Below is the uncorrected machine-read text of this chapter, intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text of each book. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.
7 Energy Requirements, Energy Intake, and Associated Weight Gain During Pregnancy Optimal maternal and fetal outcomes of pregnancy are contingent upon nutrient intakes sufficient to meet maternal and fetal requirements. Energy is the major nutrient determinant of gestational weight gain, although specific nutrient deficiencies may restrict that gain. Clinical and public health interventions designed to improve gestational weight gain may be directed at energy intake or expenditure (see Figures 2-2 and 2-3 in Chapter 2~. Effective dietary intervention, however, requires an understanding of the energy requirements of pregnancy and the relationship between energy intake and gestational weight gain. The subcommittee reviewed energy intakes in the context of gestational weight gain, the effectiveness of energy supplementation on weight gain, and net energy balance during pregnancy. Extra energy is required during pregnancy for the growth and main- tenance of the fetus, placenta, and maternal tissues. Basal metabolism increases because of the increased mass of metabolically active tissues; maternal cardiovascular, renal, and respiratory work; and tissue synthesis. Energy requirements are greatest between 10 and 30 weeks of gestation, when relatively large quantities of maternal fat normally are deposited. Substantial fetal demands (56 kcal/kg per day) are offset in the last quarter of pregnancy by the near cessation of maternal fat storage (Sparks et al., 1980~. Hytten (1980) estimated the energy cost of pregnancy to be 85,000 kcal, or 300 kcaVday, based on theoretical calculations that assumed a 3.4-kg infant, deposition of 0.9 kg (2.0 lb) of protein and 3.8 kg (8.4 lb) of fat, and an increase in basal metabolism ('Ibble 7-1~. No allowance was made for the increased energy cost of moving a heavier maternal body 137
138 NUTRITIONAL STATUS AND WEIGHT GAIN TABLE 7-1 Theoretical Cumulative Energy Cost of Pregnancy and Its Componentsa Energy Cost, kcal/day (Mean Daily Increments of Protein and Fat, g/day) by Period of Gestation, wk Component () 10 1~20 2~30 30~0 Cumulative . Total, kcal (g) 5,186 (925) Protein deposition 3.6 (0.64) b Fat deposition 55.6 (5.85) Increase in basal 44.8 metabolism Total net energy 104.0 Additional energy 114.0 required from food (total net energy + 10%) 10.3 (1.84) 26.7 (4.76) 34.2 (6.1) 235.6 (24.80) 207.6 (21.85) 31.3 (3.3) 36,329 (3,825) 99.0 148.2 227.2 35,717 344.9 382.5 379.0 421.0 292.7 77,234 322.0 84,957 a From Hytten (1980), with permission from Blackwell Scientific Publications, Inc. b Heat of combustion defined as 5.6 kcal/g for protein and 9.5 kcal/g for fat. mass; it was assumed that this expenditure was compensated by a reduction in physical activity. The validity of these estimates has been challenged, as described later in this chapter. On the basis of theoretical calculations, recommended allowances for energy intake during pregnancy have been set at 200 to 300 kcaVday (FAO/WHO/UNU, 1985; NRC, 1989) above nonpregnant levels; however, few dietary studies of pregnant women corroborate increments of this magnitude. Hytten (1980) suggested that the increased needs of pregnancy could be met by reductions in physical activity. RELATIONSHIP BETWEEN ENERGY INTAKE AND GESTATIONAL WEIGHT GAIN Tables 7-2A and 7-2B list studies in which the relationship between energy intake and gestational weight gain was described. Longitudinal studies of well-nourished pregnant women indicated a slight, although not always statistically significant and not universal, increase in energy intake during pregnancy. One study showed that the energy consumption of Scottish women increased gradually through the second and third trimesters to the extent that energy consumption at parturition was approximately 150 kcal/day higher than intake before pregnancy (Durnin, 1987; Durnin et al., 1986~. In a study of well-nourished Dutch women, energy intake was unchanged throughout the first two trimesters and increased in the third trimester by approximately 47 kcaVday (van Raaij et al., 1986, 1987~. In an
139 U) ._ au ._ - Ct ._ ._ Ct a) ~4 c ._ Ct ._ Ct ;^ a' ._ Ct au ¢ C o ,o _ _ en ~ ~ ~ ~ s o ~ ~ ~ C) V) o . _ Ct ~ ~ o ·C~ Cal ,= +1 - ^ ~ Ct ·= C: ~ 5 D .= al ._ ~ ~4 ~t 5 ~ c',. C Cal C' O ~ D iV C ~ C) ;~O of _ LLi m~ ~ O o ._ Ct - o Ct ~ i_ O ~ 3 D 3 ~ C D S: D ~ I I D o~ ~ Z ~ D V, .= ~; .= _ ~ ~1 ° ~ e4 ~ - ^ ~ ~ ~ ~° c 3 r1~ cc ~ 3 C ~U) C~ X X X X X C,, V) ~C ~C.q C ~ ~ ~,= ~,s "s: ~ 't D D "D D D :: ts ~t: ~ O O O O O O O ~C~ ~ ~ O ~^ C~^ -^ -^ -^-^ ~: ~ 3 3 3 3 3 o o o o o o ~ls o~ ~o ~o ~o~ 11 3 11 3 11 3 11 3 11 ~11 ~U ~C ~r~ o V o ~o ~o ~o ~°~ C U ~C~CO U C) . _ · _. _. _ . _ ~3 ~O ~O ~O 5 0 ~O ~o 5 ~·~ c: ~ ~'=' ~O ~ o 11 X ~4 11 o ~o 11 o 11 11o~ 11 11 ~11 ~ ~oo ~C~ ~ C ~ ~oo ~ V ~ 2 ~^ ~ 2 - ^ C) 2 c~^ ;: 2 /\ ;: 2 ~^ ~ 2 _ ~ 0 s~ e, ~ E j D V A oo D Z ~ C~ a~ ~C~ O ~ ~ C~ O ~ _^ C ~
140 ._ A_ a: Ed o a, - ~ o hi, C.) A- ~ C) Cal o ~ Cal Cal ~ tl sit ~ C) m -^= .,, tl.°- ~ , ~ ~ . O - I_ cut ,.D ~ Cal ~ ~ ~ Ct oc ~ ^ ~ V: .o al o ~ ;^ so CQ Ct ~ ~ '= ~ o Cal o ~tic ~ . - ~ · is, 3 ~ ~3 5 ~ ° 11 ° ~ 5 ~ is · - ~S ~ o . ~. ~ ~ ~. ~ . ~ 3 11 ~ V 3 3 .- ° 3 3 ~ ~ ~ Z ~ Z S V ~ V) ~ Z .S Z .= Z .= _ ~ ~.= Z .= .= ~ ~, ~ ~ ~ .= ~ .= ~ ~ ~ ._ ~3 ~ ~ ~ ~3 ~3 ~ ~3 ~3 ^ U~ ', X tl ~ o D ~ ._ · C: t . C.) tl ,= oo o ~D ~ ._ · C: tl 11 · =, C) X tl u, co~o] 5 tl 11 P.4 o ~ ~4 ) X tl .s oo ~ · C: tl 11 {:~4 ~ x +1 ,= °O D oo · '_ 11 ~ X tl ~ "s: o 5 O ~ · C: tl 11 ~ ~4 o C: s ~ ~C) ~C) ~ ~_ ~ C ~C ~Cpq C ~C ~U: ~C) ~ .S .s .s .s .s .s ~ S ~- , ~I') ~t~ ~O ~ +1 ~) co tl ~ ~tl ~ ~tl ~ ,~, tl ~ c ~t ~^O 2 ~^O 2 - ^O 2 - ^O 2 ~^O 2 - ^O 2 Ct ;` oo - ~o o o o ~U) C ~C~ U) Ct Ct Ct Ct ~> ~:` 't ~t- ON ~ o ~o ~ ~C~ C~ ^ C'0 ~ ~ _ C., - Ct Ct ~ C~ ~ ._ Z ~ .= .- ~·-
141 on o ~ o ~ V ~3 V ~3 ~ ._ ~ ~ 5 ~ ~c, ~o . ~ ~ ~ ~. ~ ~ . . ~. ~ ~. ~= ~ 3 ~ ~ · 3 ~ ~ · 3 · 3 .- · ~ 3 11 ~ · 3 11 ~ 11 ~-3 11 ~ 11 .= ~ce 11 .t~ ~ ,, ct en; ct c/) = ~ ~to .= A: on -^ ° .~: ~ on -^ g $= -^ o ~ Z of -^ g _ = · = ~,o t~ V = ~ Of 'C) V ~ ~ V = . = ~V ~ ~ ~Z Ct (a) ~ X ~ no, ~ o ~ X ° X ~ X +1 c, ~tl ,_ +1 ~tl ~0 0 0 ~ O 0 0 0 0 Z - ^ ~- ^ - ^Z Z ~ ~'t ' ' - ~ _ 0 ~ ._ ~ ~ ° tl 11 tl 11 tl 11 tl 11 tl 11~ 11 3 11 ~ ~ ~ ~ ~ ~0 ~0 ~ u ~c~ ~s~ u, cn · ~· 0 ~cq C~: C~ ~.s .s . I_ s_. ~· _ _ ~c~) t- -o ~ ~ ~ ~-) ~1' 1 ~1 ~ =} tl ~ ~tl ~ 0 tl ~ 0 +I t~ oo ~ ~ ~a ~ O c~ ~ + 11 oo ~., 11 ~ =, 11 o~ =,. 11 ~ =,, 11 ~,. 11 ~ 11 o ~,, 11 o ~,, 11 - ^O ~- ^O ~ ~^V 2 ~^O 2 - ^O 2 - ^O 2 - ^O 2 - ^O 2 - ^O 2 ._ ~C~ E . _ ' ~3 w D ~D ~3 n 3 ~w o oO _ ~_ c ~.- =, ~ =, r ~3 ~1
142 o ~ ce ~ _ _ Ct ~ ~ ~ ~ o o ~ ~ ~ ~ V, S ~ ~ ~4 o U) ~ a ~ tl ~, - ~ of ~ m ~ Ct ·= C: =' ~ a tl ° ._ ._ Ct .= ~ .° - ._ Ct ~4^ °Z on ~ _ ili ' tl t ;> ~ a:; ~ o A: ._ ¢ o Ct o o ~ o ~ ~ Cal ~ Cal - ^ en Cal - en C;: - I: ~ 't ~ ~ 't Go ~ ~ oo ~ ~ 3 11 Vl c ~ A ~ <~ ._ ~._ ~ ._ ,_ ~ ~^ 8 oj: ~ tl =: ~ tl · ~ ~ 0 V e<> ~ t~ ~ Ct ~ 3 ~ 3 ~ ~ ~ ~ ~ ~ o X tl ~tl ~ c`) 0 ~o O Z Z Z - ^ Z ~ ~a' ~ ~s~ ._ ._ ._~ ._ ._ ~ ._ ~- ~- , ~ 11 ~s 11 ~11 tl 11 ~s 11 tl 11 V v, ~n £ {,., { ~c' ~5 ~c`, CJ~ ~') ~ ~O ~3 ~ ~Cr, ~oOo ~^ tl t~ = ~tl ~ o ~+1 ~ 0 +1 ~ en +1 ~ ~ +1 ~ x c~ ~cr~ ~a~ ~oc ~o ~c~ ~ ~ P~ ~^O ~ ~^O 2 ~^O 2 - ^O 2 - ^O 2 - ^O - ^O 2 U · E - ' v o , CL. D V , = o 3 3 _ ° ~0 3 ~ ~t ° ~c ~ 3 ~ + o0 Ir ~,,: °- ~ON ~.^ ct ~ct _ 0 - v: v~ c. ~ ~ \c ~,( , ~ ,
143 . ~ ._ D ._._ 3 ~ Cal C,) ~ Z ._ ~ ._ ~ ~ ^ ~ to of ~ on . _ pat ~ ~4 s 3 ~ Z ~ Z Z X d" X tl ~tl a= ~ ~° Z Z Z - ^ ~ 3 3 ^ 5 · - - . A - 1~ ~ cad ~HI tl 1 ~4 to C ~ {A c) ~{ ~,3.) <~ ,a,~ <3, ~< ~V ~C.) .~ .s .s ~.s .s ~.s .e I_ ~ ~ I_ $_, \,., ~_ I_ 5 ~c~ ~ o ,= ~ ~ ~ .= c~ ~ ~s, . ~oo ~ ~ ~, c'> - tl ~ tl ~ ~ tl ~ tl ~ tl ~ tl ~' t~ tl ~ tl ~ tl ~D 11 11 ~11 11 o 11 ~ 11 11 - 0 1I cr 1I r~ 11 o~ 11 11 ~ 11 ~ 11 ~ 11 11 ~^O 2 ~^O 2 - ^O - ^O 2 - ^O m^O - ^O - ^O 2 - ^O - ^O - ^O 2 c: oo ~ ~ ~ ._ I A ~=^ tv ~ ~^ ,1, ~ ~^ ~ Ce ~ Ct _ C 5 S ° C c c, o 0 0 3 3 ~ °° ° ~ ~'t 3 ~ tl ~ 3 ~ t oo _ _ `,, O °c ~ ~ ~= _ 3 50 - ._ ~:; Ct U, Ct 3 C) o o~ - o s o Ct .o Q o Ct ~ o o ~. _ C~ _ . Ct _ - ~ _ _ ~ ~ c=t Z Z 11 11 (: ce C~? C~ Z Z
144 ;D . _ ._ o - ;> ._ ;^ so ._ so .= Ct ._ 3 Ct a) Ct i_ ~4 .= - Cal ._ m a O C) ·_ O ;^ - . ~ ~ ~ Cal O . ~ Ct ~ O ~ of ; - ~ tl so: .- =O m -^ ;~` ~ ~ 5 Ct ·_ ~ .= .0 ·3 o^ ~ Cal ·- ~ tl c,, hi ~ ~ O - ~ . ~ tl Ct ~o Z =' ~ ~ ~ ~ ~ ~ 0 o ._ ce o c~ . - ~ .= O^ D Cl) 11 --0, s: 3 ._ ,] 0 c~ ~ ~i ~Z X ~ X - ) X ~ X Ir) X tl ~+I ~tl ~ tl '= +l ,: O o O o ~0 0 ~ O C-] O ~c ~c ~ c ~u, . - ._ c' 0 ~·,. ._ c~, tl 11 tl 11 11 11 11 o~ c ', =, ~ =. C: O C: 00 5 ~ ~ d" 5 =' II E ~`,, II E =' O II ~3 E ~^C: 2 ~^O 2 ~^C: 2 ~4_ ~ ,- ~.oc .oc .o~ 3 r: ~·= 3 3 3 · _ - ~;^ ;^ ~oc D O D O C .o CL ~ °O CL ~' 0 ~c~ V ~c ~ `,: A 3 ~ o c~ ~_ ct _ ct _ c13 ~ ~ ._ C: _
