Adolescent Female

As indicated above, peak prevalence and intensity of urinary and intestinal schistosomiasis generally occur in adolescence—that is, during the second decade of life. By age 15, 37 percent of males and 53.1 percent of females in highly endemic areas in Nigeria (Anya and Okafor, 1986) had urinary schistosomiasis. Earlier observations in northwest Tanzania produced similar findings (Forsyth, 1969). Gender differences would appear to be role-related, since it is in adolescence that girls become more involved in the traditional female responsibilities of fetching water, washing clothing, and helping with agricultural tasks that combine to expose them to infective sites for longer periods than is the case for males.

Schistosomiasis also has severe effects on the female reproductive system, which become manifest in adolescence (see Table 10-11). Primary amenorrhea, delayed menarche, and other menstrual abnormalities have been attributed to ovarian schistosomiasis; later sequelae include risk of ectopic pregnancy, premature birth, and spontaneous abortion. The overall nutritional deficit has made anemia among adolescent females and younger girls of school-age a standard feature in Sub-Saharan Africa; the synergy of undernutrition and schistosoma-related hematuria in endemic communities might be expected to generate even higher rates of anemia, but there are no studies that have quantified these putative effects either by gender or age.

Schistosomiasis in Adult Females

Until the advent of ultrasound techniques, egg counts and hematuria and proteinuria detection were the only measures of schistosomiasis-related morbidity (Mott, 1982). A review of these measures by Tanner (1989)

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-11 Schistosomiasis and the Female Genital Tract

Organ

Findings

Symptoms, Sequelae

SH

SM

SI

Breast

Granulous, mimicking the mammographic pattern of carcinoma

None

+

0

0

Vulva (vestibule labia)

Ulceration with carcinomatous appearance; granulous, rapidly increasing in size

Irritation/pruritus, secondary infection, destruction of the external meatus

+++

+

0

Vagina, vaginal fornices

Polypoidal granulomas, papillomatous growth; vesico-vaginal fistulas

Fibrosis

+++

+

0

   

Incontinence

+

+

0

Cervix

Erosion, ulceration, polypoidal granuloma, papillomatous growth

Fibrosis; bloody discharge, dyspareunia, intermenstrual bleeding

+++

+

0

Uterus

Endometritis

Lower abdominal pain; menstrual irregularities, menorrhagia

+++

+

0

Fallopian tubes

Salpingitis, granulomas

Chronic backache, lower abdominal pain, dysmenorrhea, menstrual irregularities, sterility, ectopic pregnancy

+++

+

0

Ovaries

Oophoritis

Delayed menarche, primary menorrhea, menstrual irregularity, sterility

+++

+

0

NOTE: + = proven, but rare, +++ = proven, common, 0 = not proven or no data, SH = S. haematobium, SI = S. intercalortium, and SM = S. mansoni.

SOURCE: Feldmeier and Krantz, 1992.

concluded that while examination for hematuria is a reliable and sensitive morbidity indicator, egg count reliability is questionable because of the high day-to-day variability in egg excretion.

The most significant morbidity effects from schistosomal infection are urinary tract sequelae, including calcification in the lower tract, vesico-ureteric reflux, and hydronephrosis from S. hematobium. S. mansoni infection produces gastrointestinal sequelae, including large gastrointestinal granulomas, obstruction, ascites, esophageal varices, fibrosis, and portal hypertension.

Diagnosis of urinary tract pathology is particularly difficult because of several confounding factors in females: menstruation, since both hematuria and leukocyturia may be complicated by menstrual bleeding; pregnancy, since ultrasound detection may be confounded during that period; and ovarian changes at any point in the life span (Poggensee, 1992).

While schistosomiasis is debilitating for both adult males and females, the complications of chronic disease—including anemia, genital involvement, hepatosplenomegaly, and obstructive uropathy—affect women of reproductive age most severely. Several studies (McMeeley et al., 1988; Parker, 1992) note that, as in the case of malaria, pregnancy is a time of particular vulnerability both to schistosomal infection and the troublesome sequelae that derive from the disease; the condition is thus, by definition, one of high-risk. Pregnancy is, however, not the only time of risk: the ova of S. hematobium may migrate to the female genital tract at any time, and frequently do; potential sequelae are sterility; infertility; and, later in life, cancer.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

AFRICAN TRYPANOSOMIASIS

An estimated 25,000 new cases of African trypanosomiasis occur each year, there are an estimated 20,000 trypanosomiasis-related deaths annually, and approximately 50 million individuals in 36 Sub-Saharan African countries are at risk of infection (WHO/TDR, 1991a). Of the six major parasitic diseases, it is the only one that is exclusive to Sub-Saharan Africa, and its range on that continent is confined to a third of the Sub-Saharan belt, with some patchy distribution in eastern, east-central, and western Africa.

African trypanosomiasis is caused by two morphologically identical subspecies of Trypanosoma brucei, which are transmitted by the tsetse fly Glossina. The first is T. brucei gambiense, the classic African sleeping sickness. It has a gradual course, sometimes lasting for years before onset of the typical sleeping sickness syndrome preceding its terminal phase, and occurs largely in the western, west-central, and northern regions of Sub-Saharan Africa. The second is T. brucei rhodesiense, which has an acute and rapid clinical course, typically ends in cardiac failure as the cause of death, and occurs mainly in eastern and southern Africa. Cattle and other mammals are important reservoir hosts for these diseases, as well as being vulnerable themselves to a third trypanosome, T. brucei brucei; cattle mortality from T. brucei brucei has important consequences for local economies and human nutrition (Hajduk, et al., 1984).

While each disease form manifests differently, in general the early stage of the disease, when the trypanosomes are in the human peripheral blood system, is either asymptomatic or characterized by vague symptoms of malaise, lassitude, and irregular fevers. These are classically followed by a range of symptoms including headache, anemia, sensory disturbances, nausea, disturbed circadian rhythms, joint pains, and swollen tissues. Symptoms become progressively worse as the parasite passes into the central nervous system (CNS) (much more quickly in the case of Rhodesian trypanosomiasis) and precipitates the late-stage of immune suppression, cardiac involvement, general deterioration, coma, and death (Buyst, 1977; WHO/TDR, 1991a).

Early treatment of trypanosomiasis, before there is CNS invasion and before epidemic situations can develop, is crucial (WHO, 1979). Yet males, females, and entire communities are affected by difficulties in diagnosis that are peculiar to the disease, whose variable and unspecific symptoms are easily confused with the fever, headache, and general body and joint pains typical of malaria. Currently available diagnostic tools are insufficiently sensitive and primary health care personnel are not trained for even reasonably reliable diagnosis of presumptive symptoms. The effectiveness of vector management programs has been limited by the wide distribution of the flies, the presence of animal reservoirs, the underground habitat of their pupal stages, and uneven success in motivating adequate levels of community participation (Hajduk et al., 1984). Prospects for a vaccine seem remote, and research has been focused on understanding the causes of disease pathology, vector control measures, and therapies that are effective and free from the high toxicity and teratogenicity of currently available treatments (WHO/TDR, 1991a). FDA approval in 1990 of a new trypanocidal drug, eflornithine (trade name, Ornidyl), will be very helpful in treating late-stage gambiense infections, but it must be administered intravenously in hospital and its cost (US$140 per adult dose) is high, even though its producer, Marion Merrell Dow, has been providing the drug for several years at lower than production costs and will eventually donate all patient rights, licensing agreements, and the like to WHO (WHO/TDR, 1991b). Beyond eflornithine, the most promising intervention so far appears to be development of new diagnostics with high specificity and sensitivity (WHO/TDR, 1991a).

As in the case of so many tropical infectious diseases, exposure to the infective vectors of African trypanosomiasis is closely related to individual and community behavior, notably the work patterns of males and females and the different age groups (Robertson, 1963). Duration of exposure to tsetse fly bites is a major contributory factor to infection for individuals of any age and either gender. Thus, the division of family labor that is performed in fly-dense areas becomes pivotal.

African Trypanosomiasis in Children

The greatest overall burden of African trypanosomiasis, as measured in DALYs, is borne by individuals of both sexes between the ages of 5 and 44. The highest rates of mortality occur in the cohort aged 5–14, and are

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

somewhat lower between ages 15 and 29; the cohort with the highest rates of disability is between the ages 15 and 44 (Murray and Lopez, 1994). Transition from asymptomatic status—that is, change from early stage, peripheral-blood-system involvement to late-stage CNS invasion —can occur in early childhood (Brabin and Brabin, 1992), although the mechanism precipitating transition remains obscure (WHO/TDR, 1991a). Preschool children who experience transition and survive may be severely disabled, sometimes severely mentally retarded. Good information on the epidemiology of these different sequelae is nonexistent.

