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May 2007: 233–245 Special Article Age and Gender as Factors in the Distribution of Global Micronutrient Deficiencies Patrick Webb, PhD, Chizuru Nishida, PhD, Ian Darnton-Hill, MBBS, MPH Although micronutrient deficiency is a global prob- lem, the burden is not evenly shared within affected households. This review suggests that there are im- portant non-linearities in relationships among food intake, sharing, and caring behavior within the house- hold. Since micronutrient status relates to interactions among biological, social, behavioral, economic, and environmental processes, outcomes are not always predictable by age, gender, or location. Understand- ing such variability is crucial to identifying appropri- ate solutions. This review represents an exploratory first step toward unmasking population-specific vari- ations that are important for better understanding the nature of micronutrient deficiencies and for improving the focus of public health action. Key words: age, deficiency diseases, gender, micro- nutrients, public health © 2007 International Life Sciences Institute doi: 10.1301/nr.2007.may.233–245 INTRODUCTION It is well known that although important micronu- trient deficiencies are a global problem, the burden is not evenly shared among or within countries. Less well known is the fact that deficiencies are not evenly shared even within households. This review explores variability in micronutrient deficiency conditions by gender and age in diverse developing country settings. We argue that unmasking demographic diversity in deficiency out- comes can generate a better understanding of the nature of global problems and hence improve the targeting and effectiveness of public health actions. The focus here is on vitamin A, iron, and iodine, but other minerals and trace elements are included where relevant. Published papers were found with the use of specialized Web-based search engines (such as Medline), searches through numerous journals (such as The Lancet, The European Journal of Clinical Nutrition, Social Sci- ence Medicine, The Journal of Nutrition, etc.), and search engines relevant to non-nutrition domains (such as CABI), which deal with agricultural economics and other disciplines. Of almost 400 papers considered, 72 studies were retained for in-depth review based on: 1) presentation of data disaggregated by gender and/or age; 2) sound methodology; and 3) peer-reviewed output. An effort was made to achieve geographic and linguistic coverage. Roughly two-thirds of the studies presented are “clinical” studies based on laboratory assessment or evaluation of public interventions; the rest are secondary analyses of national surveys, anthropological investiga- tions, and household economic surveys. This review makes no claim to be an exhaustive compilation. It is not a meta-analysis of primary data, nor is it an exhaustive review of all extant studies on micro- nutrient deficiencies; it represents a first critical analysis of the data from a particular “lens.” ENTERING THE HOUSEHOLD It is paradoxical that while nutrition science offers increasingly sophisticated age- and gender-specific di- etary recommendations for micronutrients, knowledge of who is most affected by what deficiencies, when, and where is still limited. Although statistics on the global prevalence of deficiencies are widely circulated, most represent extrapolations based on sparse information. Much effort has gone into aggregating small surveys up to the national level so that a sample of, for example, 423 children 0 to 60 months of age in Zambia can be compared with 22,335 children 4 to 72 months old in Bangladesh. However, much less effort has been directed Dr. Webb is with the Friedman School of Nutrition Science and Policy, Tufts University, Boston, Massa- chusetts; Dr. Nishida is with the Department of Nutri- tion for Health and Development (NHD), World Health Organization (WHO), Geneva, Switzerland; Dr. Darn- ton-Hill is with the Nutrition Section, UNICEF New York, and the Institute of Human Nutrition, Columbia University, New York. Please address all corresondence to: Dr. Patrick Webb, Friedman School of Nutrition Science and Policy, 150 Harrison Ave., Boston, MA 02111; Phone: 617-636-3779; Fax: 617-636-3781; E-mail: [email protected]. 233 Nutrition Reviews, Vol. 65, No. 5

Age and Gender as Factors in the Distribution of Global Micronutrient Deficiencies

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Page 1: Age and Gender as Factors in the Distribution of Global Micronutrient Deficiencies

May 2007: 233–245Special Article

Age and Gender as Factors in the Distribution of GlobalMicronutrient DeficienciesPatrick Webb, PhD, Chizuru Nishida, PhD, Ian Darnton-Hill, MBBS, MPH

Although micronutrient deficiency is a global prob-lem, the burden is not evenly shared within affectedhouseholds. This review suggests that there are im-portant non-linearities in relationships among foodintake, sharing, and caring behavior within the house-hold. Since micronutrient status relates to interactionsamong biological, social, behavioral, economic, andenvironmental processes, outcomes are not alwayspredictable by age, gender, or location. Understand-ing such variability is crucial to identifying appropri-ate solutions. This review represents an exploratoryfirst step toward unmasking population-specific vari-ations that are important for better understanding thenature of micronutrient deficiencies and for improvingthe focus of public health action.

Key words: age, deficiency diseases, gender, micro-nutrients, public health© 2007 International Life Sciences Institute

doi: 10.1301/nr.2007.may.233–245

INTRODUCTION

It is well known that although important micronu-trient deficiencies are a global problem, the burden is notevenly shared among or within countries. Less wellknown is the fact that deficiencies are not evenly sharedeven within households. This review explores variabilityin micronutrient deficiency conditions by gender and agein diverse developing country settings. We argue that

unmasking demographic diversity in deficiency out-comes can generate a better understanding of the natureof global problems and hence improve the targeting andeffectiveness of public health actions.

The focus here is on vitamin A, iron, and iodine, butother minerals and trace elements are included whererelevant. Published papers were found with the use ofspecialized Web-based search engines (such as Medline),searches through numerous journals (such as The Lancet,The European Journal of Clinical Nutrition, Social Sci-ence Medicine, The Journal of Nutrition, etc.), andsearch engines relevant to non-nutrition domains (suchas CABI), which deal with agricultural economics andother disciplines. Of almost 400 papers considered, 72studies were retained for in-depth review based on: 1)presentation of data disaggregated by gender and/or age;2) sound methodology; and 3) peer-reviewed output. Aneffort was made to achieve geographic and linguisticcoverage. Roughly two-thirds of the studies presentedare “clinical” studies based on laboratory assessment orevaluation of public interventions; the rest are secondaryanalyses of national surveys, anthropological investiga-tions, and household economic surveys.

