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able of contents1. An analysis of anemia and pregnancy-related maternal mortality................................................................ 1

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Document 1 of 1

An analysis of anemia and pregnancy related maternal mortalityAuthor: Brabin, Bernard J; Hakimi, Mohammad; Pelletier, DavidProQuest document link

Abstract: The relationship of anemia as a risk factor for maternal mortality was analyzed by using cross-sectional, longitudinal and case-control studies because randomized trials were not available for analysis.

Full text: HeadnoteAn Analysis of Anemia and Pregnancy-Related Maternal Mortality1,2

HeadnoteABSTRACT The relationship of anemia as a risk factor for maternal mortality was analyzed by using

crosssectional, longitudinal and case-control studies because randomized trials were not available for analysis.

The following six methods of estimation of mortality risk were adopted: 1) the correlation of maternal mortality

rates with maternal anemia prevalence derived from national statistics; 2) the proportion of maternal deathsattributable to anemia; 3) the proportion of anemic women who die; 4) population-attributable risk of maternal

mortality due to anemia; 5) adolescence as a risk factor for anemia-related mortality; and 6) causes of anemia

associated with maternal mortality. The average estimates for all-cause anemia attributable mortality (both

direct and indirect) were 6.37, 7.26 and 3.0% for Africa, Asia and Latin America, respectively. Case fatality

rates, mainly for hospital studies, varied from 50%. The relative risk of mortality associated with

moderate anemia (hemoglobin 40-80 g/L) was 1.35 [95% confidence interval (CI): 0.92-2.00] and for severe

anemia (


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The relationship of anemia as a risk factor for mortality is derived mainly from cross-sectional studies and can

be confounded for several reasons. Most studies report hospital data, often for moribund women, and there is

limited attention to factors such as pregnancy hemodilution, hemoglobin rise in late pregnancy, concurrent

infection, hemorrhage, prior treatment or poor maternal nutritional status. In young women living under endemic

malaria conditions, especially in urban areas in which adults may have poor malaria immunity, severe malarial

anemia and cerebral malaria may occur and can rapidly lead to death (Granje et al. 1998). For these reasons,most studies form an inadequate basis for determining how anemia relates causally to maternal survival in

communities, and extrapolation from hospital delivery data must be considered an approximation that may be

misleading.

Intervention studies with maternal mortality as an outcome measure are required to determine causality, but

these are very difficult to conduct for both ethical and logistic reasons. For example, there are very few studies

that did not use transfusion as an emergency procedure in severely anemic women at term (Fullerton and

Turner 1962). If transfusions are taken into account, then near-miss fatality could be an alternative outcome

measured, but the true risk in such cases remains uncertain. In view of these difficulties, a number of alternative

approaches that independently assess this risk must be adopted. Consistency between analyses of severe

anemia and poor survival would add credence to the strength of a causal relationship. Several issues are

related to estimating attributable risk for specific causes of anemia and in quantifying risk for moderately anemic

women because less anemia may still contribute to death from other causes. Such information would be helpful

for intervention decisions.

METHODS

Identification of published studies. Published studies on the relationship between anemia (defined by severity)

and maternal mortality were identified using Medline, references in published papers, Cochrane Review issues

and personal communications. Unpublished data from Nigeria available in a detailed hospital report by Lawsonand Lister were reanalyzed and included in a separate summary of Nigerian data. Studies that included

postnatal deaths up to 40 d were included, although in practice few studies reported follow-up data beyond

delivery.

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Selection of studies for inclusion in the analyses. Studies included in the review were limited to cross-sectional,

longitudinal and case-control studies because no randomized controlled trials were available for analysis.

Attention was given to the assessment of possible biases in studies of mixed validity. Studies identified were

reviewed with regard to the following factors: maternal age, parity, anemia severity, clinical presentation,

gestational age, use of blood transfusion, length of follow-up, etiological diagnosis, laboratory estimation of

hemoglobin (Hb)^sup 4^ or hematocrit, and analytical methods. Hematocrit was converted to a Hb value bydividing by 3 and multiplying by 10. Studies that listed anemia as a direct cause of death were of particular

value, permitting the estimate of the total number of maternal deaths attributed to anemia. Data from the WHO

compilation of maternal mortality was reviewed and categorized by source (hospital or community), direct or

indirect cause of anemia, region and number of studies available. Hemoglobin midpoint values were calculated

when the range was available. For other studies, anemia cut-off points were used below which proportional

groups of women with anemia were defined.

Analyses. The definition of maternal death used in this review was based on the 10th revision of the

International Classification of Diseases, which defines a maternal death as the death of a woman while

pregnant or within 42 d of termination of pregnancy, regardless of the duration and site of the pregnancy, from

any cause related to or aggravated by the pregnancy or its management but not from accidental or incidental

causes (WHO 1992a).

Maternal deaths were also divided into two groups as follows: 1) direct obstetric deaths, resulting from obstetric

complications of the pregnant state (pregnancy, labor and the puerperium), interventions, omissions or incorrect

treatment, or a chain of events resulting from any of the above; and 2) indirect obstetric deaths, resulting from

previously existing disease or disease that developed during pregnancy and was not due to direct obstetric

causes but was aggravated by the physiological effects of pregnancy.