145 Cot .= o , A ~ X ~ X ~ X~! ~(~ X ~ X +1 ~ tl ~ tl ,,tl ,= tl ,= tl ~ o o o oo o ° o ° o O D Cam D ~ DD c~4 D O D c-] ~(~\ ~Ad ·- ~ ~ ~ a.;, ~ ~ c' Is 11 11 11tl 11 tl 11 tl 11 o ~ - . ~ ~ ~ o tV ~ ~ ~c`) ~ ~ er i ~· ~11 [~ ~11 ~0 ~1 ~^C: 2 ~^O 2 ~ ~2 - ^c: 2 J: ~ oc ~0 . _ · _ - s ~ ·= 3 ~ ; ~> ~;~- ~L) Ct ' ~- ~ t: ~ ._ C~ y C;S Ct Ct ~ 5 o ~ 04 ~ Y ~ ~,. ~ ~ ,.= ;~. '~ ;;~` 1 ~ ~ C~ O o _ ce V ct ~ ct A 't .= 3 3 ~ V~ oo Ct C~ ._ o Ct .O Ct _)
146 U: o ~ ~ · _ ;> Ct ~ ~ _ ~ ~ sly 1 I ~ O Cal ~ _ ~ ~ A ~ ~ ~ CQ o ~ Ce ~ o ~ o~ s~ tl t4 C) ~ ;.~ ~ o.e ~ Ct ·_ ~ ~> ~ ~ '~ o o ._ Ct U. ~ D ._ ~ ~^ U) tl z oo (,, {', X tl o o :: tl 11 oo V o ~_ o D ~t t o o ~ 1 _ o c _ c ~ ~ ., c 2 _ c ~ O ~ A _ O _e~] s.= X ~ ._ 1 m S~ o . ;> _ Ct C~ C ~ O U' ~ Ct t~ Q ^ ~ ~ oo oo - - ~ ~ .
147 Z Z X ~ X d" X~ ~ X tl V: +1 V' tl U.tl v: tl ,= O D ~ D ~ D°O D Q0 = ,~ 3 3 . ~. ~. ~. ~,= o C ~t ~ at o ~ Is 11 11 11 tl 11 tl 11 ~ p. ~ P.4 ~ =4 A- in' ~ C o (: ~ ~ ~ ~ ~ ~o ~Cal ~ ( ) =- ~ to 00 ~ ~ (~) ~ ~ ~ ~ Dot tl ~ ~ tl ~ ~ tl ~ ~ tl ~ ~ +1 ~ ~ tl - ° II AL 11 ~-° II ~0 1111 11 ~0 11 ~ 11 ~ C4 ~ ~ C ~ ~ ~ ~ ~ ~ 00 P~. ~ t- ~ ~ ~^c: ~ ~^O ~ ~ 2 ~^O ~ ~ 2 oc ~04 ~ '_ ~ 't ~ ~a ) ~ ~ In ~O C C ~C ~ ~ c.) = .'~ ,~ oo C C;: V :;, ~ ~ A 't 3 ~ tl CC 3 '= tl tl CL oo oo cr ~ oo cr _ ~ Ct V' ~Ct . ~ O O ~ ~·o :_ E_ o D C~ _% C~ -5 C O ~ ._ o Ct . _ ~ 5 o Z ~ 11 Ct C~
148 NUTRITIONAL STATUS AND WEIGHT GAIN Australian study, energy intake did not increase during pregnancy Swell et al., 1988~. Minor, but not consistent, changes in energy intake have been reported in other studies of well-nourished pregnant women (King et al., 1987~. Failure to detect significant trends in energy intake may be due to the substantial variability in food intake, the cross-sectional design of many studies, and measurement sensitivity and error. Results of energy intake studies in pregnant women subsisting on low energy intakes in developing countries are inconsistent. In one study from Thailand, energy intake progressively increased during pregnancy (Thongprasert et al., 1987~. In studies conducted in the Philippines and Mexico, a slight, but insignificant, decline in energy intake was observed in the third trimester (Hunt et al., 1987; 1hazon et al., 1986, 1987~. If energy intake does not increase in chronically undernourished women during pregnancy, fetal and maternal tissue accretion may be restricted to that which can be achieved by adjustments in nutrient utilization. Statistically significant correlations between energy intake and gesta- tional weight gain have been reported by some investigators (Bear, 1971; Haworth et al., 1980; Picone et al., 1982a,b; Thomson, 1959) but not by others (Ancri et al., 1977; King et al., 1972; Langhoff-Roos et al., 1987; Papoz et al., 1982~. Thomson (1959) cited a correlation coefficient (R) of .30 between these two variables. Beat (1971) noted a significant negative correlation between preconceptional energy intake and weight gain, but positive relationships throughout pregnancy (R = .05 to .29~; statistical significance was demonstrated in the second trimester only. In a large sample, Haworth et al. (1980) detected a significant relationship between energy intake and weight gain (R = .16~. Picone et al. (1982a) reported a relatively high correlation for nonsmokers only (R = .44), possibly the result of clustering of subjects at the extremes of the range of weight gains. During the first trimester, a positive correlation was observed between the increase in food intake and weight gain (R = .17) (Papoz et al., 1982~. Associations between energy intake and weight gain were evident in other studies, but no correlation analyses were reported (Anderson and Lean, 1986; de Benoist et al., 1985; Endres et al., 1987; Paul et al., 1979~. The relatively weak correlation may accurately reflect or may un- derestimate the actual relationship between energy intake and gestational weight gain. Assessment of the relationship between these two variables is problematic (Kramer, 1987~. Precise and accurate measurement of energy intake is difficult, particularly over the 9-month gestational period. High variability in food intake by pregnant women, as is found in general in the United States, was reported in all studies. The relationship between energy intake and weight gain is confounded by intervening variables such as physical activity and body size. Because weight gain or loss is determined by net energy balance, an evaluation
ENERGY AND ASSOCL4TED WEIGHT GAIN 149 of the impact of energy intake on weight gain requires information about or control of energy expenditure. An accurate measurement of energy expenditure by indirect calorimetry throughout pregnancy is technically difficult. Application of the doubly labeled water method to pregnant women should refine estimates of the energy available for weight gain. The energy cost of weight gain may be overestimated by excessive extracellular fluid expansion, which occurs at negligible energy cost to the pregnant woman. Toward the end of pregnancy, the rate of weight gain often decreases; thus, differences in the length of gestation between individuals may be confounding. Imprecise quantification of energy intake, gestational weight gain, and modifiers such as physical activity would decrease the probability of detecting a statistically significant relationship, even if one exists. Alternatively, the actual association between energy intake and gesta- tional weight gain may be weak. Variation in energy intake among pregnant women is determined largely by body size and the level of physical activity not by gestational weight gain. The failure to achieve statistical significance in the majority of studies reviewed in Bibles 7-2A and 7-2B may have been due to insufficient statistical power. The sample size required to detect a significant correlation of .1, .3, or .5 would be 784, 195, or 86, respectively, at a significance level of .05 and a power of .8. Gestational weight gain is unquestionably a function~of energy intake, although the strength of the relationship is confounded by intervening factors. Maternal weight gain, skinfold thickness, and birth weight have been reduced by iatrogenic dietary restriction during pregnancy (Campbell and MacGillivray, 1975~. Acute maternal deprivation during the Dutch famine of 1944-1945 in the western part of The Netherlands provided a dramatic demonstration of the impact of energy intake on the course and outcome of pregnancy (Stein and Susser, 1975a,b). Pregnant women were subjected to 6 months of gradually increasing deprivation (~670 to 1,414 kcaVday), followed by rapid rehabilitation (~3,200 kcaVday). Birth weights were reduced substantially ~-300 g) at the height of the famine and rebounded (+400 g above the famine nadir) after the famine. Detrimental effects on birth weight were confined to women who consumed fewer than 1,500 kcaVday during the third trimester. The limited data indicate that postpartum maternal weight declined 4.3% during the famine and rose 10.5% above famine levels during rehabilitation. Some studies, particularly those conducted in nutritionally vulnerable populations, have shown that energy supplementation results in increased gestational weight gain and birth weight (Bhatnagar et al., 1983; Herrera et al., 198~, Iyenger, 1967; Kardjati et al., 1988; Tontisirin et al., 1986~. The compilation of studies in Tables 7-2A and 7-2B indicates that energy intakes by adult pregnant women living in industrialized countries are generally
