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,



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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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,

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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.

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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.

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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.

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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.

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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.

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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)

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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)

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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

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IN HER LIFETIME: Female Morbidity and Mortality in Sub-Saharan Africa 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. 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