This review makes no claim to be an exhaustivecompilation. It is not a meta-analysis of primary data, noris it an exhaustive review of all extant studies on micro-nutrient deficiencies; it represents a first critical analysisof the data from a particular “lens.”

ENTERING THE HOUSEHOLD

It is paradoxical that while nutrition science offersincreasingly sophisticated age- and gender-specific di-etary recommendations for micronutrients, knowledge ofwho is most affected by what deficiencies, when, andwhere is still limited. Although statistics on the globalprevalence of deficiencies are widely circulated, mostrepresent extrapolations based on sparse information.Much effort has gone into aggregating small surveys upto the national level so that a sample of, for example, 423children 0 to 60 months of age in Zambia can becompared with 22,335 children 4 to 72 months old inBangladesh. However, much less effort has been directed

Dr. Webb is with the Friedman School of NutritionScience and Policy, Tufts University, Boston, Massa-chusetts; Dr. Nishida is with the Department of Nutri-tion for Health and Development (NHD), World HealthOrganization (WHO), Geneva, Switzerland; Dr. Darn-ton-Hill is with the Nutrition Section, UNICEF NewYork, and the Institute of Human Nutrition, ColumbiaUniversity, New York.

Please address all corresondence to: Dr. PatrickWebb, Friedman School of Nutrition Science andPolicy, 150 Harrison Ave., Boston, MA 02111;Phone: 617-636-3779; Fax: 617-636-3781; E-mail:[email protected].

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toward disaggregating survey data by age and genderwith a view to clarifying interactions among nutrients fordifferent individuals in different environments.

This is an important gap given that the developmentliterature is so attuned to age and gender biases. House-holds are not unitary enterprises that maximize welfarefor all members. The success of public policy or inter-ventions often depends on allowing for trade-offs inresource access among different individuals. This appliesto nutrients as much as it does to income or productiveassets. Researchers in India,1 Indonesia,2 Nepal,3,4

Peru,5,6 and the Philippines7 have explored multiple age,gender, and status differences in nutrient access or nu-tritional status, but most have focused narrowly on youngchildhood or maternal outcomes. For example, of areview of over 500 studies on anemia, only 39 includedadolescents and a mere handful considered the status ofmale adults or school-aged children.8 In the currentreview, almost two-thirds of the studies are principally, ifnot exclusively, concerned with the condition of infantsand mothers alone.

Such a focus derives from an understanding of thephysiological demands facing pregnant and lactatingmothers, and of the dual dangers to infants of earlymortality or “early trauma-later deficit.” Even these cat-egories can obscure more than they reveal. Depending onthe nutrients concerned and prevailing policies of inter-national agencies, young children can be specified as“children under five years of age,”9 “children from 6 to36 months of age,”10 or “children 6-24 months ofage.”11,12 The focus on “mothers” is similarly diverse inthat it can refer to lactating mothers or to adult womenwith offspring of any age.2

The paucity of data disaggregated beyond youngchildren and mothers makes it difficult to assess states ofsufficiency among all household members and can evendeflect attention from underlying causes. For example,measuring iron deficiency anemia among mothers inisolation from problems of other household memberscarries two risks: 1) missing important deficiencies af-fecting adolescents, the elderly, school-aged boys, non-pregnant adult women, and working men; and 2) incor-rectly interpreting a deficiency—that is, mistakenlyattributing a mother’s deficiency to gender bias or lowstatus of women when it may be a problem that affects allhousehold members. Thus, deficiencies of mothers andinfants need to be addressed in the context of overallhousehold conditions if a net gain is to be sustainable.

WHO SUFFERS WHAT MICRONUTRIENTDEFICIENCIES AND WHEN?

Three broad generalizations are often repeated in themicronutrient literature. The first is that boys are “at

greater risk of xerophthalmia (night blindness and Bitot’sspots) than are girls.”13 The second is that females,especially women of reproductive age, suffer a higherprevalence of iron deficiency than men.8 The third is that“girls have a higher prevalence [of iodine deficiency]than boys,” especially from adolescence onwards.13

These statements have served as a vital platform forinforming policy targets and programming decisionsthrough the late 20th century, but to what extent are theyaccurate representations that can usefully guide action toresolve such deficiencies? We use these merely as illus-trations of the problem.

Vitamin A

It has been reported that vitamin A deficiency is upto 10 times more common in males than in females.14

However, most studies used to illustrate this point datefrom 1960 to 1982; more recent empirical support forsuch a generalization is not strong. Of 49 studies thatdeal with vitamin A compiled here, less than one-thirdreport that boys have a lower vitamin A status than girls(Tables 1 and 2). This seems to hold for all parts of theworld; no region has a majority of studies showing boysto be statistically significantly more vitamin A deficientthan girls. For example, although one study in Indonesiashows that boys have a higher prevalence than girls,15

another from the same country (included in a meta-analysis) finds no significant difference in the risk ofxerophthalmia by gender.16 Similarly, boys from oneEthiopian province displayed significantly lower retinollevels than girls,17 but a different study found no differ-ence in mean serum retinol levels by gender.18 Whileboys in school in South Africa were found to have aserum retinol level below the recommended level,19 asample taken from South-African hospitals found nosignificant difference by gender.20

Consequently, the a priori assumption that boys arealways more at risk than girls requires revisiting. Of the35 studies in which boys do not have more deficienciesthan girls, 25 (71%) found no significant differences.While numerous studies do report a higher relative riskor prevalence of vitamin A deficiency for one genderover the other (in Indonesia,16 Malawi,16 Thailand,21 andZambia16), in no case was the difference statisticallysignificant.