150 NUTRITIONAL STATUS AND WEIGHT GAIN greater than 1,900 kcal/day, and their gestational weight gain exceeds 10 kg (22 lb). The energy intakes by women in developing countries are generally less than 1,900 kcal/day, and associated weight gains are less than 10 kg. STUDIES OF ENERGY SUPPLEMENTATION DURING PREGNANCY Energy intake is one determinant of pregnancy outcome amenable to experimental intervention; studies that evaluated the effectiveness of en- ergy supplementation on weight gain during pregnancy and on birth weight are summarized in Tables 7-3A and 7-3B. The subcommittee reviewed the findings and limitations of intervention studies conducted in both develop- ing (Thble 7-3A) and industrialized countries (Table 7-3B). The likelihood of demonstrating the effectiveness of energy supplementation during preg- nancy is enhanced in nutritionally vulnerable populations. This explains the focus on developing countries in this review. Although not without exception, the studies in developing countries represented more poorly nourished women than did studies conducted in industrialized countries. The subcommittee focused on the impact of energy supplementation on gestational weight gain and fetal growth. Information regarding other fetal or maternal outcomes was not consistently provided in reports of the supplementation studies. Supplementation Studies of Pregnant Women in Developing Countries In the following discussion, women are described as chronically under- nourished, malnourished, or marginally nourished. Different investigators used different criteria to categorize the women based on customary dietary intake or anthropometric measurements. Guatemala Chronically undernourished women from four Guatemalan villages were offered either a protein-energy supplement (stole) or a low-energy supplement (Fresco) (Delgado et al., 1982a,b; Lechtig et al., 1975a,b, 1978~. Initially, the study was designed to test the effect of protein supplemen- tation, but the investigators discarded the initial design on the premise that the effects of energy supplementation might be masked, because no advantage of the Atole over the Fresco supplement was evident. There- fore, post hoc analyses were performed in which women were categorized according to self-selected levels of energy intake (Table 7-3A). The mean monthly rate of gestational weight gain was 1.2 kg (2.6 lb); the adjusted correlation between supplemented calories and monthly weight gain was .213 (N= 137) (Lechtig et al., 1978~. The greater the level of energy supplementation, the lower the proportion of mothers with low gestational
ENERGY AND ASSOCIATED WEIGHT GAIN 151 weight gains, defined as less than 0.5 kg (1.1 lb) per month. Birth weight was significantly related to energy intake over the course of gestation (29-g increment in birth weight per 10,000 kcal from the supplement). Compar- ison of the high energy intake group (>20,000 kcal) and the low energy intake group (<20,000 kcal) indicated that a net increment of 149 kcaVday was associated with an 111-g increase in birth weight and reductions in the incidence of low-birth-weight (LBW) infants and preterm births. The major limitations of this study included subject self-selection and exclusion of 38% of the sample because of missing birth weights. Colombia Poor women at risk of undernutrition were randomly assigned to sup- plementation or control groups for the third trimester of pregnancy (More et al., 1979~. Energy supplementation (net increment of 155 kcaVday) had a significant effect (p <.05) on the birth weight of male infants only (+95 g). Weight gain of the women who were supplemented for 13 weeks or more and had male children was also higher (+140 Greek) than that of controls, suggesting that improved maternal nutrition influenced birth weight. The gender-specific effect of supplementation may have been due to the achievement of the greater fetal growth potential in males. Post hoc stratification of the sample by maternal weight-for-height ratio at 6 months of gestation revealed that supplementation had a significant impact on the birth weights of infants of both sexes (+181 g) among women with lower weight-for-height ratios (Herrera et al., 1980~. Taiwan A group of rural lkiwanese women was given a protein-energy supple- ment (800 kcaVday) or a low-energy supplement (80 kcal/day) from 3 weeks after the birth of their first (male) child until the end of the lactation period for the second child of either sex (Adair and Pollitt, 1983; Adair et al., 1983, 1984; McDonald et al., 1981~. Supplementation prior to and during the second pregnancy had no effect on anthropometric measurements (ges- tational weight gain, body weight, or skinfold thickness) of these women whose usual diet was only marginally adequate. Maternal weight gain aver- aged 7.6 kg (16.7 lb). Comparisons of outcomes of the second pregnancies (birth weight, incidence of LBW infants, and fetal deaths) revealed no statistical differences between the two groups. Within the supplemented group, however, male infants born after a nutrient-supplemented pregnancy had significantly higher birth weights than those of first-born males (+162 g) These findings suggest that some infants benefited from maternal supplementation, even though maternal anthropometric measurements did
152 ._ 3 - Ct 4 - Ct Ct -~ UP ~ ._ :: o 3 ~ o m ~ AL ~ cq ~ O O Ct ·- O ~ 3 Ct ~ so o ~ .o U. ~ ._ ~ ~ 1 ~ Cal o ~ c: ~ o ~ C) - ~ I: <, ~ Ct ~ ^ .= IS ( Cal - Cal . it Ct o ~ 4 · Cal o 3 Cal ~ ~ m ~0 .- tl me Ct ._ ~ 3 ._ Ct 3 Ce Cat ~ tl on ~- ILL tl 't A> Ct 0C U: . O ;^ ~ ~ ~_ V, _ - Ct CO o . _ Ct C Ct ~ _ _' O C~ O ~ Ct CD O ~ 3 ~ V ·3 V ~ 3 ~ ~ ~ ~ ~ e~ .~: ~ ~ .= 3 ~c, 3 o C ~ ~ ~ D ~ ~ o ~ Z Z tltl tl tl ~oo ~ o ~o o o o =: .. oo tl tl ~: o ~Z Z Z Z o oo tl tl o ~o oo ~ ~0 ~ _- ~ '_ _ Il Ge ·c E ~ E ° E ,~ 2 _ E ~ ~ ~c ~ ~ . 7c ~ ° 2 c C S ~> i~8 r°~ O ~ O ~ ~ ~ ~ ~ s^ M0 ~ s^ ~ ~ ~ 11 ~ c~ 11 c ~ ~L + 'c.r, C -C ~ ~ C ~ D o 5 D ~ 3 ~ 2 ~ ~ 2 E e c e, 0 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ . _ _ ~ D ~4 5 ^ ~ ~ O ^ · ~ c ~ 3 ~
153 .= ^ two £ ~ O to ~ ° ~ To 0 ~; O e u, ,,, e v 3 c ~ e ~ ~ c ,_ 3 ~,0 c 0 C O D ~ C C 3 V C V c, D C ~ ~ C) ,C E ° c 3 D R: C o ~ D ~ ~ D ~ ~O ~O °O tl tl~^ °° <~ ~tl tl tl ~ 0~ ~ (~, 0o ~0 ca~) - ^~^~ ~ ~ ,~,: ^,~d ~oc ~t- ~ 0 ~ 0 ~ u ~oo ~ ~ ~0 ~c ~0 ~ 0 0 tl ce tl ce tl c;, tl ce tl 0 ~ 0 ~ 0 oo 0 oo ~ ~ ~u~ ~u~ ~ ~ ~ Z Z ~c ~o {,. ~ ~ ~ ~o ~ 0 tl +1 u, ~ ~ ~ ~ v° ~ =' +1 ~D ·- ~ c~) c~ .~- ~ ~ ~ z - - ~ ~ct o ~) o C ~c s c e 0 c 0 c 3 ~ ~ oc c ~ E ° - A _- 0 s ~ ~ c c e c e c s 0 ~c .: 0 E ~ s V O _ ~ 3 c _ E ~ D ~ g o C O - E ~ CL _ _ s 0 ~ oo ^ ~0 7 ^o ~ ~ m 0 0 O s c x s . D ~c ~ e °~ e 0 ~3 ~ s . 3 A ~ C
154 V, D Ct ._ U) ~ ~, O ._ Ct ~ ·O C) o 3 C~ ~q ~ ~ m 00 .- tl m ~ c: ~ Ct ._ ~ 3 ._ o~ ._ ~ tl ;^ ~ ,= tl 't ~5 C~ a ._ o 1 Ct ~: U. . ° ;` C~ e~ C: o . _ Ct _. ~ o > _ _ o ~ Ct z Ct . ° Ct C) ~ o C) , E ~ ~ 3 ~ ~ ~ 5 ~ G ~ E - , ' ~ ~ ~ _ D ._ ._ ~ C ~C~ oo C~ O tl tl cr ~ oo o o 3 o o tl o o ~ o o tl oo o oo cr~ .. .. ~ oc 3 ~: tl tl oo ~ ~ o tl o ~ 3 ~ o o tl ~ol~- ~oo 4 . '7 - o C ~ ~oo ZZ ~^ ~^ -- U,^ - ~: =^ ~ ~o o (,,)o ~o < c ~ c _ 0 ~ ~ c C ~U) ~ C) ._ o ~ ~ 3 ~o ~ C~ oo .= 5 Ct ~ ._ Ct ~ ~ .^ .= ·s ~ c<5 - ^ cn c~ ~
155 ~.= o ._ ~ . - ~ ~ c ~ C ~ 3 .= ~ c >~ cL C C = o C V C V o Cat ~To tl tl tl tl ~o o ~ Cal ~ AL Ct & C-< on ,Y ~ ~ -t ~ 2 ~2 ~ ct ~ ~ ct ~ tl ce tl ct o ~ o ~ ~ o ~ o o ° eLl) C ~C, ~ ~ ~ ~ ~ t- "o 5 ° If tl If tl If tl If tl If tl If tl ° en, ~.. .. .. .. .. .. Cat + - ct c\: - ~ ,,, ~ ,,, E ~ 0 m c < ~0 m ~0 ~ ~ E o ' ~o- ~E o ,~ ,, ~ ~ E C ~C ~ U) ~? G ~ ~ ~ ~ ~ c ~; C e ~ c Z ~ 00 .= _ ~ C _ ._ ~ (~\ ^-3 = ~om o (~5 . ~ Ct ce ~ e. C~ ~ ~; Ct Ct ~C~ o S: o o ·3 Ct ·;~ O O · ~cO~ . _ . Ct =~ 5 ~ ~ E ~ ~ Z ~ ~ ~ 3 o u, ct u, 11 oo
156 ._ 3 Ct so Ct a' Ct ~Cal c: ~ _, . _ to a) 0 3 .- me U: .= o S. Ct _ .. O Ct ~ I-, o ~ HI, ~ .o U. ~ ~ 1 ~ U. .o - o ~ _ ~ 0 em en ~ .S ~ Ct U) - Ct . v, ct O o 3 Cal u, cry ~ m 00 . - +1 m ~ Ct ·_ ~ 3 ._ Ct ._ 3 +1 ;^ OF ~- +1 't c) Ct c\5 ~ > e ~? o~ ~ c) c~ ~ c ~ .o ct ct =, e~ ( . - ~ ct o ~ A o A - - - Y o e A e e 3 ~ e 3 _ v 0 D 3 e V O _4 A o`, C ~C · · O A ,,, 3 c ., D - ~ e c,, u 3 Z c) 0 0 U~ 0 0 ~0 U ~U~ +1 +1 +1+1 ~D Z Z Z oo a~ +1 +1 ~D +1 oc oo ~oo ~ ~^ 7 e ~ ~ 2 <- ~ · Z 9 3 ~ _ v, c ~Z ;> ·^0 ~ e , e ~ A o c ° C _ C C U ~ O ° 5 AC _ C 3 e_ 3 _c, o~ c ~3 ,~, c ct ~ ~ 0 v' Z
157 ° u,^ ° _, c V c ~ 3 , ~ _ e .= ~ ~ ~ ~ 3 CAL .= ~ 5 ~ ~ `: .= 3 ~5 Al +1 0 Go cr ~ Do of ti to ~0 00 . . . ~O O _4 ~ O ~ _ _ Ct en C) C) $ O ·_ C-) ~ t- ~ ._ ~ 11 ~ ° .. o =2< ~m ~ ~ ~ _ ~ .~ E O ~ ° it,, ~ O ~ :~ ~ ° ~ + 2 ~ + 2 cat cat o o 0 3 c -,, ce en I- ~ on cat .- . v) z; ~ o o ~ ;~` ~ ~ - ;> 5 ~ ·- ~ _ ~ C) o _ ·^ (~\ Ct Ct ^ ._ ', ~L O O 3 c~ ~
158 A a: m AS , Ct .- =0 - ~ o 3 Cal Cal ~ m AS .- +1 m ~ 0.C Ct ._ ._ Cal V _ =: Ce Cal ~ al ;` C -= Ct Ct a ~ Is: ·C,0 o Cal Ct ° Ct ~ Ct _ U' ·_ C: Ct ._ _ ~ Ct ~ o ~ ~ ~ OC ~ O O D C E 2:'~ C <<s D C c, cL a c`, C C ~ V =- ~ ~ ~cL + ~ ~ ~ 3 ~ ~ ` m ~ O O O ~ tl tl tl tl tl ~0 0 0 u~ u ~c ~0 u ~ c ~0 0 o ~a ~0 3 3 o ~oc ~4 ,~: ,. ~,Y 0 0 ~3 3 ~3 tl tl ~C ~c ~O 0 ~0 oo 0 0 tl t ~ ~ ~ o ~ Z Z Z Z Z Z - ^ - ^ _ , _ A ~ ~ · ~ E ~ ~, ~' ~ ,r, - ~] 2 r- ~ ~ ~ E ~ 0 ~- v' ~c ~c ~c~ . ~· ^ . ~ u O s v, ° u , E E ~ _ <, - c ~ _ ~ ~' ' ~E E ~ ~ 3 3 _ 0 0 P~ c~ s: ~' ~ 0 ~ ~_ °D ~D, ~ o~ ~m ~