Similarly, the epidemiologic picture of prevalence of the African trypanosomiases by sex is extremely unclear, partly because of the wide divergences between results from parasitological and serological studies, and partly because of the mysteries around transition from asymptomatic status. For example, in areas of endemic rhodesiense sleeping sickness where prevalence is high (for example, The Gambia and southeast Uganda), males have been reported to be at greater risk than females (Mulligan and Potts, 1970; Robertson, 1963; Scott, 1970). Yet in a study in northeast Zambia, where a higher proportion (66.7 percent) of all children under 10 had rhodesiense trypanosomes in their cerebrospinal fluid compared with older subjects (39.2 percent), females under age 10 displayed higher infection rates than boys of the same ages (Boatin et al., 1986). And again, in a study in Zaire based on parasitologically diagnosed cases of gambiense sleeping sickness, infection rates were found to be higher in females under age 10 than in boys of the same ages (Henry et al., 1982).

African Trypanosomiasis in Adolescent and Adult Females

Under the kinds of epidemic conditions that have prevailed in the past—for instance, in Zaire and several other countries of the region between 1920 and 1981—both male and female adults are, theoretically, et equal risk of infection (Morris, 1960; Robertson and Baker, 1958). Under "nonepidemic" conditions, risk of infection derives primarily from regular patterns of exposure and sex differences in those exposures, most significantly involvement in farm work. Until relatively recently, the theory has been that since males bore the greatest responsibility for on-farm labor, their exposure and infection rates would be considerably greater than those of the female members of the family, whose role was seen as largely confined to the home site. That contention now seems inaccurate or, at best, not widely applicable.

First of all, the epidemiologic data do not support this view. Although the distribution of the burden of African trypanosomiasis does not differ dramatically when aggregated for all ages for each sex (899,000 DALYs for males, compared with 883,000 for females), the burden of trypanosomiasis in females between ages 15 and 44 is higher than it is for males (see Table 10-2). Individual studies would seem to corroborate these aggregate data. Household surveys in Zaire (Henry et al., 1982) and Côte d'Ivoire (Felgner et al., 1981) show higher rates of trypanosomiasis in females under age 30 than in males of the same ages. Of 3,500 Ivoiriens studied, higher percentages of females than males tested positive for T. gambiense infection in almost all age groups, with women ages 20–29 having the highest infection rate. And, in the 1964 epidemic in Central Nyanza, Kenya, while both sexes were equally infected, peak prevalence was found in women aged 20 through 29 (Willett, 1965). That same female cohort has been implicated in other studies, including two predicated on serological surveys, one in the Congo (Frezil, 1981) and another in Nigeria (Edeghere et al., 1989). In a recent review, Brabin and Brabin (1992) suggest that the observed sex differences in these cohorts are attributable either to increased susceptibility to disease in women of reproductive age or to loss of asymptomatic status during pregnancy.

Patterns of historical change are also highly explanatory. Data from a study of rural women's economic roles in Kenya, collected between 1974 and 1976 (Smock, 1979); from time allocation studies in Burkina Faso and Zaire (Carael and Stanbury, 1983; McSweeney, 1979); and from a 1984 review by the Food and Agriculture Organization (FAO) all concluded that it is adolescent and adult females, rather than males of those ages, who are the greatest contributors to agricultural production. As Chapter 2 explained, the introduction of cash-crop farming in central and southern Africa led to the recruitment of men from rural areas for work on large plantations and in the mines; other waves of males have flowed out of rural areas in more recent decades in search of white- and blue-collar job opportunities in urban areas. Thus, large populations of adult males have been cumulatively removed from the tsetse fly belt, leaving women with the major responsibility for subsistence farming and family welfare, and exposure of adult females to the infective bites of the Glossina vectors of T. brucei gambiense and T.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

TABLE 10-12 Typical Workday for Zambian Women during the Planting Season

Task

Percentage of Time Spent

Waking Hours

Walking to the field with baby on back

30 min

3.2

Plowing, planting, hoeing

9 hrs, 30 mins

59.4

Collecting firewood and carrying it home

1 hr

6.2

Pounding or grinding grain or legumes

1 hr, 30 mins

9.4

Fetching water

45 mins

4.7

Lighting fire and cooking meal for family

1 hr

6.2

Serving food, eating

1 hr

6.2

Washing children, self, clothes

45 mins

4.7

Total

16 hrs

100.0

NOTE: Percentage of workday spent outdoors away from the family compound is 71.9.

SOURCE: Modified from Sadic, 1995.

rhodesiense increased strikingly, particularly during the planting period, which coincides with the rainy season when rates of tsetse fly infectivity peak. Females of all age groups were also left with their traditional responsibilities for water and fuelwood collection (UN/ECA, 1974) (see Table 10-12), leading to even greater exposure in areas of high fly density.

Unfortunately, these historical changes are not reflected in numbers of trypanosomiasis cases reported at the hospital-level, where women do not appear to present for treatment in numbers commensurate with presumed morbidity rates. The theory has been advanced that this stems from the cultural requirement that women seek medical help only with a husband's permission and only when clinical signs and symptoms are obvious and severe. Because at least some males are absent, as noted above, this theory is open to question.

African Trypanosomiasis and Pregnancy

Like malaria, African trypanosomiasis has special impact on women during pregnancy. First, and perhaps most important, there appears to be generalized immunosuppression in women already suffering from trypanosomiasis, and loss of asymptomatic status during pregnancy. Even when infected females remain asymptomatic for longer periods than men during infancy and adolescence, pregnancy appears to reverse this gender-related advantage (Goodwin et al., 1972). In pregnancy, infection with T. gambiense can convert from its typically slow course, become acute, and lead to spontaneous abortion, stillbirth (Duboz, 1984), greater maternal morbidity, and possibly mortality. Data on the speed and timing of this process, as well as the factors that precipitate it, do not exist.

The other possibility is that the infection will not convert and will remain subclinical, with subsequent intrauterine transmission of the infection to the fetus, which will not manifest until later in the infant's lifetime (Olowe, 1975). One case report, by Woodruff and colleagues (1982), underscores the implications of this slower, occult course of the disease: a "healthy carrier" mother, asymptomatic for over three years following infection in an area endemic for gambiense trypanosomiasis, gave birth and remained asymptomatic for yet another 39 months, at which time her child was found to have been infected in utero. Rhodesiense trypanosomiasis can also be

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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congenitally transmitted (Boatin et al., 1986; Brabin and Brabin, 1992; Henry et al., 1982; Lowenthal, 1971; Morris, 1960; Robertson and Baker, 1958; Traub et al., 1978; Willett, 1965).

While such cases are not uncommon, we do not know how common they are, nor do we understand the mechanism of transplacental transmission in either type of trypanosomiasis. Given the high prevalence of the disease in women ages 20–29, and given the sequelae of the disease for both mother and child, further research would seem to be merited. Brabin and Brabin (1992) comment on the direction such research should take: "To concentrate attention on classification of cases is likely to obscure the public health significance of asymptomatically infected mothers, who give birth to apparently normal babies in whom neurological sequelae and illness may not develop until the second year of life."

TRACHOMA

Trachoma is a chlamydial infection that occurs epidemically in many developing areas. The current annual toll of trachoma worldwide is 500 million cases, which include 6 to 8 million individuals in whom it has caused blindness (CDC, 1993). Although the disease is not fatal, it generates a huge burden of disability and ranks fourth among all the tropical infectious diseases included in the GBD calculations. The total burden of DALYs from trachoma in Sub-Saharan Africa for both sexes of all ages was 901,000 in 1990; still, that burden is half the 1.8 million DALY burden produced by the third-ranked disease, African trypanosomiasis.

The ubiquitous etiologic agent of trachoma is Chlamydia, a genus of nonmotile, gram-negative, small coccoid bacterial parasite that causes infection in birds, humans, and other mammals. Chlamydia trachomatis includes human pathogens and is separated into three biovars on the basis of their behavior in laboratory animals and in cell culture: trachoma, lymphogranuloma venereum (LGV), and one mouse pneumonitis strain.

Trachoma is not one of the WHO/TDR priority diseases, perhaps because its incidence and severity have decreased greatly over recent decades in areas with improving hygienic conditions and living standards. Although there are still pockets of the disease somewhere on virtually every continent, its main foci are in North and Sub-Saharan Africa and the Middle East, where its presence was first recorded in 1500 B.C., and where it is still the major cause of preventable blindness. The C. trachomatis biovar in these areas causes trachoma, inclusion conjunctivitis, and eye infection and respiratory infection (pneumonitis) in the newborn. Clinical trachoma is rare in Europe and North America, where the C. trachomatis biovar is, instead, the most common cause of sexually transmitted disease, with highest incidence in young adults during the period of maximum sexual activity (Grayston and Kuo, 1984). This sexually transmitted form of the biovar is also present in much of the developing world, including Africa, where it is the cause of several acute diseases (urethritis, cervicitis, salpingitis), pregnancy-associated conditions (ophthalmia and pneumonia in the newborn; postpartum endometritis in the mother), and chronic conditions (infertility, ectopic pregnancy) (Germain et al., 1992).