This raises two important issues relating to surveydesign and analysis. First, there are difficulties in com-paring methods. Of the 15 studies where vitamin Adeficiency was greater among boys, only four were basedon biochemical analysis of serum; the rest were based onestimations of food intake or on clinical examination forocular signs. One study found that male neonates havesignificantly lower cord plasma levels of vitamin A than

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girls22; another found that adult women have a lower-intake of green leafy vegetables than men in a 24 hour-recall food survey.3 However such findings are not nec-essarily indicative of the same type or degree ofdeficiency problem, and different confounders may applyto one method more than to another. As a result, greatcare is needed in interpreting deficiency outcomes basedon differing approaches. More sensitivity analysis andcross-validation of techniques are required.

Second, there is an issue of age categorization. Asample of Thai children showed that there was no dif-ference in vitamin A status by gender when consideringmean values.21 That is, the mean retinol level for boys(all ages) was 0.72 �mol/L compared with 0.76 �mol/Lfor girls (not statistically significant). However, a highlysignificant difference did apply to standard deviationsaround the mean (for both retinol and ferritin). Indeed,deviation from the mean was not only higher for girlsthan boys (showing greater vitamin A deficiency amongcertain groups of girls), but it occurred in some ages andlocations more than in others. That is, rural boys andgirls 3 to 6 years of age had significantly lower serumretinol levels than urban children, but rural children ofother age groups did not show much difference from theirurban counterparts. In other words, aggregating age groupscan obscure important differences in outcomes.

Similarly, while beta-carotene levels were withinnormal ranges for both boys and girls 60 to 72 months ofage in Ethiopia, they were significantly lower for allchildren less than 23 months old, in particular for boys.18

In South Africa, 11- to 14-year-old boys were found toconsume more dietary retinol equivalents than 6- to10-year-old boys.19 Both cases illustrate that an averagedstatistic for “boys” obscures age differentiation, and alack of statistical significance may be due to a maskingof differential outcomes by gender and age.

Thus, aggregation of age and gender in an undiffer-entiated sample means obscures demographic dynamicsthat may be of concern. One danger is that there may bea large-scale underestimation of the magnitude of theglobal vitamin A deficiency due to a focus on youngerchildren (while young girls definitely face serious phys-iological risks of deficiencies, men, boys, and femaleadolescents all suffer this deficiency to varying, largelyunmeasured, degrees). Also, where national surveys arenot available, multiplication factors are usually derivedfrom subnational surveys and applied to the young childpopulation. This approach has been criticized as overes-timating the problem in preschoolers. However, if onegender is more at risk than the other, then there may alsobe overestimation of the magnitude of the problem, sinceonly half the child population may be involved. Withoutappropriately disaggregated data that are representativeof whole populations we cannot know.

Iron Deficiency and Iron Deficiency Anemia

Iron deficiency and anemia also have complex age/gender specificities. On the one hand, the search continuesfor simple, functional measures of iron status that allowconsideration of interactions among iron and other micro-nutrients for different age and gender categories.23 On theother hand, it is increasingly accepted that an integratedapproach is required to tackle iron deficiency, includingdietary diversification, fortification, and supplementationintegrated into programs to control intestinal parasites andmalaria, as well as environmental interventions.23,24

There is a well-documented higher risk of anemia inwomen of reproductive age due to menstruation andrepeated pregnancies,8 with pregnant women and chil-dren under 5 years of age at greatest risk of being irondeficient when anemia is used as the major clinicalmanifestation.11 Nevertheless, anemia is also foundamong men (where its impact on labor productivity canbe serious) and children between 5 and 18 years of age,depending on the environmental and disease profiles ofcommunities. For example, although little difference wasfound in iron intake between 6- to 10-year-old South-African boys and girls, 46% of boys had low serumlevels compared with 33% for girls, and 36% of boys hadlow transferrin saturation levels (defined as �16%) com-pared with only 17% of the girls.19 In 11- to 14-year-olds, there was no statistical difference in dietary ironintake, but more boys were anemic. Following menarche,adolescent females often do not consume sufficient di-etary iron to offset menstrual losses, so a peak of irondeficiency occurs in this age group.

In Thailand, there was no significant differencebetween boys and girls (1 to 8 years of age) in terms ofhemoglobin, hematocrit, serum iron, transferritin, ortransferritin saturation levels—only ferritin was different(higher among girls than boys).21 Similarly, in Haiti,boys 2 to 5 years of age had a higher prevalence ofanemia (42%) than girls (36%), although there was nostatistically significant difference in terms of ferritin ortransferritin levels.25 In Indonesia, a significant declinein hemoglobin was found among boys relative to girlsduring the late-1990s crisis,26 and a separate study foundthat although both boys and girls both suffered a decline,boys recovered significantly more quickly post-crisisthan girls.27

But are “fathers” and “mothers” alike in all house-holds? Information allowing comparisons among adultmen or between adult men and adult women is scarce.The rate of anemia among elderly males in Jakarta wasfound to be 9%, which is as high as the rate among maleschoolchildren, compared with 13% for elderly women.2

In the Philippines, while all adult men (“fathers”) ex-

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Table 1 (Part 1). Studies Reporting Intra-Household Variability in Micronutrient DeficienciesGeographic

Location Study Sample Size/TypeSurvey

Methods* Findings†

Asia

Nepal (rural) Shankar et al.(1996) and(1998)

162 households with1–6-year child;village case-control study

FFQs (weekly),Clinicalcohorts(1996)

More xerophtalmia in girls 3–4 ythan boys, but not for otherage—stat. sig. not reported.Child (either gender) eatingwith man more risk of VADD.