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RESULTS Maternal mortality and anemia prevalence. A detailed compilation of anemia prevalence in women

published by WHO includes estimates of maternal mortality from anemia for nine selected countries (WHO

1992b). These estimates range from 27 per 100,000 live births in India to 194 per 100,000 live births in a

hospital-based study in Pakistan to 42 of 44 maternal deaths in Somalian refugee camps. The cut-off values for

defining anemia vary for these studies as does anemia prevalence in the communities in which these women

live (WHO 1992b). The WHO tabulation adopts the international definition for anemia for pregnant women of


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The graph shown in Figure 1 uses data on anemia prevalence from the WHO tabulation of available information

on nutritional anemia in women (WHO 1992b), and maternal mortality ratios reported by United Nations

Children's Fund (1999) for the years 1990-1997. Anemia prevalence values for individual countries were

selected by using the following criteria: national data if available, altitude


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malarious area, estimated the maternal mortality ratio as 398 (per 100,000 live births) and found an anemia

prevalence (hematocrit


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how increased susceptibility to injection is related to nutritional anemia. Increased infection risk could provide a

plausible biological mechanism for increased mortality risk in moderately anemic women.

How can acute and chronic influences on mortality risk in anemic women be distinguished, and is there a

threshold effect for anemia severity at which maternal mortality greatly increases? Tables 5 and 6 summarize

available data on case fatality in relation to pregnancy hematocrit or Hb values. Nearly all of these studies are

hospital based and report women dying mainly in the perinatal period. Several provide no information on

exclusions or duration of postpartum followup. The proportion of women treated by transfusion is unclear except

for five studies (Cheng-Chi et al. 1981, Fullerton and Turner 1962, Harrison 1975, Harrison and Rossiter 1985,

Isah et al. 1985). Differences in available obstetric care and blood transfusion greatly influence mortality risk inseverely anemic women, and disparity among findings for individual countries could primarily reflect these

differences. In this context, it is of value that there are seven studies for comparison from Nigeria alone, three of

which are reports by Harrison and his colleagues (Harrison 1975 and 1982, Harrison and Rossiter 1985). Case

fatality fell with transfusion from 27.3 to 1.7% in women with hematocrit values


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Wickramasuriya (1937) in Ceylon stratified case fatality by the presence or absence of hookworm infection and

showed significantly higher risk of death in infected women who presumably had chronic iron-deficiency

anemia, [relative risk 2.1; 95% confidence interval (CI): 1.3-3.41. Most reports were from malarious areas, and

malaria is an important contributor to pregnancy anemia, especially in primigravidae (Brabin 1983). However, in

a recent study in Malawi, the attributable risk of anemia in pregnancy was greater for iron deficiency than

malaria (Verhoeff et al. 1999).Population-attributable risk of maternal mortality due to anemia. Attributable risk can be a useful summary

statistic for describing the effect of a risk factor on mortality at the population level. However, the more severe

anemia becomes, the more likely it is to have multiple causes and not be due to iron or nutritional deficiency

alone. This creates difficulties in establishing attributable risk, particularly across populations whose

epidemiological background and disease exposure may be very different. This problem was addressed by

Pelletier and colleagues (1993) in discussing the epidemiological evidence for a potentiating effect of

malnutrition on child mortality.

Causality should be inferred only in the light of the consistency of the epidemiological evidence, and in the

present discussion, terms such as PAR are meant to refer only to statistical associations. Rush (2000)

estimated relative risks for anemia-attributable maternal mortality and discussed in detail the limitations of

several of the studies cited in Tables 5 and 6. On the basis of evidence available, he considered it a reasonable

working assumption that maternal mortality is greatly increased with severe anemia, and the strength of the

relationship made it appropriate to assume a causal association with severe anemia but that the association

with moderate anemia was less clear.

By way of deriving the most reliable estimates of the effects of moderate anemia, the relative risks from five of

the studies that had adequate data were calculated using only internal reference values and mutually exclusive

categories of Hb concentrations. These estimates are shown in Tables 7 and 8. For the moderate Hb range (40-

80 g/L), there is no consistency in the relative risk estimates among the five studies although all are from one

country (Nigeria). The table also highlights the small sample size for most of these analyses, suggesting caution

in drawing inferences from these individual values. When the data from all five studies are pooled, the relative

risk of mortality associated with moderate anemia was estimated to be 1.35 (95% CI: 0.92-2.00). The lack of a

significant association arises in part because mortality risk in the referent groups was not low and none of these

groups were nonanemic. The relative risk of maternal mortality for severe anemia (


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Estimates of PAR derived from these data are shown in Table 9. The PAR value of 31% reported by Zucker et

al. (1994) for a group of women with a 6% severe anemia prevalence (Hb


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(Hb


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There is a scarcity of data on adolescent mortality and severity of anemia in developing countries. Presumably,

onset of nutritional anemia at an early age results in chronic anemia that perpetuates any risk of anemia-related

mortality through subsequent pregnancies. Effective antenatal care may reduce these risks because more

frequent antenatal care visits for pregnant adolescents in Malawi correlated with a significant reduction in theprevalence of severe anemia (Brabin et al. 1998).