159 o arc 3 o :, C c, o ,, C C C 3 c o c ,_ ~ 3 o o o o c, ~ o C ~ ·,,, <,4 c · ~ at, - ·- ~ 11 ~ cat 11 5 =: 11 ~ c, ~ ~ ~ >~ ct p .= ~ ,, ~ ~ .= D ~ ~ ~ ~ .= ~ ~ ~ ~ ~ ~ Y O ~ .~ 3 ~ ~ ~ ~ ~ 3 LO ~ oo Us Vet ~ oo Cat ~_. 17 ^ ^ Cot of oc Z Z Z Z PI ~° o ZZZZI_ - ^ ~ oo oo °°11 ° - 11 ~11~ 11 =,2z:2~ 2 e ~ct .= oo ~.= ~ ~.=, u, c' ~ s: ~ ~ ~c~ ~ ct ~ _ ~ C!S ~ _ C~: i- ~L c,, 11 c,) ~ 11 ~, sL, o 0 2 ,= 0 2 , ~0 ,~ Z ~Z ~Z~ ^ 0 v . 8 G 3 O _ D U , O. . 3 c 03 c · e ~ 3 r~ - ~03 ~= c~ Z7 7 _ 00 ~ C ~ C~0 00 ~ e y ~, ~ :, g ~ ~ ._ Ct U. o 3 11 ~o ~ ._ .= ~ ct 0 E =L c~ 11 ~Z3 ct o~ . O 5 5_ o o o .= ;> s~ Ct C~
160 NUTRITIONAL STATUS AND WEIGHT GAIN not differ between the supplemented and unsupplemented women. The weight gain of approximately one-third of all these women during lactation suggested, however, that their usual energy intake was adequate. Weight gain during pregnancy and maternal weight for height may have been almost optimal for these women. The potential to increase birth weights in this population was limited, because pregnancy outcomes were already favorable: the mean birth weight was >3 kg and the proportion of LBW infants was <6~. A positive energy balance was maintained throughout gestation and lactation in this group of women who reported low usual energy intakes (1,200 kcal). Estimates of energy intake were seriously flawed, however. No information was collected on between-meal food consumption or preintervention dietary intake. Thus, it was impossible to determine the extent to which the feeding program supplemented home diets. The original design to study supplementation of marginally nourished women was not achieved for two reasons: indiscriminate subject selection and failure to quantify the intervention variable. The Gambia Rural Gambian women received an energy-dense dietary supplement (net increment of ~400 kcaVday) throughout pregnancy (Prentice et al., 1987~. Since all pregnant women in the community were included in the experimental group, it was necessary to use retrospective controls. Supplementation had no impact on weight gain or fat changes (as measured by triceps skinfold thickness) in either the wet season, when food shortages and agricultural work caused negative energy balances, or the dry season. Stratification of the mothers by height, weight, or weight for height did not indicate an advantage of supplementation for the more undernourished women. Supplementation was highly effective in augmenting birth weight (+225 g) in the wet season, but was ineffective in the dry season. The proportion of LBW infants decreased significantly from 23.7 to 7.5% in the wet season. There appeared to be a threshold above which birth weight was protected from the acute effects of malnutrition; birth weight was compromised when the women were in negative energy balance. The mechanism by which birth weight increased during the wet season but maternal weight gain did not change is unclear; the authors suggest that the supplement shortened the otherwise long overnight period when women took no food and thereby increased glucose availability to the fetus. Theories of adaptation have evolved to explain how these active preg- nant women existed on energy intakes that barely exceeded estimated basal requirements. Subsequent studies on the energy expenditure of pregnant Gambian women, however, have cast doubt on the energy intake records of the earlier investigations (Lawrence et al., 1986~. In the later studies,
ENERGY AND ASSOCLi4TED WEIGHT GAIN 161 mean daily energy expenditures during pregnancy exceeded previous esti- mates of energy intake by approximately 950 kcal. It is believed that this large discrepancy between energy intake and expenditure resulted from an underestimation of energy intake. Although understanding of the energy balance of these Gambian women is incomplete, the major impact of sup- plementation on birth weight and the incidence of LOW infants during the wet season was undeniable. Chile The effects of supplemental powdered milk (498 kcal/day) on maternal nutritional status and birth weight were compared with those of a milk- based product fortified with minerals and vitamins (470 kcaVday) in a group of underweight pregnant women (Mardones-Santander et al., 1988~. The supplements were distributed from approximately 14 weeks of gestation onward. For full-term births without complications, the fortified product was associated with statistically higher maternal weight gain (+0.9 kg, or 2.0 lb) and birth weight (+63 g). The relatively high increment in birth weight relative to maternal weight gain (74-g birth weight per kilogram of maternal weight gain) may have resulted from the increased supply of micronutrients. Greater rates of weight gain in those with similar energy intakes may have been caused by greater maternal fluid retention and plasma expansion. The lack of randomly assigned unsupplemented controls precluded evaluation of the overall effect of supplementation on weight gain and birth weight. Supplements were distributed monthly; sharing of part of the supplement with other family members was acknowledged, but the amount was not quantitated. Supplementation Studies of Pregnant Women in Industrialized Countries Canada A retrospective matched-pair analysis was performed on pregnant women who had received nutritional counseling and, if it was deemed necessary, dietary supplementation at the Montreal Diet Dispensary (Rush, 1981~. A small and nonsignificant increase in weight gain (+0.3 kg, or 0.7 lb) was observed. A significant increase in birth weight (53 g more than that of controls) was limited to infants born to women who weighed less than 63 kg (139 lb) at the time of conception. The proportion of LBW infants was not statistically different. Scotland A group of primagravid women (N = 90) was selected for energy supplementation on the basis of poor nutritional status associated with a
162 NUTRITIONAL STATUS AND WEIGHT GAIN high risk of delivering an LBW infant (Campbell-Brown, 1983~. At 20 weeks of gestation, women classified into the lowest quartile for weight, height, or rate of weight gain qualified for supplementation (300 kcaVday during the third trimester). Maternal weight gain and birth weight were greater in the supplemented group than in the matched control group, but the differences were not statistically significant. United States Reports of intervention trials and evaluations of the Special Supple- mental Food Program for Women, Infants, and Children (WIC) often omit consideration of program effects on gestational weight gain; evaluation of the program effects on birth weight are conflicting. A fundamental problem germane to these studies is the selection of unsupplemented controls. The use of women enrolled in WIC postnatally as control subjects tends to lead to overestimates of the impact of food supplementation, since one criterion for postnatal WIC enrollment is delivery of an LBW infant. Alternatively, control subjects recruited from the community tend to be at lower risk of an adverse perinatal outcome compared with WIC recipients. In a nationwide evaluation of WIC, food supplementation for longer than 3 months was associated with an increase in weight gain and in mean birth weight (+68 g for 3 to 6 months and +136 g for more than 6 months of program participation) (Edozien et al., 1979~. The duration of gestation was 5 to 6 days longer for women who were enrolled for more than 6 months. A major limitation of this evaluation was the small number (41) of non-WIC participants used as controls. In a prospective, randomized, controlled evaluation of WIC conducted in Oklahoma (Metcoff et al., 1985), women eligible for WIC were ran- domly assigned to WIC or to an unsupplemented control group. The WIC group had neither greater mean weight gains nor infants with higher birth weights compared with controls. Food supplementation was reported to be beneficial among smokers (+168 g increase in infant birth weight) but not among nonsmokers. A longitudinal study was designed to overcome some limitations of previous investigations of the effectiveness of WIC supplementation (Rush et al., 1988~. In this study, WIC participation was associated with increased energy intake, normalization of weight gain that had been low in early pregnancy, and decreased triceps skinfold thickness late in pregnancy. There was no apparent relationship between WIC supplementation and birth weight. The failure to demonstrate any positive effects of WIC supplementation on birth weight may have resulted from the small size of the control sample or from insufficient adjustment for differences in social factors between WIC participants and controls. Lower frequencies of early