Nepal (rural) Gittelsohn(1991)

767 adults andchildren in 115households (in 6villages)

WF, FFQ,Qualitative

Adult women more deficient incarotene intake and vit. C. Nosig. diff. by child gender.

Nepal (rural) Gittelsohn etal. (1997)

105 households,adults andchildren. Village-based case-control

24HR, FFQQualitative

Male gender and age bestpredictors of carotene, vit. Cand iron intake. Adult womenmost deficient but age biasdiffers by nutrient.

Nepal (rural) Ohno et al.(1998)

245 people 10–72 yin two villages.Stratified random.

24HR,Biochemical

Overall females all ages sig.,lower serum iron than males.In one village, women also sig.lower niacin, in the otherwomen lower calcium.

Indonesia(urban)

Schultink etal. (1996)

1 child (2–5 y) plusparents in 40households.

24HR, 3DR,WF

Poor women and men inadequateintake vit. A and ironcompared with richer adults.Adolescent girls 10 timeshigher prevalence anemia thanboys.

Indonesia(rural)

Muhilal et.al. (1994)

18,508 children �6y in 15 provinces

Clinical Bitot’s spot sig. more in boys(twice the prevalence as girls).Same for night-blindness.

Indonesia(rural)

Block et al.(2004)

108,000 children �6y in C. Java.

Clinical Boys and girls sufferedhemoglob. fall during mid-1990s crisis, but boys’recovery sig. faster.

India (rural) Kapil et al.(1996)

1277 adults 24HR Zinc intake 70% of RDA formen and only 50% of RDA forwomen (non preg./non-lac.).But, iron intake much lowerfor women.

India (rural) Levinson(1974)

496 children 6–24 m 24HR Girls lower intake vit A thanboys, but higher caste girlsbetter iron intake than othergirls or boys.

India(rural/urban)

MHRD(1996a,1996b)

Varying state-levelsample sizes (for10 states) all agescombined

Clinical Prevalence Bitot’s spot varies bygender and state. But cornealxerosis mostly higher in boysin all states.

*FFQ, Food frequency questionnaire. 3DR, Three-day dietary recall questionnaire. 24HR, 24-hour recall of foods consumed. WF,weighed foods methods. ANT, anthropometry. Biochemical, laboratory analyses (blood, serum, etc.). Qualitative, direct observationand other qualitative techniques.†Abbreviations: diff., difference; stat., statistical; sig., significant; SD, standard deviation.

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ceeded recommended dietary allowances for iron con-sumption, women (“mothers”) did not.7

An important distinction among adults also relates topoverty. A strong correlation was found between highserum ferritin/hemoglobin levels and place of habitation;

that is, adults in Johannesburg were much less likely tobe iron deficient than those living in the poor area ofSoweto, suggesting that anemia in Soweto may be linkedmore to diseases and socioeconomic deficiencies than todeficiencies in iron intake.28

Table 1 (Part 2). Studies Reporting Intra-Household Variability in Micronutrient DeficienciesGeographic

Location Study Sample Size/TypeSurvey

Methods* Findings†

India (rural) Pushpammaet al.(1982)

1435 members of 280households

WF, ANT Adolescent and adult women sig.lower intake iron. No sig. diffby age/gender for vit. A, orvit. C.

Thailand(rural, urban)

Bloem et al.(1989a)

1772 children 1–8 y,of which 863 fullbiochemical data.

ANT, clinical,biochemical

Girls (1–8 y) sig. better retinol,retinol-binding protein andferritin than boys of same age.

China(rural, urban)

Tian et al.(1996)

3652 adults 15–64 y,representative,stratified random

3DR, WF24HR

Rural women lower intake of 14micronutrients than men, andlower than urban women.

Philippines(rural)

Klemm et al.(1993)

11,378 children, 6–83m, random.

ANT, clinical,FFQ.

Mild xerophthalmia highestamong boys in 4–6 y cohort.

Philippines(rural)

Chula et al.(1980)

Children 3–6 y in 58households

WF Boys above RDA most nutrients,no sig. diff. in sibling order.

Kiribati(national)

Schaumberget al.(1996)

1428 0–6 y children(case-control)

Clinical, FFQ Boys, post-weaning, sig. higherrates of xerophthalmia.

Kiribati (rural) Danks et al.(1992)

150 0–7 y childrenfrom 3 villages

Clinical Boys sig. higher Bitot’s spot andnight-blindness.

Bangladesh(rural)

Bouis et al.(1997)

Children and adultsfrom 590households

WF, 24HR Male adequacy of iron, vit. Aand vit C higher than women.Boys/girls 13–18 y leastadequacy.

Bangladesh(urban, rural)

Hussain andKvale(1996)

248 children 2–15 y,case-control

Clinical, FFQbiochemical

Serum retinol sig. lower for girls.Ages 4–6 y worst bothgenders.

Bangladesh(urban)

Stanton et al.(1986)

Children 0–14 y incase-control study

FFQ, clinical Boys, of older cohorts (6 yversus 3 y) sig. morexerophtalmia.

Pakistan(urban)

Lindblad etal. (1998)

Infants 0–6 m andadults

Clinical,biochemical

Women (pregnant and non-pregnant) sig. lower serumretinol than men. No sig. diff.for infants.

Malaysia(rural, urban)

Ismail(1989)

Children 4–13 y andadults 14–59 y

3DR, weighedfood

Women (20–59 y) lower vit. Aintake than men, few sig. diffs13–19 y by gender for iron/calcium

Vietnam(national)

Giay et al.(1988)

23,782 children 0–59m

Clinical Boys generally, sometimes sig.,worse than girls in nightblindness, Bitot’s spot, totalrate.