In endemic areas, trachoma is a chronic, familiar disease perpetuated by eye-to-eye transmission. Overcrowding, close family grouping, inadequate water supply, and low standards of hygiene increase frequency of reinfection and enhance severity. Under these conditions, where a "pool" of infection is established and maintained, the disease usually runs a course of recurrence and remission, with repeated scarring and deformation of the conjunctiva, which may eventuate in blindness. Chronic or latent infections occur frequently, immunity produced in the host is usually incomplete and short-lived, and drug administration may fail to eradicate the infecting agent, so that prolonged antimicrobial therapy with a long period of patient observation is desirable. Because of the high-risk of familial and community reinfection, the best course is simultaneous antibiotic treatment of all active cases in household units, and even entire communities (Grayston and Kuo, 1984; Taylor et al., 1989).

Trachoma in Children

In trachoma-endemic areas, the highest rate of active infection is found among children under 10 years of age. The disease is perpetuated in the family by infection of susceptible young children, so that almost all the older children and adults in the family will almost inevitably reacquire active disease because of their exposure to the

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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younger children. There are no data on differential rates of infection by gender (and, indeed, there is no reason to suspect any at this early age).

The disease can also be contracted during delivery through the birth canal of a mother with C. trachomatis genital infection. Again, there would seem to be no reason to suspect that either sex of newborn would be at differential risk in this mode of transmission. There is, however, some variation in site of infection in newborns infected in the birth process. While the primary infection site for both male and female newborns is ocular, there may also be some vulvovaginitis in baby girls. This seems to subside after an acute phase, although there seem to be no data from Africa on whether this infective manifestation has any further sequelae of significance. There are some clues, nonetheless, that might justify further inquiry. Episodes of inclusion conjunctivitis after infancy are transmitted by autotransfer or heterotransfer of genitourinary material to the eye, and the sequelae of transmission can be either ocular or genitourinary.

Infants are also at risk of C. trachomatis pneumonia, a distinctive respiratory syndrome in infants less than 6 months of age that is acquired from the infected cervix of its mother during delivery. Eyes and nasopharynx are the initial colonization sites, and diagnosis is aided by a positive maternal history of sexually transmitted disease, as well as by isolation cultures (Grayston and Kuo, 1984).

Trachoma in Adolescent and Adult Females

For both males and females, by far the greatest burden of disability from trachoma occurs between ages 15 and 44—that is, their most economically productive years and the reproductive years of females (Murray and Lopez, 1994). This is not in itself surprising, since the principal disabilities caused by the disease are progressive. Although the disease is initially acquired in early childhood, deteriorated vision, disfigurement, and, ultimately, blindness do not occur until the adult years, after a cumulative process of reexposure, repeated infection, scarring, and distortion of the upper eyelid. While the accumulation of scars can be halted with appropriate interventions, changes that have already taken place cannot be reversed (Taylor et al., 1989).

The special relevance of trachoma to this volume is the stunningly large burden of the disease it produces in Sub-Saharan African women. In 1990, that burden amounted to 690,000 DALYs, over three times the burden of 210,000 DALYs produced by trachoma in males. It is somewhat surprising that this large gender differentiation appears to have been noted only relatively recently (cf. Congdon et al., 1993). The range of sequelae produced by trachoma, from cosmetic disfigurement to total blindness, are highly likely to have more severe implications for females than for males: that is, exclusion from marriage possibilities, social isolation, dependency, neglect, or any or all of these events.

In addition, the pattern of transmission for the disease is such that adult females who care for young children in domestic environments are at distinctively high-risk. A meticulous study in Tanzania provides evidence that close physical contact with preschool children, especially preschool children with trachoma, is associated with an increased odds ratio for active trachoma in women and may also be associated with development of chronic sequelae (Congdon et al., 1993). The researchers raise the question of whether the mothers were the source of infection for their children, rather than the converse, but since other epidemiologic data suggest that preschool children are the reservoir of active trachoma in village environments, and men have much lower rates of active disease, the conclusion is that women are the recipients of infection within the family, not its source. These data underscore the need for intervention strategies that interrupt transmission at the household level and programs of antibiotic therapy that are aimed both at children and their caretakers.

DRACUNCULIASIS (GUINEA WORM)

Dracunculiasis is a helminthic infection caused by the nematode parasite Dracunculus medinensis. A communicable disease, it is acquired solely through ingestion of water contaminated with tiny crustaceans called copepods, or "water fleas," that act as intermediate hosts of the organism and harbor infective larvae. When the ingested copepods are killed by the digestive juices in the stomach, the larvae are released and move to the small intestine. They penetrate the intestinal wall and migrate to the connective tissues of the thorax, where male and female larvae

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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mature and mate 60 to 90 days after infection. Over the next year, female worms grow to maturity, reach a length of 2 to 3 feet, and slowly migrate to the surface of the body, where they form burrows in subcutaneous tissues. When they reach maturity, a blister is formed, which eventually ruptures, exposing the worm. Shortly before the skin lesion forms, pronounced systemic symptoms may occur, including intense itching and pain, nausea, vomiting, diarrhea, and dizziness. Worms emerge from the lower extremities in about 90 percent of cases, but can also appear in the upper extremities, trunk, buttocks, genitalia, or other parts of the body (Ruiz-Tiben et al., 1995).

Dracunculiasis is endemic in areas of severe poverty in India, Africa, and the Middle East. Its transmission is limited to periurban and rural communities lacking any form of public drinking water supply, and where water for household use is consequently drawn from artificial ponds and bodies of stagnant water (Muller, 1984). About 120 million people are at risk of dracunculiasis in 17 African countries; in 1986, there were an estimated 3.32 million cases of the disease in the Sub-Saharan region (Hopkins, 1987).

Guinea worm infection is seldom fatal, but it is typically debilitating, often frankly crippling for long periods, and complications are common. As the worm emerges through the skin lesion, the affected person pulls it out slowly and carefully, usually by winding a few centimeters each day on a stick, a very painful process that may last many weeks (Ruiz-Tiben et al., 1995). In about 50 percent of cases, there is secondary bacterial infection of the worm track, which also provides entry for tetanus spores and possible process to mortality (Muller, 1984). In addition, over the time it takes for an entire worm to be expelled, numerous ulcers may be formed, some of which may become chronic. Other possible chronic sequelae include fibrous ankylosis of joints, tendon contraction, arthritis, and synovitis. In addition, since each worm is the result of a separate infection event and immunity does not seem to be acquired, each year may bring dracunculiasis reinfection, for which there is no cure.

Infected individuals are also carriers: when they wade or bathe, the immature forms of the worms they carry enter the water source to continue the cycle. It is also the case that some proportion of a population at risk will never become infected; one explanation is that high gastric acidity, which kills the larvae when they reach the stomach, confers protection in such individuals (Muller, 1984).

Dracunculiasis in Children and Adolescents

The picture of age and sex differences in Guinea worm infection, like every other tropical disease, is spotty. Information about the disease in infancy is slight, except for published epidemiologic surveys that show dracunculiasis infection to be rare in the first year of life. The average 12-month incubation period of the disease means that any infection acquired during the neonatal period is unlikely to become patent until after the first year of life (Kale, 1977).

There is some limited information concerning Guinea worm infection in children under age 5. In a recent survey of 501 households (n = 6,527 persons) in Nigeria, incidence of dracunculiasis was higher in girls under age 5 (12.8 percent) and between ages 5 and 15 (32 percent) than it was among boys in those same cohorts (6.5 percent and 25.9 percent, respectively). In contrast, rates in males over age 15 were higher than in females at the same age (Ilegbodu et al., 1991).

The impact of dracunculiasis on school-age children has been demonstrated in a number of studies in Nigeria, and elevated absenteeism and drop-out rates have been reported among infected children (Edungbola, 1983; Edungbola and Watts, 1984; Ivoke, 1990; Nwosu et al., 1982), but the data are not disaggregated by gender. These appear to be the only studies that take adolescents as a group specifically into account.

Generally there is a high correlation between rates of school absenteeism and infection (Edungbola, 1983; Nwosu et al., 1982). Ivoke (1990) examined monthly variations in absenteeism among 617 children in 14 primary schools in Nigeria's Imo State, and encountered the highest rate of absenteeism (35 percent) in March, the peak month for farming activities; 17 pupils missed the promotion examinations in November because they were incapacitated by dracunculiasis. Ilegbodu and colleagues (1986) studied the impact of Guinea worm disease on 727 school-age children in southwestern Nigeria and found that infected children were absent from school for about 25 percent of schooldays, and noninfected children were absent only 2.5 percent of schooldays, while almost 6 percent of children dropped out of school because of dracunculiasis. (See Figure 10-1).

For girls, an unknown proportion of this absenteeism may also be attributable to their mothers' disability

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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FIGURE 10-1 Absenteeism caused by dracunculiasis-induced incapacitation in 14 primary schools in Imo State, Nigeria.