ENERGY AND ASSOCLi4TED WEIGHT GAIN 163 delivery (<33 weeks of gestation) and of preterm delivery (<37 weeks) among the WIC participants did not reach statistical significance. In a New York City trial, women at risk of preterm delivery were given one of three specially formulated supplements: high protein-energy, balanced protein-energy, or vitamin-minerals (Rush et al., 1980). Weight gain in this study was significantly related to energy and protein intakes. The balanced protein-energy supplement was associated with increases in the duration of gestation and higher mean birth weights (+41 g), although the differences were not statistically significant. The proportion of LBW infants was decreased in this group. The high-protein supplement was associated with significantly depressed birth weights among preterm infants; associations with an increased number of early preterm deliveries and neonatal deaths were both of borderline statistical significance. Women who entered the treatment group early and had a history of previous LBW deliveries were especially adversely affected by the high-protein supplement. Total weight gain and the average rate of weight gain (unadjusted) tended to be markedly depressed among the women who delivered preterm infants. Interpretive Summary Despite their dissimilar experimental designs, important inferences can be drawn from published supplementation trials. The basic premise of prenatal energy supplementation programs is that birth weight can be increased by greater energy intake and that this erect is associated with increased maternal weight gain. Few experimental designs discerned the specific, independent effect of supplementation, since most supplements used in the experiments provided not only energy but essential nutrients as well. Also, the relationship between energy intake and gestational weight gain is confounded by several other intervening factors, such as physical activity and body size. Few supplementation trials confirmed the direct link between energy intake, weight gain, and birth weight. It remains unclear whether the effects of energy intake on birth weight are a result of changes in gestational weight gain. Energy supplementation studies of undernourished women demonstrating a statistically significant impact on birth weight showed that gestational weight gain was increased, except in Gambian and Taiwanese women. In these studies, birth weight was increased with no apparent change in maternal weight gain. In the energy supplementation trials of more adequately nourished women, only minor changes in weight gain were observed. Gestational weight gain before intervention was substantially higher in women in developed countries (~12 kg) compared with that in women in developing countries (~7 kg). The impact of energy supplementation on birth weight appeared to be influenced by the nutritional vulnerability of the pregnant women and
164 NUTRITIONAL STATUS AND WEIGHT GAIN the extent to~which the supplement diminished the deficit between usual energy intakes and requirements. In the series of reports of undernourished women in developing countries, customary intakes averaged approximately 1,500 kcal/day, net supplementation in field trials ranged from 118 to 511 kcal/day, and mean increments in birth weight in the supplemented groups ranged between 50 and 321 g ~-40 g in one trial). In the reports of more adequately nourished women in developed countries, usual intakes were approximately 2,000 kcaVday; supplements added between 15 and 261 kcaVday and differences in birth weights in the supplemented groups ranged between-177 and +273 g. The potential for improvement in birth weight was greater in the undernourished populations, in which birth weight before intervention averaged approximately 2,900 g, in comparison with approximately 3,100 g in better-nourished populations, and the incremental increase in energy intake was higher. The proportion of LOW infants was effectively reduced by prenatal energy supplementation, especially in chronically malnourished populations (Table 7-3A). Modest reductions were demonstrated in better-nourished populations. Except for the studies of Delgado et al. (1982a) and Kennedy and Kotelchuck (1984), energy supplementation was shown to have no effect on the duration of gestation. The supplementation of more adequately nourished women at risk of delivering LBW infants produced meager or even negative results if high-protein supplements were used. The lower the nutritional status of the pregnant women, the greater the probability of detecting a statistically significant effect of energy supplementation. In several studies, stratification of the study sample by maternal or environmental factors revealed that energy supplementation had significant effects on weight gain and birth weight. Discriminating factors included weight-for-height ratio in Bogota, Colombia (Herrera et al., 1980), socio- economic status and height in Guatemala (Lechtig et al., 1975a,b), triceps skinfold thickness in Birmingham, United Kingdom (Viegas et al., 1982), season in The Gambia (Prentice et al., 1987), and prepregnancy weight in New York City and Montreal (Rush, 1981; Rush et al., 1980~. Fundamental problems with research design may have prevented the detection of significant effects of energy supplementation in some studies. Effectiveness of supplementation may have been underestimated by imper- fect matching of control subjects or inadequate sample size. Randomization to include control groups was sometimes ruled out for ethical reasons re- lated to the population's nutritional need. The amount of supplement consumed may have been insufficient, because it was shared with other family members, because of noncompliance, or because subjects replaced their customary diet with the supplement. Subjects may not have been undernourished, and intrauterine growth retardation in the population may have resulted from factors other than undernutrition.
ENERGY AND ASSOCLi4TED HEIGHT GAIN 165 FACTORS INFLUENCING ENERGY BALANCE DURING PREGNANCY Weight gain during pregnancy is a direct consequence of energy bal- ance, that is, the difference between energy intake and energy expenditure. The basic components of energy expenditure basal metabolism, thermo- genesis, and physical activi~are discussed below in relation to pregnancy. Basal Metabolism Longitudinal measurements of basal metabolic rate (BMR) or resting metabolic rate (RMR) have been made to ascertain the degree to which metabolism is increased during pregnancy (%ble 7-4~. Basal metabolism is measured in the morning after awakening, whereas resting metabolism may be measured at any time during the day after resting for at least 30 minutes. Resting metabolism tends to be about 10% higher than basal metabolism. Both are related to the amount of lean body mass. Since lean and fat tissues are increased in obese women, their basal requirements are higher than those of women of normal weight. Although all reports indicate a net increase in basal or resting metabo- lism, the magnitude of change differed considerably between populations (Banerjee et al., 1971; Blackburn and Calloway, 1976a; Durnin et al., 1986; Forsum et al., 1985; Illingworth et al., 1987; Lawrence et al., 1986; Nagy and King,.1983; Thongprasert and Valyasevi, 1986; 1hazon et al., 1986; van Raaij et al., 1986~. The reported increase in RMR by the third trimester ranged from 5% in unsupplemented Gambian women to 39% in well- nourished women in the United States. The increase was generally greater in pregnant women from developed countries (27%) than it was in those from developing countries (15%~. Compared with the nonpregnant state, the total increment in resting metabolism for the entire pregnancy ranged from a reduction of 10,700 kcal in unsupplemented Gambian women to an increase of 46,500 kcal in well-nourished Swedish women. The increase in total resting metabolism in women from developing countries was lower than the theoretical value (36,000 kcal), in part as a consequence of their smaller size, but possibly also the result of metabolic adaptations. Thermogenesis The thermic effect of feeding refers to the increase in energy expen- diture above basal metabolism following the ingestion of food. It is due mainly to the energy costs of digestion, absorption, transport, and storage and averages approximately 10% of the energy intake. A reduction in the thermic effect of feeding during pregnancy could minimally conserve energy.