*FFQ, Food frequency questionnaire. 3DR, Three-day dietary recall questionnaire. 24HR, 24-hour recall of foods consumed. WF,weighed foods methods. ANT, anthropometry. Biochemical, laboratory analyses (blood, serum, etc.). Qualitative, direct observationand other qualitative techniques.†Abbreviations: diff., difference; stat., statistical; sig., significant; SD, standard deviation.

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Table 1 (Part 3). Studies Reporting Intra-Household Variability in Micronutrient DeficienciesGeographic

Location Study Survey Sample Size/Type Methods* Findings†

Asia (continued)

Papua NewGuinea(rural)

Simon et al.(1990)

Adolescents aged 10–19 ySample size nospecified

Clinical Female prevalence goiter (total rate)double that of men.

Micronesia(national)

Lloyd-Puryearet al. (1991)

448 children 3–7 y Clinical Boys twice rate Bitot’s spot, andhigher night-blindness, versusgirls.

West Asia/North Africa

SaudiArabia(urban)

Tolba et al.(1998)

105 neonates randomlyselected in hospital

Biochemical Boys neonates sig. lower cordplasma levels of vit. A than girls.

Yemen(rural)

Rosen et al.(1996)

2438 children stratifiedcluster sample

12–60 m,Clinical

Boys sig. more nightblindness andBitot’s spot than girls. Allchildren 4–5 y sig. more at riskthan �4 y.

Egypt(rural)

El-Sayed et al.(1998)

6750 children 8–18 y,2-stage cluster sample

Clinical,biochemical

Girls sig. more goiter (iodinedeficiency) than boys).

Morocco(national)

MSP (1995) 1094 adults over 18 y.(National samplesurvey)

Biochemical Pregnant women �4 times morelikely to be anemic than adultmen

Sub-Saharan Africa

SouthAfrica(rural)

Badenhorst etal. (1993)

296 children, 6–14 y.Random sample inElementary schools.

24HR, ANT,Clinical,Biochemical.

Girls 6–10 y higher intake thanboys vitamin A, C, Ca, K andsugar. No diff. in iron. But, girls11–14 y lower intake vit. A, B12,and C. SDs often greater foryounger cohorts.

SouthAfrica(rural)

Tichelaar et al.(1994)

296 children, 6–14 y.Random from clinics

Biochemical Diet imbalance of n-3/n-6 fattyacids seems linked tomalnutrition. Boys 7–12 y higherimbalance.

Madagascar(rural)

Hardenbergh(1997)

619 children 0–17 y plusadults, random.

ANT, 24HR,WF

Girls aged 6y lower vit A. in dryseason (but not iron or girls 7–9y) In wet season girls also lowerbut intake meets RDA. Girls andboys 10–17 y all deficient in iron.

Ethiopia(rural)

Tafesse et al.(1996)

147 children 6–72 m,Arssi province

Clinical,biochemical

Serum retinol deficiency and Bitot’sspot sig. higher for boys thangirls

Ethiopia(rural)

Wolde-Gebrielet al. (1991)

6636 children aged 6–72m, stratified sample byagroecology

Clinical,ANT,biochemical

No sig. diff. by age or gender inserum retinol values, but boys�12 m sig. higher Bitot’s spotand xerosis.

Ethiopia(national)

Wolde-Gebrielet al. (1992)

35,635 national surveyfrom 1980/81

Clinical Girls/women higher iodinedeficiency. Diff. increases withage from 6 y on.

*FFQ, Food frequency questionnaire. 3DR, Three-day dietary recall questionnaire. 24HR, 24-hour recall of foods consumed. WF,weighed foods methods. ANT, anthropometry. Biochemical, laboratory analyses (blood, serum, etc.). Qualitative, direct observationand other qualitative techniques.†Abbreviations: diff., difference; stat., statistical; sig., significant; SD, standard deviation.

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Table 1 (Part 4). Studies Reporting Intra-Household Variability in Micronutrient Deficiencies

Geographic Location Study Sample Size/TypeSurvey

Methods* Findings†

Sub-Saharan Africa (continued)

Ethiopia (urban/rural) De Sole et al.(1987)

2647 children 6–72 m,cluster, case-control

Clinical,biochemical

Bitot’s spot sig. higher in boysthan in girls (p � 0.03).

Tanzania (rural) Tanner andLukmanji(1987)

All inhabitants of 32households.

FFQ, 24HR,WF

Iron sig. low among infants ofboth genders, but girls 10–16 y and women sig. lessthan boys/men.

Sudan (rural) Nestel et al.(1993)

29,615 children 6–72 min 5 districts ofKhartoum and Geziraprovinces

Clinical, ANTFFQ

Risk of xerophthalmia sig.higher for boys than girls,and increased with age andpoverty.

Liberia (rural) Lemaire(1993)

1,707 adults (more thanhalf women)

Clinical Females three times highergoiter prevalence than men(all grades)

Latin AmericaVenezuela(national)

Layrisse etal. (1996)

�1200 (in 3 rounds)Random samplesfrom schools, clinics,homes.

Biochemical Girls aged 11 y sig. more irondeficient than boys. Girls�15 y generally moredeficient.

Mexico (urban) Backstrand etal. (1997)

91 school children (inCRSP study)

ANT, 24HR,weighing

School-age girls sig. lowerintake of vitamins E, B6and iron, zinc, thiamine,niacin.

Chile (urban) Ruz et al.(1997)

98 children in day-carecentres, 27–50 m old.Double-blindsupplmtn.

Biochemical Boys in zinc supplementalgroup sig. higher growththan placebo group, but noeffect for girls in eithergroup.

Chile (rural/urban) Muzzo(1986)

1015 children 6–18 y inSantiago-Temuco

Clinical Girls twice the rate of iodinedeficiency than boys.