SOURCE: Ivoke, 1990.

rather than their own, and the resulting need to stay at home to take care of domestic responsibilities. The disability inflicted by the disease on adult women requires them to depend on family members and friends for help with their customary responsibilities, typically on another woman, generally a relative or neighbor. If there is an adolescent female in the family, it is often she who must take on household chores and childcare; this means either that she must abandon her schooling or enter the informal sector of the labor force to support the family financially (Ivoke, 1990; Nwosu et al., 1982).

Dracunculiasis in Adult Females

The highest rates of Guinea worm infection occur in adults between ages 15 and 45 (Belcher et al., 1975). In an exhaustive review, Muller (1971) found infection rates for males and females in most surveys to be approximately the same, suggesting comparable exposures for both sexes. In a study in Imo State, Nigeria, in four of six communities studied (n = 6,539), infection rates were similar for both sexes; in the remaining two communities, prevalence rates were higher in males (26.5 percent) than in females (15 percent) (Ivoke, 1990).

The importance of dracunculiasis resides not in mortality rates, but in the prolonged disability it produces in infected men and women and its consequences for the individual, family, and community. Three factors influence the degree of disability: worm burden, location of the lesions produced by the infection, and the nature of clinical complications.

Duration of disability varies widely and depends on age, the site of the lesion, initial degree of disability, and treatment effectiveness. According to several studies, average duration of incapacitation for effective work is between 90 and 100 days; the mean is three months, but disability sometimes extends for as long as 30 weeks (Kale, 1977; Smith et al., 1989). Although a number of studies report differences in prevalence rates by sex, none compares duration of disability by gender.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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Epidemiologic surveys conclude that gender differences in Guinea worm infection are primarily dependent on exposure to infection foci; that is, the quantity of infected water consumed during the peak period of transmission, which invariably coincides with peak agricultural activity (Kale, 1985) and/or with the secondary rainy season (Petit et al., 1988). Because dracunculiasis-endemic villages tend to be farming communities, and peaks of agricultural demand coincide with the peak periods of disease transmission, in effect, whole villages can become disabled. In such cases, there are few alternative labor sources to replace ailing agricultural workers, and there is a marked reduction in agricultural output; the socioeconomic consequences can be severe (Ivoke, 1990; Kale, 1985; UNICEF, 1987). In southern Ghana, average work loss in untreated adults with Guinea worm disease was over five weeks (Belcher et al., 1975). According to a UNICEF report (1987), dracunculiasis was responsible for significant reductions in person-days of rice production in four Nigerian states. Another study in Nigeria, utilizing interviews with 20 male and female farmers incapacitated by infection, found a total income loss for the group of 25,590 Naira (approximately US$1,163.18) because of their inability to plant their crops (Brieger and Guyer, 1990). Disability in this group lasted from one to seven months, and all crops were affected. In a study in Burkina Faso, agricultural loss attributable to dracunculiasis was estimated at an equivalent of 8 percent of all annual grain imports to the country (Guiguemde et al., 1984).

None of these studies disaggregates findings by gender. For the most part, epidemiologic research on Guinea worm disease has addressed its prevalence in the general population and in the agricultural labor force as a whole, so that its economic impact on women in particular is largely a matter of hypothesis.

Guinea worm infection of the pelvis affects both men and women but, at least in West Africa, is more common in women, for whom it has obstetric and gynecologic implications (Scott, 1960). St. George (1975) reported bleeding during pregnancy caused by retroplacental worm location, as well as a pattern of repeated spontaneous abortions of uncertain etiology in a very short time period, a pattern terminated successfully by worm removal.

The debilitation produced by Guinea worm infection makes itself felt across much of the female life span. The best documentation of its serial effects to date comes from a 1988 study in Nigeria sponsored by the Water and Sanitation for Health (WASH) Project. A total of 42 mothers of children 24 months of age and younger were interviewed, using focus group and in-depth techniques, and mothers' morbidity histories were analyzed through four variables—self-care functions, childcare duties, domestic activities, and economic pursuits (USAID, 1988).

According to the report, over one-quarter of the sample had experienced an episode of Guinea worm at some point during their most recent pregnancy; 76.9 percent of this subgroup reported that pain from Guinea worm had worsened during the pregnancy itself, and 13.5 percent had experienced a worm attack during the postnatal period. The entire sample reported anorexia and consequent reduction in food intake; arrested breastfeeding because of fever and pain; and inability to care for themselves or their new babies. Brieger and colleagues (1989a,b) observed that disability from dracunculiasis had been responsible for 50 percent of child immunization defaults in two Nigerian communities and had also kept women from making adequate use of antenatal services and engaging in regular trading activities. Incapacitation was so severe in some cases that women ate and drank sparingly simply to avoid the need to go outside to defecate (Watts et al., 1989).

In another Nigerian site (Idere), 21.3 percent of mothers interviewed had developed dracunculiasis during their last pregnancy or since the most recent birth. Average number of sick weeks for the total sample was 6.1, 96.9 percent had worms in their legs, and 45 percent had secondary infections that had produced further incapacitation (Brieger et al., 1989b). Of the 53 mothers who experienced the disease during pregnancy, over two-thirds had been unable to continue with family care and domestic chores.

Dracunculiasis has especially severe implications for female-headed households. These women report being unable to work and earn money to send children to school, and in cases where they are the principal agricultural laborers, their exposure is the same as similarly employed males, but their vulnerability as the sole providers of family income is considerably greater.

Prospects for eliminating this burden of disease from the lives of Sub-Saharan African women are more promising than for any other tropical infectious disease. Dracunculiasis has been the subject of a global eradication campaign initiated at the U.S. Centers for Disease Control in 1980 in connection with the beginning of the International Drinking Water Supply and Sanitation Decade (1981–1990). The eradication effort was first endorsed by the World Health Assembly (WHA) in 1986; in 1991, the WHA officially set the global target of

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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TABLE 10-13 Changes in the Status of Dracunculiasis Eradication, 1990–1994

Dracunculiasis Cases Reported, 1990a

Dracunculiasis Cases Reported, 1994b

Country

Number of Cases

Country

Number of Cases

Nigeria

Ghana

Burkina Faso

Benin

Mauritania

India

Togo

Cameroon

Pakistan

Chad

Côte d'Ivoire

Ethiopia

Kenya

Mali

Niger

Senegal

Sudan

Uganda

Yemen

394,082

117,034

42,187

37,414

8,036

4,798

3,042

742

160

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

N.A.

Sudan

Nigeria

Niger

Uganda

Ghana

Burkina Faso

Mali

Togo

Mauritania

Côte d'Ivoire

Benin

Ethiopia

Chad

India

Senegal

Yemen

Kenya

Cameroon

Pakistan

53,092

39,774

23,568

10,409

8,432

6,859

5,396

5,045

5,029

4,700

3,440

1,252

640

371

186

74

37

30

0

NOTE: N.A. = No information available at this time.

a Cases reported to the World Health Organization from countries completing national case searches or from active village-based surveillance.

b Provisional data reported to the World Health Organization from countries completing national case searches or from active village-based surveillance. Sudan's report to WHO includes cases reported by the Passive Surveillance System.

SOURCE: Ruiz-Tiben et al., 1995.

achieving eradication by the end of 1995—a target that African ministers of health in almost all the dracunculiasis-endemic countries had already set for themselves as of 1988 (Hopkins and Ruiz-Tiben, 1990).

Guinea worm is eradicable for several reasons. There is no human carrier beyond the one-year incubation period and there is no known animal reservoir, detection of patient infections is easy, transmission is markedly seasonal, control methods are simple, and the disease is well recognized by local populations in endemic areas (Ruiz-Tiben et al., 1995). The simple, economical procedure of filtering drinking water through a cloth to remove the crustacean intermediate host seems to be a culturally acceptable and effective control intervention in many endemic areas, and is the method of choice for controlling this helminthiasis until enclosed water supplies are available. Provision of such supplies, combined with health education, has been shown to eradicate the disease within three years (Edungbola et al., 1988; Edungbola and Watts, 1990).

Table 10-13 displays the changes in the status of dracunculiasis eradication in Africa between 1990 and 1994. It is clear that progress has been significant, but success has been mixed. Two major challenges remain. The first is to complete implementation of the case-containment strategy and other control interventions, such as insecticide use, in villages of all affected countries. The second is to mobilize greater public support in those countries; the initiative still has to deal with lack of public and political awareness and inadequate funding (CDC, 1993), as well as the characteristic difficulties of changing human behavior.