166 a' ct o - ~ At · - o Hi · - a: Lit EN ~ ~ ~ - ~ =.= ~ ~ . - - ct as: at at · at ;^ c) ct of ct At ·D o V) ^ {~d O O ~ Z Ct t) t_ te) O ~ - ACE ~) ON ~04\ ~ED oc ~- ~^ _ _ ~; <~ 0 ~·~ _ c, ~l_ ~ _ - U 0N ~ ~ A _ e 5 3 3 G ~o 0 0 0 0 0 ~0 0 0 0 0 0 ~0 p ~ ~ u~ ~o ~o ~- 0 ~ ~l7 0 ~ Z Z ~ ~ ~Z 1 + - 3 o 0 ~ 0 u~ ~ ~ o ~00 ~oo 0 a~ _ · · · ~ ~ _1 ~_* - ~- O - 3 o 0 3 o ~ 0 c~ ~ _ r ~ o~o o ~ o o ~crx o oo 0~ ~ ~ ~. ~Z 0 0 . ~0 cr~ 0 0 ~C° ~o ~ ~ Z Z 00 ~Z 0 0 0 0 >, c ~ ct O O ~00 V) ~D 0 ~ 0 ~oo crs ~ 0 0 oo c ~oo oo Z ~0 0 0 0 ~0 0 0 0 0 cn ~ ~0 ~ _ O 5 ~e D 3 ~ _ ~ A 09 ~- 04 ._ C~ C) Ct o Ct ._ Ct C) Ct o Ct Ct C~ o C C~ Ct Ct C) Ct s~ 0 ~ Ct ~ . ~ V) O O Ct 1 1 Ct ~_ O ~ ._ ~ .C ~ ~.o ~_ O ~D "S 3 i ~ °O D ~_ . ~ m ~ - ~ ~ .= ~ ~ a' 0 O Z Z 11 11 ~ ~ Z Z CS ~ ~ ~ Ct Ct o Ct Ct m C) V: s~ v: . - ~ ct o ~ 3
ENERGY AND ASSOCIATED WEIGHT GAIN 167 The thermic effect of feeding was measured in seven primigrav~d women at 12 to 15, 25 to 28, and 34 to 36 weeks of gestation and after the cessation of lactation (Illingworth et al., 1987~. The metabolic response to a 533 it 41-kcal (standard deviation) liquid test meal was significantly reduced by 28% (5 kcal) in the second trimester compared with postpartum values. The response was reduced by 15% in the third trimester, but the reduction failed to reach statistical significance. In a contrasting report, the thermic response to a 750-kcal meal was not different among six women in early pregnancy (10 to 20 weeks of gestation), four women in late pregnancy (30 to 40 weeks of gestation), and six nonpregnant subjects studied cross-sectionally (Nagy and King, 1984~. Physical Activity Assuming that increased energy costs of pregnancy were compensated by a reduction in physical activity, Hytten (1980), in his theoretical estimates of energy requirements, did not include an allowance for the energy cost associated with movement of a heavier body mass. Studies of activity patterns of North American pregnant women do not indicate reduced activity (Blackburn and Calloway, 1974, 1976b). Women from industrialized societies tend to have sedentary life-styles but they do not become even less active during pregnancy; reductions in recreational activities during pregnancy are slight. Subtle changes in physical activity, i.e., less walking and more sitting, by pregnant Scottish and Dutch women were noted in two reports (Durnin et al., 1986; van Raaij et al., 1986~. Women in developing countries are generally more active and may have more latitude in adjusting their level of physical activity during pregnancy. For example, pregnant women in The Gambia conserved energy by reducing the amount of heavy farm work and housework they performed (Roberts et al., 1982~. In New Guinea, they decreased the intensity and duration of arduous tasks (Durnin, 1980~. Thai and Philippine women increased their sitting time and decreased the heavy agricultural and household tasks they performed during gestation (Thongprasert and Valyasevi, 1986; 1hazon et al., 1986~. Despite these adjustments, food scarcity combined with hard work during the rainy season in The Gambia was detrimental to fetal growth (Prentice et al., 19874. The rates of weight gain in Ethiopian pregnant women who engaged in hard work were lower, and the birth weights of their children were compromised, compared with women with lighter work demands (safari et al., 1980~. Lower energy intake and lower weights during early pregnancy in the Ethiopian women may have been contributory factors. The energy cost of physical activities has been measured at progressive stages of pregnancy (Durnin et al., 1986; Emerson et al., 1972; King et al.,
168 NUTRITIONAL STATUS AND WEIGHT GAIN 1987; Seitchik 1967; Torun et al., 1982~. The energy cost of non-weight- bearing activities, such as cycling, was not increased during pregnancy. In absolute terms, the energy expended in sedentary activities such as sitting and standing was 15 to 30% higher in pregnant women, but was not different if standardized by body weight. The energy expenditure of weight-bearing activities such as walking was increased in proportion to gestational weight gain; however, the energy expenditure of treadmill walking expressed per unit of body mass did not differ between pregnant and nonpregnant women. Because of their higher weight for height, obese women expend more energy during physical activity than do lighter women. In contrast to these findings, results of the Dutch, Thai, and Gambian studies suggested greater energy efficiency for weight-bearing activities during pregnancy. When expressed per kilogram of body weight, the energy cost of walking on a treadmill at a fixed speed was reduced by approximately 5% in late pregnancy compared with prepregnancy or early pregnancy values (Thongprasert and Valyasevi, 1986; van Raaij et al., 1986~. No increase in the energy cost of 40 activities was found in pregnant Gambian women, despite substantial weight gain (Lawrence et al., 1985, 1986~. Rates of energy expenditure, normalized by body weight, were reported to be less than those of nonpregnant Gambian women, suggesting higher levels of work efficiency. However, walking (nonstandardized and at a set pace on a treadmill) displayed the expected increase in energy expenditure in Gambian women. Various investigators have reported that pregnant women reduce the pace and intensity of certain activities (Banerjee et al., 1971; Blackburn and Calloway, 1974; van Raaij et al., 1986~. Pregnant women may expend less energy per unit of time performing a task, but they take longer to complete the task. Although activity patterns and work intensity can be adjusted to con- serve energy in pregnant woman, the energy expenditure of weight-bearing activities increases in most populations in proportion to weight gain. The impact of physical activity on the energy requirements of pregnancy depends on the proportion of time spent in such activities. Total Daily Energy Expenditure The total energy requirements of pregnancy have been estimated to be 2,115, 2,275, and 2,356 kcal/day for the three successive trimesters. The mean ratio of total expenditure to basal energy expenditure was 1.5 (Blackburn and Calloway, 1976b). The doubly labeled water technique has been applied to three pregnant women in Britain to estimate their total daily energy expenditures (Prentice et al., 1985~. Total energy expenditures of 1,912, 2,490, and 3,009 kcal/day were equivalent to 1.40, 1.39, and 1.77
ENERGY AND ASSOCIATED WEIGHT GAIN 169 times the basal expenditure, respectively, emphasizing the considerable in- dividual variation in physical activity. The total energy expenditure of rural Gambian women has been estimated from time-motion studies (Lawrence and Whitehead, 1988~. Total daily energy expenditure declined from 2,400 kcal/day in early pregnancy to 2,200 kcaVday at term. When adjusted for stage of pregnancy or lactation, total daily energy expenditure averaged 2,300 kcal/day, or 1.68 times the basal expenditure in the dry season, and 2,700 kcaVday, or 1.97 times the basal expenditure in the wet season. Energy Balance During Pregnancy The mean total energy cost of pregnancy computed from data derived from five diverse populations (Table 7-5) was approximately 55,000 kcal for all groups except the Gambian women (Durnin, 1987~. Small differences between the Scottish, Dutch, Thai, and Philippine women may be due primarily to variable amounts of fat deposition, which ranged between 1.3 and 2.3 kg (2.9 to 5.1 lb). Although the ranges of weight gains (8.5 to 11.7 kg, or 18.7 to 25.7 lb) and fat gains (1.3 to 2.3 kg) were wide, variability diminished when these rates of fat gain were expressed as a percentage of initial weight (2.9 to 4.0% of initial weight). Total weight gain was from 17 to 20% of initial weight. The Gambian women had exceptionally low weight gain (7.3 kg, or 16 lb), fat storage (0.6 kg, or 1.3 lb), and cumulative increase in basal energy expenditure (1,900 kcal). Chronically undernourished Gambian women apparently adapted to their pregnancy by decreased basal metabolism and activity and mobilization of adipose tissue; energy supplementation partially reversed these changes by increasing the BMR and fat deposition. In all countries, the estimation of the energy cost of pregnancy was subject to error, specifically in the estimation of maternal body fat and nonpregnant baseline values of BMR, but their estimates were all substantially lower than the theoretical estimates of Hytten (1980~. Increases in energy intake recorded for these populations did not approach the estimated energy costs of pregnancy, except for the Thai women. Apparent energy deficits may be explained by an underestimation of energy intake or by undetected compensatory reductions in physical activity. With the exception of the Gambian study, the investigators were confident of their food intake records. There was some question in the Thai study as to whether the energy intakes recorded at 10 weeks of gestation underestimated prepregnanc`,r intakes and resulted in inflated estimates of increased intake during pregnancy. Underreporting of food intake in the Gambian study was strongly suspected. The investigators fully recognized the limitations of the techniques used to derive energy balance values. The methods used to measure energy intake and energy expenditure during pregnancy were not sufficiently accurate to discriminate to levels of 150
170 NUTRITIONAL STATUS AND WEIGHT GAIN TABLE 7-5 Energy Requirements of Pregnancy as Estimated by the Five-Country Studya Energy Cost and Additional Intake During Pregnancy, kcal, by Country FactorScotlandHollandThe GambiaThailandPhilippines Energy cost Fetus8,1108,2307,1407,1406,900 Placenta730740560600600 Maternal tissues2,8902,9502,4802,4802,410 Maternal fat25,23014,3006,60015,40014,300 Basal metabolism30,10034,5001,90024,00019,000 Total energy67,06060,72018,68049,62043,210 cost Additional energy21,0005,200NRb56,9000 intake Discrepancy in - 46,060 - 55,520 NR - 7,280 - 43,210 energy balance a Adapted from Durnin (1986~. b NR = Not reported. to 200 kcaVday-the expected net increment. Although the absolute COSt of pregnancy is uncertain for such diverse populations, strong scientific evidence suggests that the energy cost of pregnancy is less than previous theoretical estimations. SUMMARY Effective public health intervention aimed at improving gestational weight gain, and thus birth weight, requires an understanding of energy requirements during pregnancy. The total energy cost of pregnancy is now believed to be approximately 55,000 kcal. Prenatal energy supplementation may increase birth weight through greater rates of gestational weight gain. The impact of energy supplemen- tation appears to be influenced by the nutritional vulnerability of pregnant women and the extent to which the supplement diminishes the deficit between usual energy intakes and requirements. Gestational weight gain is a function of energy intake, although this re- lationship can be modified by the extent to which basal metabolism changes, by increased work efficiency, by compensatory reductions in physical activity, and by the composition of accumulated maternal and fetal tissue. Within the limitations of these physiologic and metabolic adaptations, gestational weight gain may be affected by changes in energy intake.