Peru (rural) Imai et al.(1997)

91 adults aged �19 yand 100 children

7DR,biochemical

Women 25–50 sig. higher riskof selenium deficiency interms of %RDA bybodyweight. Only girls 7–10closer to RDA than boys.

Industrialized Countries

Canada (urban) Wolever etal. (1997)

700 people �9 y fromOjibwa-Cree tribe

24HR, WFBiochemical

Women sig. lower iron, niacin,and folate intake than men.

UK (urban) Nelson(1986)

343 people all ages in797 households inCambridge

DR, WF Women �18 y sig. lowercalcium, retinol caroteneand vit. C. versus male headof household. No sig. diffiron.

USA (urban) Finley et al.(1994)

40 adult men/women,case study

Biochemical Absorption manganese sig.higher in women, but half-life longer for men.

*FFQ, Food frequency questionnaire. 3DR, Three-day dietary recall questionnaire. 24HR, 24-hour recall of foods consumed. WF,weighed foods methods. ANT, anthropometry. Biochemical, laboratory analyses (blood, serum, etc.). Qualitative, direct observationand other qualitative techniques.*Abbreviations: diff., difference; stat., statistical; sig., significant; SD, standard deviation.

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It is because of such environmental factors that irondeficiency anemia is often linked to parasitic infestations. InTanzania, the combination of ascariasis and iron deficiencywas found to be linked to low weight gain among children,while schistosomiasis was correlated with low heightgains.29 Similar links have been found between malnutri-tion and low serum magnesium levels,30 imbalances be-

tween n-6 and n-3 fatty acids,31 vitamin E-related neuro-logic deficits,32 and low levels of bioavailable zinc.33

While the causal nature of such relationships is oftenuncertain, it is clear that macronutrient status, illness, andmicronutrient deficiencies are interrelated and that thenature and severity of food insecurity influence the pre-cise outcome.

Table 2 (Part 1). Studies Not Reporting Intra-Household Variability in Micronutrient Deficiencies

Geographic Location Study Sample Size/TypeSurvey

Methods* Findings†

Meta-analysis

Nepal, Zambia,Malawi,Indonesia

Katz et al.(1993)

30,000 children 0–6 yfrom 4 independentstudies

Clinical Boys higher risk of xerophthalmiathan girls overall, but not sig.diff.

Asia

China (rural, urban) Zhang et al.(1996)

6500 adults 35–64 yin 65 communes

Biochemical No diff. by gender for zinc status.

Philippines (rural) Bouis, et al.(1998)

c. 4000 children andadults

24HR, ANT,qualitative

No sig. diff in intake ofmicronutrients/minerals by ageor gender (not controlling forrequirements)

India (rural) Behrman(1988)

800 children 0–15 yfrom VLS studies

24HR No sig. diff. (boys/girls) in intakecarotene, vit. C, calcium,riboflavin even adjusting forrequirements.

Nepal (rural) Upadhay et al.(1981/85)

National randomsample, children0–14 y.

Clinical Higher prevalence of Bitot’s spotfor boys, but not statisticallysig.

Pakistan (national) NIH (1988) 10,406 children under5 y.

Clinical No difference in prevalence ofBitot’s spot by gender of child.

Thailand (rural,urban)

Bloem et al.(1989b)

127 children 1–3 y inSakon Nakhonprovince

Biochemical No sig. diff. in mean level or SD.for serum retinol, (except forages 3 to 6 when boys hadlower level).

West Asia/North Africa

Morocco (rural) Oldham et al.(1998)

197 children from110 hhs in 19villages (randomsample)

Biochemical,clinical

No sig. diff by gender of child forurinary iodine status.

Morocco (rural/urban)

GoM (1998) 1453 children 6–72m, stratifiedrandom

ANT, clinicalbiochemical,FFQ

No sig. diff. in clinical or serumretinol levels by gender ofchild.

Oman (national) GoO (1995) 759 children 0–6 m Clinical No diff. in mean levels of serumretinol by gender, or in SDs.

Djibouti(rural/urban)

Resnikoff(1988)

114 children 4–10 y Biochemical No diff. in serum retinol level(�0.70 umol/l) by gender inurban areas (but higher prev.for rural girls than boys)

*FFQ, Food frequency questionnaire. 3DR, Three-day dietary recall questionnaire. 24HR, 24-hour recall of foods consumed. WF,weighed foods methods. ANT, anthropometry. Biochemical, laboratory analyses (blood, serum, etc.). Qualitative, direct observationand other qualitative techniques.†Abbreviations: diff., difference; stat., statistical; sig., significant; SD, standard deviation.

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Iodine Deficiency and the Iodine DeficiencyDisorders

In some regions, the soil and water are so deficientin minerals and trace elements that micronutrient defi-

ciencies result. Iodine provides a good example. Land-locked arid environments and mountains tend to havelow iodine levels in soil, bedrock, and groundwater thattranslate into iodine deficiencies among local inhabitants.

Table 2 (Part 2). Studies Not Reporting Intra-Household Variability in Micronutrient DeficienciesGeographic Location Study Sample Size/Type Survey Methods* Findings†

Sub-Saharan Africa

South Africa(rural)

Willumsen et al.(1997)

57 children(hospitalized)

Biochemical No sig. diff. vit. A by gender

Cameroon (rural) Wilson et al.(1996)

5352 children 0–5 ymulti-stage clustersample

Clinical, FFQ No sig. diff. by age orgender in vit. A status, butall worst in remotemountain ecology.

Malawi (rural) Tielsch et al.(1986)

5436 children �6 y.Lower ShireValley.

Clinical Bitot’s spot higher for boysthan girls but no stat. sig.

Malawi (rural) GoMi (1986) 5436 children �6 y.Lower ShireValley

Clinical No sig. diff. by gender fornight-blindness or cornealscars.