The countries that pose the greatest eradication challenge are Sudan, Niger, and Nigeria. One Nigerian study reported that over two decades of health education activities concerning communicable diseases, disseminated through the satellite facility of the University of Ibadan Medical School, had made little or no difference in the behavior of residents of Idere village, only 5 kilometers from the university. Lack of response in this instance was

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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attributed to a belief that the disease was in the blood of the members of this particular village, sent by God, and unique to them (Ilegbodu et al., 1991). Success appears to be associated with instances where villagers have come to appreciate the link between Guinea worm infection and the water supply and have responded with such village-based preventive measures as well-digging (Edungbola and Watts, 1990). Yet even countries with the fewest cases will require markedly tighter control measures to completely interrupt dracunculiasis transmission by the end of 1995. This will depend, in turn, on the continued support of national and international entities (Ruiz-Tiben et al., 1995).

ONCHOCERCIASIS AND LYMPHATIC FILARIASIS

Both onchocerciasis and lymphatic filariasis result from infection by parasitic nematode worms of the family filariidae. Four species are of particular importance: Onchocerca volvulus, which causes onchocerciasis and is transmitted by Simulium blackflies; and Wucheria bancrofti, Brugia malayi, and Brucheria timori, all responsible for lymphatic filariasis transmitted by various species of mosquito. Infection with W. bancrofti leads to the most severe form of lymphatic filariasis, affecting breasts, genitalia, and all limbs; it can also induce tropical pulmonary eosinophilia. There are two subspecies of O. volvulus, identical under the microscope but with different vectors and ecological niches, one of which causes savanna onchocerciasis, the other forest onchocerciasis. Its Simulium vector breeds on objects in freely flowing streams and rivers, thus the name ''river blindness."

The different types of filariasis are rarely life-threatening in themselves, but all cause chronic suffering and disability. Lymphatic filariasis can lead to hugely swollen limbs (a condition known as elephantiasis), produced an estimated 90 million cases in 1991, and currently affects 76 countries with a total of 905 million people at risk. Onchocerciasis is one of the four leading causes of blindness worldwide, and it produced an estimated 17.6 million cases of disease, including 326,000 people blinded; it currently affects 34 countries, with 90 million people at risk. Over 95 percent of all the world's cases of onchocerciasis are found in the Sub-Saharan region, most in equatorial Africa.

Onchocerciasis begins with inoculation of infective larvae into the human skin by the blackfly bite. The larvae develop into adult worms over several months, and then coil into subcutaneous nodules containing males and females, which subsequently mate. Gravid females release large numbers of microfilariae, which migrate out of the nodule and throughout human host tissues. Transmission of infection to other individuals is initiated by the bite of a female fly, which ingests microfilariae from the host skin along with a blood meal. The pathology of onchocerciasis is manifested primarily in the skin, lymph nodes, and eyes, leading to intense itching and disfiguring dermatitis, and damage to the eyes, including blindness.

Over 60 percent of the W. bancrofti parasites originate—in ever-increasing numbers as the cities of the developing world swell in size—in the pools of stagnant, polluted water common in poor urban areas, ideal breeding sites for the parasite's vector, the female Culex quinquefasciatus mosquito. The bite of the vector releases infective larvae into the human body. Once matured, the adult worms make their home in the lymphatic system, in some sites for many years. The resulting systemic damage causes buildup of lymph fluid in the limbs, with subsequent edema and the painful and disfiguring swelling of the limbs typical of late-stage disease (Greene, 1984; WHO/TDR, 1991a).

Onchocerciasis in Sub-Saharan Africa produces a much larger burden in DALYs than does lymphatic filariasis: a total of 641,000 DALYs from onchocerciasis as of 1990, compared with 184,000 from lymphatic filariasis. In both instances, males bear the largest burdens compared with females; in the case of lymphatic filariasis, the burden of DALYs for males of all ages totals 132,000, compared with 51,000 for females; in the case of onchocerciasis, the DALY burden for males is 370,000; for females, 272,000. Because of the substantial difference in burden for the two diseases in Sub-Saharan Africa, this discussion will focus largely on onchocerciasis.

There are important differences in the epidemiology of onchocerciasis that warrant attention before proceeding further. The frequency of the various sequelae of the disease varies not only according to duration and intensity of exposure, as might be expected, but by geographic location. For the same degree of filarial and microfilarial load, the savanna form of the disease causes at least three times more blindness than the forest form (WHO/TDR, 1991a), and, while blinding onchocerciasis occurs in over 10 percent of the population in savanna

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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areas (Remme et al., 1989), it is quite rare in rainforest zones. Nevertheless, males and females in rainforest areas suffer from severe and irreversible skin lesions, including pronounced atrophy and depigmentation (Anderson et al., 1974; Greene, 1984); the manifestations are both less frequent and less severe in many instances in savanna zones, and prevalence is much lower (McMahon et al., 1988).

The reasons for the differences in the transmission, clinical patterns, and severity of the disease between the two zones have a complex and not clearly understood etiology. This is partly the result of the distinct nature of both parasite and vector populations in each zone (Anderson and Fulsang, 1977; Duke et al., 1966; Lobos and Weiss, 1985). In addition, intensity of antiparasite reactions in victims is quite various, almost individualized; this suggests considerable complexity in host-parasite interactions in filarial infections (Ottesen, 1984), perhaps attributable to differences in host immune responses (Anderson and Fulsang, 1977; Remme et al., 1989). Finally, because onchocerciasis occurs in foci that are determined by the relation of the population to Simulium breeding sites, levels of endemicity vary according to distance from larval and pupal habitats; hyperendemic areas are those closest to a given focus (Greene, 1984).

Onchocerciasis in Children

The epidemiology of O. volvulus infection indicates that prevalence is age-specific, rising progressively after the first few years of life to almost 100 percent by the age of 30 to 40 years in hyperendemic areas (Anderson et al., 1974). Prevalence of both ocular and dermal onchocerciasis also rises steadily, to almost 100 percent by the fifth decade of life.

Still, prevalence rates may be misleading, and microfilarial density is now considered a better measure. The risk of ocular complications actually relates more closely to intensity of infection than it does to prevalence. Risk of transmission in any area is determined by the number of fly bites and the proportion of flies harboring infective larvae (Greene, 1984). Even though the adult worms of O. volvulus do not multiply in the human host, with repeated exposure and reinfection in hyperendemic areas, human adult worm burdens and microfilaria counts mount over the years (Brabin and Brabin, 1992; Greene, 1984), and there is no persuasive evidence for development of protective immunity with age.

Because onchocerciasis is a cumulative disease, morbidity in early childhood is typically limited to mild systemic effects from early infections, such as slight pruritus. Although congenital infection has been reported from early studies in Ghana (Brinkmann et al., 1976), we found no subsequent studies that address this subject specifically. As for gender differences, where onchocerciasis is hyperendemic, microfilarial densities in females are lower than they are in males beginning in early childhood; in hypoendemic areas, densities are similar for both sexes (Brabin and Brabin, 1992).

Effects on older children can be substantial. In a study of 2,876 persons in Taraba River Valley, Nigeria, the effects of eye lesions on visual acuity were assessed using the "tumbling E" method. The striking result from this study was that, in children under age 10, particularly those with head nodules, serious and irreversible eye lesions were already present and visual acuity was significantly affected (Akogun, 1992). No differences were reported by gender.

Onchocerciasis in Adolescents

In general, males are 1.5 times as likely to be blind as females of the same age with the same level of microfilariae, and greater frequency of onchocercal eye lesions, particularly lesions of the posterior segment of the eye, is reported for males (Ottesen, 1984). Yet the Taraba River Valley study cited above reported that all forms of visual impairment increased with age in a similar fashion for both males and females, and in a study in the Onchocerciasis Control Programme area, the only significant differences in ocular lesions were found in individuals with lesions of the posterior segment of the eye, a condition more typical of male symptomatology (Remme et al., 1989). Given the present state of knowledge, the hypothesis must be that any gender-specific differences in symptomatology and microfilarial densities derive from differences in exposure rather than from any inherent sex differences (Brabin, 1990).

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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At the same time, the social consequences of the skin lesions produced by onchocerciasis can be particularly significant, if not devastating, for girls as they enter marriageable age in cultures where marriage and children are the source of identity and self-esteem. Browne (1960) observed that while blindness may be of greater clinical and economic importance than chronic lesions, the implications of lesions are far from negligible. Recent studies in forest areas of Nigeria show that cosmetic impairment from severe onchocercal dermatitis stigmatizes adolescent girls and affects their life chances (Amazigo, 1994). Girls of marriageable age with severe skin lesions are usually avoided and will not be viewed as eligible until there is evidence of at least partial cure. While young males and females with severe lesions may both feel the effects of stigma, girls with cosmetically disfiguring lesions attempt to conceal them and tend to withdraw from social activities in the community and at school (Amazigo and Obikeze, 1991).