ENERGY AND ASSOCIATED WEIGHT GAIN CLINICAL APPLICATIONS . 171 Extra dietary energy is ordinarily required to meet the increased growth needs during pregnancy. · Women who remain physically active at weight-bear~ng activities during pregnancy are likely to have energy requirements higher than those of sedentary women. Because of their larger body mass, obese women require energy intakes higher than those of normal-weight women. · Gestational weight gain Is a function of energy intake, although the strength of the relationship Is confounded by intenen~ng factors. · Prenatal energy supplementation may increase birth weight through greater rates of gestational weight gain; however, the effectiveness Is con- ditional upon the nutritional vulnerability of the pregnant woman. Energy supplementation is most likely to improve the gestational weight gain of women whose usual diet Is low In calories (e.g., below about 1,900 kcal/day). REFERENCES Abraham, R., M. Campbell-Brown, A.P. Haines, W.R.S. North, V. Hainsworth, and I.R. McFadyen. 1985. Diet during pregnancy in an Asian community in Britain energy, protein, zinc, copper, fibre and calcium. Hum. Nutr.: Appl. Nutr. 39A:23-35. Adair, L S., and E. Pollitt. 1983. Seasonal variation in pre- and postpartum maternal body measurements and infant birth weights. Am. J. Phys. Anthropol. 62:325-331. Adair, L.S., E. Pollitt, and W.H. Mueller. 1983. Maternal anthropometric changes during pregnancy and lactation in a rural Taiwanese population. Hum. Biol. 55:771-787. Adair, L S., E. Pollitt, and W.H. Mueller. 1984. The Bacon Chow study eliect of nutritional supplementation on maternal weight and skinfold thicknesses during pregnancy and lactation. Br. J. Nutr. 51:357-369. Adams, S.O., G.D. Barr, and R.L. Huenemann. 1978. Effect of nutritional supplementation in pregnancy. I. Outcome of pregnancy. J. Am. Diet. Assoc. 72:144-147. Ancri, G., E.H. Morse, and R.P. Clarke. 1977. Comparison of the nutritional status of pregnant adolescents with adult pregnant women. III. Maternal protein and calorie intake and weight gain in relation to size of infant at birth. Am. J. Clin. Nutr. 30:568-572. Anderson, A S., and M.E.J. Lean. 1986. Dietary intake in pregnancy. A comparison between 49 Cambridgeshire women and current recommended intake. Hum. Nutr.: Appl. Nutr. 40A 40-48. Banerjee, B., K.S. Khew, and N. Saha. 1971. A comparative study of energy expenditure in some common daily activities of non-pregnant Chinese, Malay and Indian women. J. Obstet. Gynaecol. Br. Commonw. 78:113-116. Beat, V.A. 1971. Nutritional studies during pregnancy. II. Dietary intake, maternal weight gain, and infant size. J. Am. Diet. Assoc. 58:321-326. Bhatnagar, S., N.S. Dharamshaktu, K.R. Sundaram, and V. Seth. 1983. Effect of food supplementation in the last trimester of pregnancy and early post-natal period on maternal weight and infant growth. Indian J. Med. Res. 77:366-37Z Blackburn, M.W., and D.H. Calloway. 1974. Energy expenditure of pregnant adolescents. J. Am. Diet. Assoc. 65:24-30. Blackburn, M.W., and D.H. Calloway. 1976a. Basal metabolic rate and work energy expenditure of mature, pregnant women. J. Am. Diet. Assoc. 69.24-28.
172 NUlFRTTIONAL STATUS AND WEIGHT GAIN Blackburn, M.W., and D.H. Calloway. 1976b. Energy expenditure and consumption of mature, pregnant and lactating women. J. Am. Diet. Assoc. 69:29-37. Campbell, D.M., and I. MacGillivray. 1975. We ellect of a low calorie diet or a thiazide diuretic on the incidence of pre~clampsia and on birth-weight. Br. J. Obstet. Gynaecol. 82:572-577. Campbell-Brown, D.M. 1983. Protein energy supplements in primigravid women at risk of low birthweight. Pp. 85-100 in D.M. Campbell and M.D.G. Gillmer, eds. Nutrition in Pregnangy: Proceedings of the Tenth Study Group in the Royal College of Obstetricians and Gynaecologists, September, 1982. The Royal College of Obstetricians and Gynaecologists, London. de Benoist, B., A.A. Jackson, J. St E. Hall, and C. Persaud. 1985. Whole-body protein turnover in Jamaican women during normal pregnancy. Hum. Nutr.: Clin. Nutr. 39C: 167-179. Delgado, H., R. Martorell, E. Brineman, and R.E. Klein. 1982a. Nutrition and length of gestation. Nutr. Res. 2117-126. Delgado, ELM, V.E. Valverde, R. Martorell, and R.E. Klein. 1982b. Relationship of maternal and infant nutrition to infant growth. Early Hum. Dev. 6:273-286. Durnin, J.V.G.A. 1980. Food consumption and energy balance during pregnancy and lactation in New Guinea. Pp. 86-95 in H. Aebi and R. Whitehead, eds. Maternal Nutrition during Pregnancy and Lactation. Hans Huber, Bern. Durnin, J.V.G.A. 1986. Energy requirements of pregnancy. An integrated study in 5 countries: background and methodology. Pp. 33-38 in Nestle Foundation Annual Report 1986. Nestle Foundation, Lausanne, Switzerland. Durnin, J.V.G.A. 1987. Energy requirements of pregnancy an integration of the longitudinal data from the five-country study. Lancet 2:1131-1133. Durnin, J.V.G.A., F.M. McKillop, S. Grant, and G. Fitzgerald. 1986. Energy requirements of pregnancy. A study on 88 Glasgow women. Pp. 39-52 in Nestle Foundation Annual Report 1986. Nestle Foundation, Lausanne, Switzerland. Edozien, J.C., B.R. Switzer, and R.B. Bryan. 1979. Medical evaluation of the Special Supplemental Food Program for Women, Infants, and Children. Am. J. Clin. Nutr. 32:677-692. Emerson, K., Jr., B.N. Saxena, and E.L~ Poindexter. 1972. Caloric cost of normal pregnancy. Obstet. Gynecol. 40:786-794. Endres, J.M., K. Poell-Odenwald, M. Sawicki, and P. Welch. 1985. Dietary assessment of pregnant adolescents participating in a supplemental-food program. J. Reprod. Med. 30.10-17. Endres, J., S. Dunning, S. Poon, P. Welch, and H. Duncan. 1987. Older pregnant women and adolescents: nutrition data after enrollment in WIC. J. Am. Diet. Assoc. 87:1011-1019. FAO/WHO/UNU (Food and Agriculture OrganizationtWorld Health OrganizationtUnited Nations University). 1985. Energy and Protein Requirements. Report of a Joint FAO/VVHO/UNU Expert Consultation. Technical Report Series No. 724. World Health Organization, Geneva. 206 pp. Forsum, E., A. Sadu~kis, and J. Wager. 1985. Energy maintenance cost during pregnancy in healthy Swedish women. Lancet 1:107-108. Haworth, J.C., J.J. Ellestad-Sayed, J. King, and LA Dilling. 1980. Fetal growth retardation in cigarette-smoking mothers is not due to decreased maternal food intake. Am. J. Obstet. Gynecol. 137:719-723. Herrera, M.G., J.O. Mora, B. de Paredes, and M. Wagner. 1980. Maternal weight/height and the eRect of food supplementation dunng pregnan~ and lactation. Pp. 252-263 in H. Aebi and R. Whitehead, eds. Maternal Nutrition during Pregnancy and Lactation. Hans Huber, Bern. Hunt, I.F., N.J. Murphy, P.M. Martner-Hewes, B. Faraji, M.E. Swendseid, R.D. Reynolds, A. Sanchez, and A. Mejia. 1987. Zinc, vitamin B6, and other nutrients in pregnant women attending prenatal clinics in Mexico. Am. J. Clin. Nutr. 46:56~569. Hytten, F.E. 1980. Nutrition. Pp. 16~192 in F. Hytten and G. Chamberlain, eds. Clinical Physiology in Obstetrics. Blackwell Scientific Publications, Oxford.