Ethiopia (national) Wolde-Gebriel(1992)

739 children 6–72 m(1981/82 nationalsurvey)

Biochemical No difference in mean serumretinol levels by gender

Zambia (national) Luo and Mwela(1999)

900 mothers and 900children (�5 y)

Biochemical No sig. diff. in serum retinolby age or gender

Latin America

Venezuela (urban) Llovera et al.(2004)

104 children (�5 y)in private pre-school

Atomic absorptn.spectophotometry

No sig. diff. serum zinc bygender

Venezuela (rural) Brunetto et al.(1999)

85 children, 2–6 y,Merida State

Biochemical No sig. diff vit A or Cu bygender

Venezuela(national)

de Hernandez(1994)

814 children 6 m to17 years old (from1981/82 nationalsurvey)

Biochemical No sig. diff. in serum retinolor iodine by gender or agecohorts

Guatemala(peri-urban)

Ribaya-Mercadoet al. (1999)

26 elderly (�60 y) Clinical,Biochemical

No sig. gender diff. in body,liver or rerum retinol.

Peru (rural) Leonard(1991a,b)

101 adults andchildren from 26households.

ANT, FFQ, WF No gender diff. in childmicronutrient intakes.

Chile (urban) Castillo-Druan.et al. (1987)

32 infants 0–24 m Biochemical No sig. diff. by gender inresponse to zincsupplementation.

Brazil (rural) Sichieri et al.(1996)

142 children 6–12 y,random in poorschools

24HR, biochemical Fe and vit. C status low forboth genders but no sig.diff by gender.

Haiti (urban) Nicklas et al.(1998)

305 children 2–5 y,of low incomegroups

Biochemical 40% of children low serumferritin, but no sig. diff.by gender.

*FFQ, Food frequency questionnaire. 3DR, Three-day dietary recall questionnaire. 24HR, 24-hour recall of foods consumed. WF,weighed foods methods. ANT, anthropometry. Biochemical, laboratory analyses (blood, serum, etc.). Qualitative, direct observationand other qualitative techniques.†Abbreviations: diff., difference; stat., statistical; sig., significant; SD, standard deviation.

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For example, the total goiter rate in the lowlands ofLesotho was found to be 5.7 compared with 28.0 in themountains.34

Females from adolescence onwards generally have ahigher prevalence of goiter than males.14 Girls 8 to 18years of age in upper Egypt were significantly morelikely to develop goiter than boys, although living in ahousehold with access to farmland of low iodine contentrepresented a high risk factor that affected both gendersand all ages.34 Similarly, findings on Papua, New Guin-ean adolescents35 and analysis of Ethiopian 6- to 12-year-olds all show that females exhibit more iodinedeficiencies than males.18 Some studies suggest other-wise. In North Korea, UNICEF found no significantdifference in total goiter rate between women and men,36

and the same was reported for preschool girls in Mo-rocco. In other words, agroecology is a strong, but notperfect, predictor of iodine deficiency, and this alsoapplies to micronutrients beyond iodine. For example,individuals of either gender (but especially boys) insemi-arid Sudan are more at risk of vitamin A deficiencythan people living near the Nile, especially during the dryseason.37

Similarly, girls in Madagascar consume too littlevitamin A in the dry season but meet minimum require-ments in the wet season.38 In northeast Brazil, signs ofxerophthalmia absent during most of the year make aregular appearance during the interharvest “sertao” per-iod.39 Thus, data on deficiencies can be highly sensitiveto the timing of assessments.

IMPLICATIONS FOR PUBLIC HEALTH ACTION

What can public action be expected to achieve whendeficiencies are inequitably shared within households?Supplementation of mothers and infants may be a goodshort-term solution to low iron intake, given that iron-rich dietary sources of iron are usually expensive. Butcan we be sure that targeted supplements or fortifiedfoods are accessible to all those who most need assis-tance? It could be argued that attention to the complex-ities of intra-household nutrient distribution sets too higha standard for public health intervention. Indeed, manypolicy-makers and politicians are already wary of “in-truding” into the realm of household decision-making,and some experts doubt the feasibility of effectivelytargeting only a chosen few individuals within otherwisecommonly poor households.

There are two important aspects of micronutrientdeficiency problems that suggest that attention to intra-household dimensions is no luxury. The first is that theprevalence of certain diseases and individual responsesto public health action can be differentiated by gender.Iodine supplementation had a greater effect on reducing

male infant mortality than female mortality in WestJava.14 Iron fortification among children and adolescentsin Venezuela showed a significantly lower positive re-sponse on anemia among 15-year-old girls comparedwith boys of the same age and younger girls.40 Similarly,a series of vitamin A supplementation trials in Indonesiashowed significant growth responses in treatment vil-lages compared with control villages, but only for non-infant males.41

However, male-female differences in supplementa-tion responses cannot be generalized. No significantdifference was found between boys and girls in responseto zinc supplementation in Indonesia41 or Vietnam.42 Nogender difference in response was found in response tovitamin A supplementation in Ghana.43 A meta-analysisof vitamin A trials suggested that the relative effect ofvitamin A in reducing mortality was not significantlydifferent by gender.44

Thus, while some evidence suggests that responsesto interventions may differ by sex and possibly by age,the empirical basis for predicting such differences islacking. Most studies that show girl-boy variability inoutcomes derive from Asia, and most are tied to studiesof supplementation trials. More needs to be known aboutage/gender responses: a) to other forms of intervention(including access to fortified foods, home-grown vege-tables, and nutrition education); b) in countries outside ofAsia; and c) in association with contextual informationallowing for better interpretation of clinical findings. Thelast requires attention to social, cultural, and behavioraldimensions of food access, distribution, and consump-tion, as well as non-food parameters linked to health anddevelopmental care. This raises the problem of behav-ioral change, the second issue with intra-household di-mensions.