Onchocerciasis in Adult Females

The skin lesions produced by O. volvulus may begin as early as age 5, and continue to be produced into adulthood; after age 40, the number of exposed persons with different forms of onchocercal lesions is significantly higher than those who will eventually become blind. The most acute onchocercal lesions are marked hypo- and hyperpigmentation, skin atrophy, and excoriation, alone or in combination. Pruritus, caused by dead filariae left under the skin after invasion by the live parasite, commonly produces incessant scratching, acute papular skin eruptions, and great discomfort. After prolonged infection and the lesions of fibrosis, irreversible atrophy, pigmentary changes, and extreme scarring of dermal tissue, there is little or no potential for clinical improvement with even the most effective filaricidal treatment (Duke, 1990). It is rare that the pruritus from onchocerciasis has no sequelae: a study of 452 individuals in western Ethiopia found onchocercal dermatitis of the typical maculo-papular type, often with excoriation, in 54 percent of 150 persons clinically examined, a percentage corresponding exactly to the proportion of individuals complaining of pruritus (Woodruff et al., 1977).

The spectrum of the clinicopathological features of the dermatologic sequelae of O. volvulus has been studied for some time (cf. Cannon et al., 1970; Connor et al., 1983; Edungbola et al., 1983; Gibson and Connor, 1978; Shafi-Mohammed, 1931). While acute lesions may be more prevalent in males (Edungbola et al., 1983), this may be a function of the unwillingness of females to present themselves in a clinical setting with an acute lesion. There do appear to be pathologies that are particular to females, such as the hanging pouch of lymphadenomatous skin produced by advanced dermatitis that is often seen in women (Connor and Palmieri, 1985).

The systemic effects of onchocerciasis can also produce substantial morbidity in women, as measured by parasitological diagnostic techniques that use shallow skin biopsy samples to take microfilarial counts. In a study of subjective complaints and measurable morbidity, Burnham (1990) found that of 5,653 subjects examined in Malawi, 57 percent of those with positive skin snips complained of itching, a frequency of subjective complaints from persons with positive skin snips was significantly higher than in subjects with negative skin snips, and reports of dizziness, backache, joint and generalized body aches and pains, pruritus, and poor vision that corresponded to higher microfilarial counts. Women with onchocerciasis-caused blindness weighed 6.8 kilograms less than normally sighted women, and bilateral blindness was correlated with an 11 percent decrease in body mass. Even women who were sighted but had positive skin snips weighed 1.6 kg less than those with negative skin snips. All correlations were statistically significant. A very few other studies report on symptoms that are generally found in females. In an early study in Tanzania, Gabuthuler and Gabuthuler (1947) implicated onchocerciasis as a cause of muscular abscesses in women.

Onchocerciasis also affects reproductive processes. An observation in Nigeria indicates that in pregnant women infected with the disease, there is severe and rapid exacerbation of skin lesions with increased gestational age, as well as deterioration of papular and pustular eruptions by 24 weeks of gestation (Amazigo, 1994). This may be the result of hormonal changes or immunosuppression. More generally, morbidity in women of reproductive age from hypergic onchocerciasis may also have something to do with lack of immune tolerance and onchocercal lymphadenopathy. Rainforest onchocerciasis may have especially adverse consequences for women's reproductive health, and studies in Tanzania, Mali, and Nigeria report that women in those zones do hold onchocerciasis responsible for a number of reproductive health problems, including infertility, sterility, abortion,

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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and stillbirth (Brieger et al., 1987; Gabuthuler and Gabuthuler, 1947; Hielscher and Sommerfeld, 1985). To date, none of these subject areas has received research attention.

Finally, onchocerciasis may have direct health effects that go beyond the immediate victim. In a preliminary study to explore the effects of onchocercal pruritus on breastfeeding, 73 percent of 75 women with positive microfilariae in skin biopsies experienced itching and other associated morbidity that were linked with early weaning of infants by 26 percent of the positive sample (Amazigo, 1994).

The relationship between onchocerciasis and mortality is not clear. Measured in DALYs, the burden of estimated mortality from the disease is much smaller than its burden of morbidity. For males of all ages in Sub-Saharan Africa, estimated deaths account for 17,300 DALYs, but years lived with a disability (YLD) amount to 108,000. For females, those figures are 12,400 and 74,000, respectively (Murray and Lopez, 1994).

Clinical analysis would also suggest a relatively modest direct connection between the disease and mortality. Some heavily infected individuals show wasting and generalized weakness, with loss of adipose tissue and muscle mass, and such persons may be at increased risk of other infections, such as tuberculosis. Although microfilariae have been found in most major internal organs at autopsy, there is no convincing evidence that significant organ dysfunction occurs as a result of widespread infestation (Greene, 1984). An additional puzzle is that, while excess mortality is found among males with high microfilarial loads, it is not seen among females with comparable loads (Brabin and Brabin, 1992).

The relationship among general disease pathology, mortality, and the blindness that is the most severe complication of the savanna form of onchocerciasis is also unclear. Using weight/height as an index of nutritional status, Kirkwood and colleagues (1983) found that the nutritional status of blind or visually impaired subjects was lower than that of subjects with normal vision; that mortality was three to four times higher among blind onchocerciasis sufferers than among those with no visual damage; and that onchocerciasis-related mortality was, overall, most meaningfully correlated with microfilarial load. Prost and Vaugelade (1981) suggest that increased mortality among the blind is indirect, and is primarily attributable to high accident rates or to social and economic conditions resulting from blindness, rather than to any systemic effects of the disability. Studies of the burden of blindness in adult populations in Burkina Faso have determined that the average life span after the onset of blindness is between seven and nine years (Prost and Paris, 1983); absent additional data on age of all subjects, it is difficult to interpret the meaning of this information.

Reported prevalence of blindness in a given village at any one time may misrepresent the true magnitude of the burden that onchocercal blindness places on the population at large, especially in the productive age group (Prost, 1986). According to Prost's study, in hyperendemic villages with an annual incidence of blindness of 5.7 percent, the real probability was that more than 46 percent of the males in those villages who were age 15 at the time of the study would become blind in adulthood. Although the proportion of females between ages 20 and 40 with some visual impairment was higher at the time of the study, a smaller proportion—35 percent—would proceed to blindness. The study provides no further information on blindness in women or its impact on them, nor does any other that the authors of this chapter have been able to identify.

LEISHMANIASIS AND LEPROSY

Four of the six major tropical diseases that produce visible disfigurement have already been discussed in this chapter: schistosomiasis, dracunculiasis, onchocerciasis, and lymphatic filariasis. Two remain: leprosy and leishmaniasis.

Epidemiological data on these diseases are generally recognized as poor, primarily because of their low case-fatality rates. Leishmaniasis is not among the reportable diseases in many countries, and the World Health Organization has estimated that two-thirds of the leprosy cases in the world are still unregistered (Htoon et al., 1993).

The best estimates are that 350 million individuals in 80 countries are considered at risk of leishmaniasis, with 12 million individuals infected and 400,000 new cases yearly (WHO, 1990). Even in countries where leishmaniasis is reportable, the actual number of cases is estimated to be three to five times higher, because the disease typically occurs in remote areas where people live within zoonotic foci and in poor countries where other health problems

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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are of higher priority (WHO/TDR, 1991a). Leishmaniasis ranks sixth in DALY burden in Sub-Saharan Africa, following not far behind onchocerciasis. The DALY burden for all Sub-Saharan African males in 1990 was 291,000; for all females it was 292,000. The burden in all cohorts for both sexes is virtually the same, with the greatest weight borne by individuals in the cohort ages 5–14, followed at some distance by the older cohorts, ages 15–44 (Murray and Lopez, 1994). The mortality component of the burden is relatively small, since just one of its three forms—the visceral form known in Africa as kala-azar—can proceed to fatality (CDC, 1993). It is the visceral form that is most prevalent in Africa (Sudan, Kenya, Uganda, Ethiopia, Central African Republic, Chad, Gabon, The Gambia, and Somalia) (Wyler and Marsden, 1984). In some countries of the region (Ethiopia, Kenya), epidemics of visceral leishmaniasis have been responsible for tens of thousands of deaths, because the disease is usually lethal if untreated (WHO/TDR, 1991a).

As for leprosy, the number of officially registered cases was 3.7 million in 1990, plus an estimated 2 million additional undetected, partially disabled patients. Ninety-three countries were affected, with a prevalence of at least one per 10,000 population. There were 2.46 million people living in leprosy-endemic countries, defined as those having a prevalence rate of at least one per 10,000 population (WHO/TDR, 1991a). It is estimated that 250,000 of those with leprosy are blind, a figure that is greater if visual acuity is less strictly defined (Htoon et al., 1993). Leprosy ranks seventh in DALYs, well behind leishmaniasis and, again, the burdens for males and females are almost the same (Murray and Lopez, 1994).

While the two diseases are similar in producing equivalent burdens of disability in both males and females, the number of registered cases of leprosy began a noteworthy decline in 1985, perhaps because of the implementation of multidrug therapy and the consequent release of large numbers of patients from treatment (Htoon et al., 1993). This advance might now be slowed, if not halted, as resistance of leprosy bacilli to chemotherapeutic drugs increases (CDC, 1993).