ENERGY AND ASSOCL4TED WEIGHT GAIN 173 Illingworth, PJ., R.T. Jung, P.W. Howie, and T.E. Isles. 1987. Reduction in postprandial energy expenditure during pregnancy. Br. Med. J. 294:1573-1576. Iyenger, L" 1967. Erects of dietary supplements late in pregnancy on the expectant mother and her newborn. Indian J. Med. Res. 55:85-89. Kardjati, S., J.A. Kusin, and C. de With. 1988. Energy supplementation in the last trimester of pregnancy in East Java: I. Effect on birthweight. Br. J. Obstet. Gynaecol. 95:783-794. Kennedy, E.T., and M. Kotelchuck. 1984. The effect of WIC supplemental feeding on birth weight: a case-control analysis. Am. J. Clin. Nutr. 40:579-585. King, J.C., S.H. Cohenour, D.H. Calloway, and H.N. Jacobson. 1972. Assessment of nutritional status of teenage pregnant girls. I. Nutrient intake and pregnancy. Am. J. Clin. Nutr. 25:916-925. King, J.C., M.N. Bronstein, W.L. Fitch, and J. Weininger. 1987. Nutrient utilization during pregnancy. World Rev. Nutr. Diet. 52:71-142. Kramer, M.S. 1987. Determinants of low birth weight: methodological assessment and meta-analysis. Bull. W.H.O. 65:663-737. Langhoff-Roos, J., G. Lindmark, E. Kylberg, and M. Gebre-Medhin. 1987. Energy intake and physical activity during pregnancy in relation to maternal fat accretion and infant birthweight. Br. J. Obstet. Gynaecol. 94:1178-1185. Lawrence, M., and R.G. Whitehead. 1988. Physical activity and total energy expenditure of child-bearing Gambian village women. Eur. J. Clin. Nutr. 42:145-160. Lawrence, M., J. Singh, F. Lawrence, and R.G. Whitehead. 1985. The energy cost of common daily activities in African women: increased expenditure in pregnancy? Am. J. Clin. Nutr. 42:753-763. Lawrence, M., F. Lawrence, WA. Coward, T.J. Cole, and R.G. Whitehead. 1986. Energy expenditure and energy balance during pregnant and lactation in The Gambia. Pp. 77-103 in Nestle Foundation Annual Report 1986. Nestle Foundation, Lausanne, Switzerland. Lechtig, A., J.P. Habicht, H. Delgado, R.E. Klein, C. Yarbrough, and R. Martorell. 1975a. Effect of food supplementation during pregnancy on birthweight. Pediatrics 56:508-520. Lechtig A., C. Yarbrough, H. Delgado, J.P. Habicht, R. Martorell, and R.E. Klein. 1975b. Influence of maternal nutrition on birth weight. Am. J. Clin. Nutr. 28:1223-1233. Lechtig, A., R. Martorell, H. Delgado, C. Yarbrough, and R.E. Klein. 1978. Food supplementation during pregnancy, maternal anthropometry and birth weight in a Guatemalan rural population. J. flop. Pediatrics. 24:217-222. Loris, P., KG. Dewey, and K. Poirier-Brode. 1985. Weight gain and dietary intake of pregnant teenagers. J. Am. Diet. Assoc. 85:1296-1305. Mardones-Santander, F., P. Rosso, A. Stekel, E. Ahumada, S. Llaguno, F. Pizarro, J. Salinas, I. Vial, and r Walter. 1988. ERect of a milk-based food supplement on maternal nutritional status and fetal growth in underweight Chilean women. Am. J. Clin. Nutr. 47:413-419. McDonald, E.C., E. Pollitt, W. Mueller, A.M. Hsueh, and R. Sherwin. 1981. The Bacon Chow study: maternal nutritional supplementation and birth weight of offspring. Am. J. Clin. Nutr. 34:2133-2144. Metcoff, J., P. Costiloe, W.M. Crosby, S. Dutta, H.H. Sandstead, D. Milne, C.E. Bodwell, and S.H. Majors. 1985. Effect of food supplementation (WIC) during pregnant on birth weight. Am. J. Clin. Nutr. 41:933-947. Mora, J.O., B. de Paredes, M. Wagner, Lo de Navarro, J. Suescum, N. Christiansen, and M.G. Herrera. 1979. Nutritional supplementation and the outcome of pregnancy. I. Birth weight. Am. J. Clin. Nutr. 32:455 462. Nagy, L~E., and J.C. King. 1983. Energy expenditure of pregnant women at rest or walking self-paced. Am. J. Clin. Nutr. 38:369-376. Nagy, L.E., and J.C. King. 1984. Postprandial energy expenditure and respiratory quotient during early and late pregnancy. Am. J. Clin. Nutr. 40:1258-1263.
174 NUTRITIONAL STATUS AND WEIGHT GAIN NRC (National Research Council). 1989. Recommended Dietary Allowances, 10th ed. Report of the Subcommittee on the Tenth Edition of the RDAs, Food and Nutrition Board, Commission on Life Seienees. National Academy Press, Washington, D.C. 284 PP. Papoz, L., E. Esehwege, G. Pequignot, J. Barrat, and D. Schwartz. 1982. Maternal smoking and birth weight in relation to dietary habits. Am. J. Obstet. Gyneeol. 142:87~876. Paul, AA., E.M. Muller, and R.G. Whitehead. 1979. The quantitative effects of maternal dietary energy intake on pregnancy and lactation in rural Gambian women. Trans. R. Soe. Trop. Med. Hyg. 73:686 692. Pieone, T.A., L.H. Allen, M.M. Sehramm, and P.N. Olsen. 1982a. Pregnancy outcome in North American women. I. Eliects of diet, cigarette smoking, and psychological stress on maternal weight gain. Am. J. Clin. Nutr. 36:1205-1213. Picone, T.A., L^H. Allen, P.N. Olsen, and M.E. Ferris. 1982b. Pregnancy outcome in North American women. II. Effects ol: diet, cigarette smoking, stress, and weight gain on placentas, and on neonatal physical and behavioral characteristics. Am. J. Clin. Nutr. 36:1214-1224. Prentice, AM., W.A. Coward, H.L~ Davies, P.R. Murgatroyd, AK. Black, G.R. Goldberg, J. Ashford, M. Sawyer, and R.G. Whitehead. 1985. Unexpectedly low levels of energy expenditure in healthy women. Lancet 1:1419-142Z Prentice, A.M., TO. Cole, F.A. Foord, W.H. Lamb, and R.G. Whitehead. 1987. Increased birthweight after prenatal dietary supplementation of rural African women. Am. J. Clin. Nutr. 46:912-925. Roberts, S.B., A.A. Paul, T.J. Cole, and R.G. Whitehead. 1982. Seasonal changes in activity, birth weight and lactational performance in rural Gambian women. Itans. R. Soc. Stop. Med. Hyg. 76:668-678. Rush, D. 1981. Nutritional services during pregnancy and birthweight: a retrospective matched pair analysis. Can. Med. Assoe. J. 125:567-576. Rush, D., Z. Stein, and M. Susser. 1980. A randomized controlled trial of prenatal nutritional supplementation in New York City. Pediatrics 65:683-697. Rush, D., N.L. Sloan, J. Leighton, J.M. Alvir, D.G. Horvitz, W.B. Seaver, G.C. Garbowski, S.S. Johnson, R.A. Kulka, M. Holt, J.W. Devore, J.T. Lynch, M.B. Woodside, and D.S. Shanklin. 1988. The National WIC Evaluation: evaluation of the Special Supplemental Food Program for Women, Infants, and Children. V. Longitudinal study of pregnant women. Am. J. Clin. Nutr. 48:439-483. Seitchik, J. 1967. Body composition and energy expenditure during rest and work in pregnancy. Am. J. Obstet. Gynecol. 97:701-713. Sparks, J.W., J.R. Girard, and F.C. Battaglia. 1980. An estimate of the caloric requirements of the human fetus. Biol. Neonate 38:113-119. Stein, A, and M. Susser. 1975a. The Dutch famine, 1944-1945, and the reproductive process. I. Effects on six indices at birth. Pediatr. Res. 9 70-76. Stein, A, and M. Susser. 1975b. The Dutch famine, 1944-1945, and the reproductive process. II. Interrelations of calorie rations and six indices at birth. Pediatr. Res. 9:76-83. Tafari, N., R.L~ Naeye, and ~ Gobezie. 1980. Elieets of maternal undernutrition and heavy physical work during pregnancy on birth weight. Br. J. Obstet. Gynaeeol. 87:222-226. Thomson, A.M. 1959. Diet in pregnancy. 3. Diet in relation to the course and outcome of pregnancy. Br. J. Nutr. 13:509-525. Thongprasert, K., and A. Valyasevi. 1986. The energy requirements of pregnant rural Thai women. Pp. 105-112 in Nestle Foundation Annual Report 1986. Nestle Foundation, Lausanne, Switzerland. Thongprasert, K., V. Tanphaichitre, ~ Valyasevi, J. Kittigool, and J.V.G.N Durnin. 1987. Energy requirements of pregnancy in rural Thailand. I~ncet 2:1010-1012. Tontisirin, K, U. Booranasubkajorn, ~ Hongsumarn, and D. Thewtong. 1986. Formulation and evaluation of supplementary foods for Thai pregnant women. Am. J. Clin. Nutr. 43:931-939. Tordn, B., J. McGuire, and R.D. Mendoza. 1982. Energy cost of activities and tasks of women from a rural region of Guatemala. Nutr. Res. 2:127-136.
ENERGY AND ASSOCIATED VVEIGHT GAIN 175 Truswell, A.S., S. Ash, and J.R. Allen. 1988. Energy intake during pregnancy. Lancet 1:49. Tuazon, P.A.G., C.V.C. Barba, J.M.^ van Raaij, M.E.M. Peek, and J.G.AJ. Hautvast. 1986. Maternal energy requirements during pregnancy of rural Philippine women. Pp. 113-146 in Nestle Foundation Annual Report 1986. Nestle Foundation, Lausanne, Switzerland. Ibazon, M.NG., J.M.~ van Raaij, J.G.^J. Hautvast, and CV.C Barba. 1987. Energy requirements of pregnancy in the Philippines. Lancet 2:1129-1131. van Raaij, J.M.A., M.E.M. Peek, and J.G.AJ. Hautvast. 1986. Maternal energy requirements in pregnancy in Dutch women. Pp. 5~75 in Nestle Foundation Annual Report 1986. Nestle Foundation, Lausanne, Switzerland. van Raaij, J. M.A. , S. . H. Vermaat-Miedema , C M. Schonk, M. E.M. Peek, and J.G.AJ. Hautvast. 1987. Energy requirements of pregnancy in The Netherlands. Lancet 2:953-955. Viegas, O.^C, P.H. Scott, TJ. Cole, P. Eaton, P.G. Needham, and B.N Wharton. 1982. Dietary protein energy supplementation of pregnant Asian mothers at Sorrento, Birmingham. II. Selective during third trimester only. Br. Med. J. 285:592-595.