A study of the immune status of malnourished chil-dren showed that it took at least two months for them toreach full immunologic recovery.45 Full recovery re-quires adequate recovery of micronutrient status andphysiological functions; however, most children are dis-charged from rehabilitation centers when they reacharound 90% of the median reference weight-for-height,but their immunologic systems are still depressed. Thelack of change in their home context means that recov-ered children return to the same disease, care, and foodallocation environment that they inhabited previously.Frequent relapses among such children are probably dueto the incomplete immunologic recovery, which goesbeyond meeting minimum anthropometric standards. Inother words, micronutrient and health status togetherplay an important role in determining recovery andgrowth.

These examples indicate that more studies need toconsider that success in addressing only one clinical

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aspect of the problem may in the long run mean thatbenefits are not sustainable. For example, a study inBangladesh considered the effects of postpartum vitaminA or beta-carotene supplementation on serum retinolconcentrations among mothers and their infants. Com-pared with a control group, mothers receiving supple-ments did have higher breast milk concentrations ofvitamin A at 3 months, but the improvements were notsustained; while both interventions were beneficial, nei-ther was sufficient to correct underlying subclinical de-ficiency among the mothers or to bring their infants intoadequate vitamin A status.46

The same result was reported from Vietnam, wheredaily and weekly supplementation did improve bench-mark levels of hemoglobin zinc and retinol, but limitedeffect was found in terms of growth rate among stuntedchildren.12 This suggests that in populations with multi-ple deficiencies, the effects of supplementation (on lineargrowth) with single nutrients alone may not be signifi-cant. More recent findings are also mixed.47,48 Multiplemicronutrient supplements caused growth improvementamong infants (�12 months) in Mexico, but no signifi-cant impact on growth was shown in Peru or Guate-mala.49,50

CONCLUSIONS

Three main conclusions emerge from this explor-atory review. First, important differences appear to existin prevalence rates for various deficiencies by age andgender. Undifferentiated aggregation of people intobroad categories of “children” or “fathers” obscures widevariations in conditions as individuals proceed throughthe life cycle in different contexts. Studies of children 6months to 4 years of age may draw misleading conclu-sions because deficiencies are greater among children 6to 10 years of age. The aggregation of data for males andfemales makes it more likely that important gender-specific differentials in risk factors will be overlooked. Anarrow focus on infants and pregnant/lactating womenalso risks ignoring problems among school-aged girls,adolescents, non-pregnant women, and the elderly. Thisdoes not suggest that generalizations are incorrect, but ifused to inform targeting and prioritization of resources,they need to be critically re-examined. One gender or agegroup may face more deficiencies than others in someplaces, cultural contexts, and times but not in others.More attention to the context-specific nature of deficien-cies is called for as a first step toward improved preva-lence estimates and a better basis for targeting publicaction.51

The second conclusion is that more attention needsto be given to measurement techniques and analyticalapproaches. Comparative studies and sensitivity analysis

of alternative techniques are needed. A critique is neededof the potential co-linearity, substitutability, or exclusiv-ity of many clinical, biochemical, anthropological, andfood recall measures now in use. Furthermore, researchprotocols need to pay more attention to the multipleinteractions among numerous micronutrients, diseases,health history, and life-cycle contexts that affect thebiochemical markers of a single micronutrient defi-ciency.

A third conclusion is that if multiple nutritionaldeficiencies are interrelated, so too must be the solutions.Operational agencies are often noted for their expertisein tackling one specific micronutrient problem or an-other. This engenders a one-at-a-time approach that mayachieve definable results in the short-term, but leavemuch to be desired in the longer term. If micronutrientinterventions are to benefit all individuals at risk (and notjust those most at risk during one period of the lifecycle), then deficiency problems must be addressed as amainstream development problem rather than as a spe-cialist technical niche within the nutrition community.

Similar conclusions have long been drawn in rela-tion to many macronutrient interventions, including tar-geted food aid, coupon programs, and supplementaryfeeding. One targeted food, income, or information trans-fer may be ineffective without additional complementaryinputs. Micronutrient deficiencies are not a differentorder of problem. The sustainability of actions aimed atresolving and preventing micronutrient deficiency prob-lems typically depends on the modification of contextualfactors by the stakeholders themselves. Enabling changesrequires a greater understanding among policy-makersand project designers of the daily trade-offs that are madein access to food, income, care and, other resources—including micronutrients—at the intrahousehold level.

ACKNOWLEDGEMENTS

This paper is dedicated to the memory of Dr. RainerGross, the former UNICEF chief of nutrition who passedaway September 30, 2006. The authors would like tothank the following people who shared data and/or in-sights: Andrew Thorne-Lyman, Tina van den Briel, andPieter Dykhuisen (World Food Programme); BeatriceRogers, James Levinson, Gary Gleason, Robert Russell,William Lockeretz, Guangwen Tang, and Judy Ribaya-Mercado (Friedman School of Nutrition, Tufts Univer-sity); Chipo Mwela (National Food and Nutrition Com-mission, Zambia); Howarth Bouis (International FoodPolicy Research Institute); Noel Solomons (Center forStudies of Sensory Impairment, Aging and Metabolism,Guatemala); Keith West, Joel Gittlesohn, and RebeccaStotzfus (Johns Hopkins University); Margaret Bentley(University of North Carolina-Chapel Hill); Martin Frigg(Task Force Sight and Life, Geneva); Nina Schlossmann

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(Global Food and Nutrition); Klaus Becker, the late PeterFuerst, and Konrad Biesalski (Hohenheim University,Stuttgart); and Victor Barbiero and Timothy Quick (US-AID). Any errors in data or interpretations of reviewedstudies are those of the authors alone and the viewsexpressed in this paper do not necessarily represent theposition or the stated policy of the associated organiza-tions or academic institutions of the authors.

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