In contrast, there is no reason to expect diminution in the overall prevalence of leishmaniasis unless an effective vaccine is developed (Wyler and Marsden, 1984; WHO/TDR, 1991a). Controlling transmission of the disease is complicated by a number of powerful epidemiological and ecological factors. The parasite can be transmitted by over 50 species of its sandfly vector, whose breeding and resting sites are diverse and widespread, and the life cycles of the various leishmanias also involve a variety of zoonotic reservoirs. The disease also flourishes under the sorts of environmental transformations that accompany certain kinds of socioeconomic and demographic change, including large-scale migrations of nonimmune individuals into leishmania-endemic regions. An additional element of complexity is that both malaria and kala-azar coexist in similar geographic areas; they may present similar symptoms, be diagnostically confused at a certain stage, and may also interact and complicate each other (Cox, 1987; Kaendi, 1992; Southgate, 1981).

Unlike malaria, which is relatively even-handed in the distribution of its burden across all age groups, the heaviest burden of leishmaniasis in Sub-Saharan Africa falls upon children ages 5–14, followed at some distance by the burden on the late teenage and adult years, from ages 15 to 44 (Murray and Lopez, 1994). Until recently, leishmaniasis was thought to affect males more than females, at least in part because of occupational demands—for instance, herding and work in forest environments. The sandfly vector has been found to be peridomestic as well, however, which obviously changes the gender equation (Mutinga, 1984; Wyler and Marsden, 1984). A reasonable hypothesis is that there is no immediately obvious reason why, overall, male and female exposures should not be comparable. There is reason to expect some difference in the male and female experience, which would derive from heightened vulnerability of pregnant females to the sequelae of malaria and consequent or preexisting anemia. Any of these could produce synergy in susceptibility to visceral leishmaniasis or to more intense and threatening episodes of the disease, although this is highly speculative. What is not speculative is that the scarring from the lesions of cutaneous leishmaniasis will be disfiguring, always more of a liability for females than it is for males.

Disfigurement is also a historical and well-understood sequela of leprosy. Until now, both the prevalence and incidence of leprosy in endemic countries has generally been understood to be higher in males than in females. That higher occurrence has been attributed to the greater mobility of males and their increased opportunity for exposure and contact with infectious cases. It may also be a product of the failure to detect disease in females because of social attitudes, which result in less thorough examination of females by health workers (Htoon et al.,

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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1993; Ulrich et al., 1992). To what extent this traditional pattern prevails today is unclear, but the GBD analysis would indicate some change.

Again, there is differential experience of the disease by gender. Because of maternal immunosuppression during pregnancy, disease in a leprous mother may become overt, relapse if previously cured, or deteriorate during pregnancy and puerperium. Especially during pregnancy and lactation, there is increased likelihood of development of erythema nodosum leprosum (ENL), a painful immune complex disease. There may also be reversal reaction during lactation, with additional progressive nerve damage and corresponding sensory and motor loss. The babies of infected mothers tend to have smaller placentae, lower birth weights and slower growth rates, increased susceptibility to infection, and higher mortality in the first year of life than offspring of healthy mothers. These sequelae are all most marked in mothers with the most severe form of the disease, lepromatous leprosy (Duncan, 1992), which is characterized by heavy bacillary load, greater infectivity, tendency to relapse even after prolonged drug treatment, and marked host cellular immunodeficiency, considered the main reason for progression of the disease into this form (Harboe, 1984).

Recent studies have raised more questions about the interactions of leprosy and the reproductive processes than they have answered. All of these suggest directions for further fundamental and operational research, particularly in development of a vaccine and therapeutic drugs, prevention and treatment of disability, aspects of case management, and education at the household and community levels (Htoon et al., 1993).

CONCLUSIONS

It is clear that the tropical infectious diseases are closely associated with deprivation: with poverty; isolation, and powerlessness; with lack of clean water, sanitation, and effective vector control; and with unavailability of adequate preventive and curative medical response. It is also clear that vulnerability to infection is closely associated with exposure and, in turn, the socioeconomic and cultural factors that shape the timing, duration, and intensity of that exposure. It is less clear that there are genetic and biological factors that influence susceptibility and physiological response to parasitic infection by age, sex, and individual.

In addition, there is no period in the female life cycle where these diseases do not threaten—episodically, because of the additional risk they impose on pregnancy and childbearing, or because of the cumulative burdens they generate across the life span. These effects are displayed in Table 10-14.

The very best way of dealing with these diseases would be to eradicate them, so that they threatened no one, or to control them so they threatened far fewer. Thus, the list of research needs that follows deliberately excludes concepts of eradication or control; these are considered gender-free goods, to be desired and sought for all affected groups, males and females of all ages. Vector control is an essential element for all these diseases, although more feasible and cost-effective for some than for others. Other strategies include: for malaria, reduction of breeding sites, bednets and curtains impregnated with synthetic pyrethroids and use of soap containing pyrethrin, use of repellents, and chemoprophylaxis where this is not problematic; for dracunculiasis, provision of safe water and treatment of secondary infection; for onchocerciasis, mass treatment with ivermectin and use of repellents; and for trypanosomiasis, avoidance of infection loci and eflornithine treatment. Because of the extent of their exposure and their pivotal role in the household and community, Sub-Saharan African women will be crucial in the success of any efforts to conceptualize and carry out activities that contribute to eradication and control; any such effort that excludes them should be considered benighted.

That said, there are some generic statements that can be made about the parasitic infections in the context of female health and well-being. First, despite the tendency to view these infections as episodic, the burden they produce is one of enormous and persistent disability. Furthermore, these diseases act synergistically with one another and with other, nonparasitic diseases, and produce more severe disability and, in some cases, mortality where it might not otherwise occur.

Second, the epidemiologic burden of these diseases, once seen to be especially heavy for males, appears to have shifted, and it is now to be more equitably distributed between the sexes. Migration and changes in distribution of labor by geography and gender appear to lead the list of factors contributing to this shift. Documenting this conclusion will require solid longitudinal data.

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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The third conclusion has to do with the traditional biomedical perspective that the only interesting distinctions between male and female susceptibility to the tropical infectious diseases lie in their relationship with female reproductive function. For that reason, where there has been any biomedical research on sex differences in manifestations of disease, it has focused on that relationship, principally in terms of pregnancy and pregnancy outcomes, placental transmission, and maternally induced protection in the neonate. This approach has excluded understanding of nonreproductive effects and limited gender-relevant research to the diseases that produce these effects. It is true that science must often proceed narrowly to achieve depth of understanding, and this sort of research—for instance, malariological research—has provided insights into the workings of all parasitic diseases that have great value. It is time to broaden that focus.

Fourth, there is another, environmental perspective that produces its own biases. While it is certain that differential exposure is a dominant factor in infection, there are tantalizing clues in research on nonparasitic infections that they may be genetic and sex-specific differences in response to infection that may not be linked to reproductive function per se. Such findings as the sex differences in the incidence of uropathy and hematuria in children between birth and age 4 are provocative; their meaning and the possibility of other such differences in additional tropical infectious diseases are unknown and could be relevant to understanding of those diseases. In addition, research on cross-sex transmission of measles raises some profound questions about the existence of genetic, physiologic, or morphologic traits associated with sex that either exacerbate or attenuate diseases in males and females. This raises questions about basic mechanisms at the cellular level and about the relative biological strength of the sexes that might have consequences for research on sex and on infection, and ultimately lead to improved control of severe and potentially fatal infections in general.

Finally, there are what might be called "nonbiological" effects of these diseases that must be taken into account in research. While there is growing knowledge about the impact of the parasitic diseases in general on the abilities to learn in school and to produce in the world of work, there is little knowledge about other effects of those diseases. For example, their ability to produce physical disfigurement is appalling. This chapter has suggested that such disfigurement is particularly difficult for females, especially females of marriageable age for whom it has large social, and even economic, implications. In societies where marriage and children are crucial to societal worth, the absence of those can be crushing, yet there are indications that young females conceal or do not report signs and symptoms of such diseases as urinary schistosomiasis or leprosy for fear of losing those options, apprehension about more general stigma, and shame. We do not know this in a quantified way, but it would be possible to find out, in zones of high endemicity, what proportion of reported cases were timely and what proportion of cases identified in the population at large had not been reported at all. It may be that in the cases of diseases for which there are effective therapies, earlier reporting might obviate the disfigurement and stigma women want so desperately to avoid. It is true that control and eradication of these diseases are desirable enough in themselves; it might also be true that until these goals are realized, more investment in methods of palliating the physical and social pain they produce would be well placed.

RESEARCH NEEDS

  • As in virtually every other chapter in this report, this review of tropical infectious diseases in Sub-Saharan African females argues for the need for consistent longitudinal data on the incidence and prevalence of those diseases by sex. These data are not only necessary to knowing what the larger trends are, but are central to keeping track of their processes in populations and individual human beings. Where these data have been collected, they are inevitably gathered among both males and females so that, for the most part, the challenge is at the level of analyzing or reanalyzing data that already exist. Nevertheless, there is now enough evidence of significant variation between the effects of these diseases in males and in females across the life span that all future data-gathering and analysis should account for both sex and age in their design and analysis.

  • Human immunodeficiency virus (HIV) infection appears to diminish a woman's capacity, particularly in pregnancy, to control falciparum parasitemia; placental infection, with subsequent severe impact on fetal growth, seems to worsen in the presence of HIV, but the mechanisms of these effects, not only in the case of malaria but in connection with other tropical infectious diseases, have not commanded research interest. This is understandable

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
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TABLE 10-14 Ages of Occurrence of Tropical Infectious Diseases and their Adverse Health Effects in Sub-Saharan African Females

In Utero

Infancy/ Early Childhood (birth through age 4)

Childhood (ages 5–14)

Adolescence (ages 15–19)

Adulthood (ages 20–44)

Postmenopause (age 45+)

Malaria (fetal wastage)

Malaria (low birthweight, birth defects)

Malaria (anemia, cerebral malaria)

Malaria (severe anemia, pulmonary edema, splenomegaly)

Malaria severe anemia, pulmonary edema, splenomegaly)

 

Schistosomiasis (fetal wastage)

 

Schistosomiasis (anemia, weight loss, lower genital tract disease

Schistosomiasis (delayed menarche, spontaneous abortions, liver cirrhosis, disfigurement)

Schistosomiasis (infertility, cerebral edema in pregnancy, liver cirrhosis, disfigurement)

Schistosomiasis (chronic backache, cancer of genital tract/bladder/liver, disfigurement)

     

Dracunculiasis (disfigurement)

Dracunculiasis (disfigurement, chronic arthritis)

Dracunculiasis (disfigurement, chronic arthritis)

   

Onchocerciasis (severe pruritus, sleep loss)

Onchocerciasis (deterioration of lesions in pregnancy, disfigurement)

Onchocerciasis (blindness, disfigurement)

Onchocerciasis (blindness, disfigurement)

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

Trypanosomiasis (fetal wastage)

Trypanosomiasis (low birthweight)

Trypanosomiasis (loss of asymptomatic status, mental retardation, anemia, myocardial involvement)

Trypanosomiasis (loss of asymptomatic status)

Trypanosomiasis (loss of asymptomatic status, organic dementia, anemia, myocardial involvement)

Trypanosomiasis (loss of asymptomatic status, organic dementia, myocardial involvement)

 

Trachoma (pneumonitis, neonatal vulvovaginitis, inclusion disease) conjunctivitis, ophthalmia

Trachoma (maximum active disease)

Trachoma (repeated infections)

Trachoma (scarring, disfigurement, blindness)

Trachoma (scarring, disfigurement, blindness)

   

Leishmaniasis (high rate of acquisition)

Leishmaniasis (high rate of acquisition)

Leishmaniasis (severe disfigurement)

Leishmaniasis (severe disfigurement)

Leprosy (impaired placental function, low birth weight)

Leprosy (poor growth, increased susceptibility to infection)

 

Leprosy (loss of asymptomatic status, reactivation/ nerve damage in pregnancy)

Leprosy (reactivation/relapse/ nerve damage in pregnancy, blindness, nerve damage, disfigurement)

Leprosy (blindness, nerve damage, disfigurement)

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

because of the justifiable urgency of understanding the HIV infections in themselves. Research into the effects of co-infection and comorbidity with all the tropical infectious diseases, however, might provide illumination on disease mechanisms that could be helpful. If there is no reason to think this is the case, then it would perhaps be a misguided investment of increasingly scarce funds for biomedical research, but the question should at least be raised.

  • Work in parasitic diseases, notably malaria, schistosomiasis, and dracunculiasis, reflects differences between Western biomedical and indigenous concepts in perceptions of the meaning and management of the tropical infectious diseases. These differences must be highly relevant to the proper design of health education and preventive interventions, but the findings from that work and experience with their applications remain largely unanalyzed, and certainly undisseminated. A thoughtful synthesis of this work, including material from unpublished documentation, would not be overly costly, and could be very useful. Lessons that have application beyond a particular disease or setting have special value.

  • Early treatment of trypanosomiasis, before there is central nervous system involvement and before epidemic situations can develop, is crucial. Yet males, females, and entire communities are affected by difficulties in diagnosis that are peculiar to the disease, which has symptoms that are easily confused with those of other diseases, including the fever, headache, and general joint pains typical of malaria. Similar confusion seems to prevail in connection with leishmaniasis (kala-azar), which also can complicate cases of malaria. All three diseases interact deleteriously with pregnancy and anemia. The testing capability required for accurate diagnosis of most tropical diseases is not available at the primary care levels typical of most rural environments. Furthermore, primary health care personnel have inadequate training for making even reasonably reliable diagnoses of presumptive symptoms, although creation of such capability is within the realm of possibility. A workable scoring system using signs and symptoms for diagnosis by rural health workers was developed as part of a study in northeast Zambia and could be adapted for use elsewhere, but to our knowledge, this has not been replicated. The analysis that could promote its replication is a research need.

  • The size of the burden of trachoma on Sub-Saharan African females —close to twice that in males when calculated in Disability-Adjusted Life Years (DALYs)—was one of the surprises that emerged during the preparation of this report. While the DALY calculations are constrained by the data base beneath them, the size of the total burden and the size of the differential would seem to be too great to be wrong in a relative sense. The hypothesis is that females, as primary child caretakers, are most exposed to the pool of domestic infection. This sounds reasonable, but search for additional support for that hypothesis and consideration of its public health and educational implications would be a worthy focus of research.

  • The role of shame or fear of losing marriage changes in late reporting or nonreporting of tropical infectious diseases for which there are early stage remedies seems important. There are other factors in the delay in health-seeking and in compliance with therapeutic regimens. All these delay factors, including the usual factors such as distance, cost, and availability of time for health-seeking, can be important in effective treatment. For example, the progression of damage from onchocerciasis may not be reversible, but it can be halted, so that early recognition and reporting are crucial. At present, the information about the behavioral aspects of individual and household management of cases of tropical infection are known largely at the level of ethnographic anecdote, and "vertically" by disease. Compilation of what is known about how younger and older females manage their experience of the tropical infectious diseases, as a basis for integrating that knowledge into case management and public education, could be very useful. The role of Sub-Saharan African women's groups at different levels—for example, university and community—in compiling this information and developing public health interventions could be pivotal.

  • Dracunculiasis is one of the diseases in the world that has the potential for actual eradication in the near future, and its target year is approaching. Any investment in new applied research or analysis and synthesis of existing research that would hasten the successful attainment of that goal should receive priority research investment. Again, this is not necessarily costly, but it is urgent.

  • Differential physiologic manifestations of disease by sex and age, and the analysis of earlier research on cross-sex transmission, raise questions about the possibility of genetic, physiologic, or morphologic traits associated with sex that either exacerbate or attenuate diseases in males and females, as well as about the relative biological strength of the sexes. Pursuit of answers to such questions might lead to fuller understanding of basic

Suggested Citation:"10 Tropical Infectious Diseases." Institute of Medicine. 1996. In Her Lifetime: Female Morbidity and Mortality in Sub-Saharan Africa. Washington, DC: The National Academies Press. doi: 10.17226/5112.
×

mechanisms at the cellular level and, ultimately, to improved control of severe and potentially fatal infections in general.

  • Life span analysis makes it clear that there are significant differences over time and by gender in the biology and behavioral management of the tropical diseases in Sub-Saharan Africa. This suggests that most research should have some dimensions that are integrated and interdisciplinary. From scientists at the bench, who now can work with epidemiological and clinical findings that suggest illuminating differences between the sexes at a very fundamental level, to the conceptualizers of public health interventions, who must educate populations who experience a number of these diseases over a lifetime, ongoing integrated and interdisciplinary ''cross-referencing" to one another's learning will be essential for a long time to come. The guidelines for all research in tropical medicine can only profit from a gender approach in which women are involved, as persons with more than biological needs and as primary providers of health within the African family and society.

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The relative lack of information on determinants of disease, disability, and death at major stages of a woman's lifespan and the excess morbidity and premature mortality that this engenders has important adverse social and economic ramifications, not only for Sub-Saharan Africa, but also for other regions of the world as well. Women bear much of the weight of world production in both traditional and modern industries. In Sub-Saharan Africa, for example, women contribute approximately 60 to 80 percent of agricultural labor. Worldwide, it is estimated that women are the sole supporters in 18 to 30 percent of all families, and that their financial contribution in the remainder of families is substantial and often crucial.

This book provides a solid documentary base that can be used to develop an agenda to guide research and health policy formulation on female health—both for Sub-Saharan Africa and for other regions of the developing world. This book could also help facilitate ongoing, collaboration between African researchers on women's health and their U.S. colleagues. Chapters cover such topics as demographics, nutritional status, obstetric morbidity and mortality, mental health problems, and sexually transmitted diseases, including HIV.

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