Causes of anemia associated with maternal mortality. Anemia in pregnancy in women in developing countries is

multifactorial in etiology. Iron- and folate-deficiency anemias are common. The former are related to nutritional

deficiency and intestinal helminthic infections and the latter to poor intake and chronic hemolytic states.

Hemolytic anemia, to a greater or lesser degree, is commonly seen during pregnancy in malarious areas of

developing countries. The observation that severe anemia is greatly reduced in patients who have received

regular malaria prophylaxis during pregnancy (Fleming et al. 1986, Garner and Brabin 1994, Shulman et al.

1999) indicates that it is related to chronic infection with Plasmodium falciparum malaria. It is therefore not

surprising to find that the number of patients admitted with severe anemia is highest during the months after the

rainy season (Fleming 1970, Verhoeff et al. 1999).

Hemolysis as a factor in the development of megaloblastosis in folate-deficiency anemia has been

demonstrated by Chanarin et al. (1959) and P. falciparum infection is an important cause in holoendemic

malarious areas (Fleming et al. 1986). A further group of patients who contribute to these severe hemolytic

anemias are those with sickle cell disease. This group accounted for


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studies in malarious areas of Africa and Papua New Guinea. The figure is derived from a previous estimate of

this excess risk (Brabin and Rogerson 2001) but includes additional studies (Isah et at. 1985, Lawson and

Listen 1964) not identified at the time of the earlier analysis. The goodness of fit shows a highly significant

association for a quadratic model (R^sup 2^ = 0.996; P = 0.0041). This model indicates that, in malarious areas,

there is only a small excess of mild anemia in primigravidae compared with multigravidae. A larger excess is

observed with moderate and severe anemia (Hb


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These calculations suggest that nutritional deficiency is a major component of severe anemia deaths even in

malarious areas. The calculations were based on primigravidae, but this conclusion should apply to

multigravidae, who are less susceptible to malarial infection and may have a higher prevalence of nutritional

deficits and iron-deficiency anemia than primigravidae (Isah et al. 1985).

DISCUSSION AND CONCLUSIONS

The more severe the anemia, the more likely it is to have multiple causes and not be related solely to iron

deficiency. This creates difficulties in establishing attributable risk. Because several factors contribute to the

prevalence and severity of anemia, it cannot be assumed that distinct epidemiological parameters predict the

effect of anemia on maternal mortality. This is a difficulty in an analysis that aims to identify specific components

of attributable risk. The specific nonmalarial components (mainly nutritional) of this attributable risk can be

estimated, but the proportion of these related specifically to iron-deficiency anemia, while uncertain, could be

substantial.

Because moderate anemias are common and less strongly associated with malaria, nutritional deficiencyanemias would comprise the larger component of anemia-attributable maternal mortality. This result highlights

the need to determine mechanisms by which nutritional deficiency anemia, especially iron deficiency, could

increase maternal mortality. Nutritional deficiency may impair immune responsiveness, and in nonpregnant

women, iron-deficiency anemia has been associated with increased risk of death from circulatory disease

(Elwood et al. 1974). Iron deficiency is likely to be a major contributory cause, although vitamin A deficiency

could also be important. Routine supplementation with vitamin A in a large trial in Nepal reduced maternal

mortality, but the mechanisms were poorly defined and not obviously attributable to anemia reduction (West et

al. 1999). Folate deficiency may also be important (Baily 1995). HIV infection, which is common in some

pregnant populations in Africa and in some studies has been associated with lower Hb levels, could enhance

the effect of nutritional deficits on mortality risk.

Figure 2 showed that high Hb values (>130 g/L) were associated with slightly increased mortality risk. This

result was obtained through the inclusion of the data of Harrison and Rossiter (1985), which showed a marked



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increase in mortality risk in women with hematocrits >0.45. The explanation for this is not known but could be

related in part to dehydration and hemoconcentration in emergencies. Mortality in nonpregnant Caucasian

women with high hematocrits was attributed to higher cholesterol and blood viscosities in such subjects and

was related in part to cardiovascular disease (Elwood et al. 1974). Similar mechanisms may apply in women

from developing countries, but some caution is required in interpreting this observation because the result is

from a single study.There is almost no evidence that the treatment of anemia other than with exchange transfusion (Fullerton and

Turner 1962) or judicious use of blood transfusion (Lawson and Lister 1954), or treatment of acute severe

malarial anemia (Gilles et al. 1969) lowers risk of maternal mortality. A controlled intervention trial would be a

stronger approach, but this would require a very large sample size and may not be ethically acceptable. Thus,

indirect methods of analysis are of particular relevance in demonstrating the strength of associations of anemia

with maternal mortality. There are several limitations to this approach that have been mentioned previously, not

least that the methods of Hb measurement vary (methods include Sahli, Talquist, hematocrit, hemacue, Coulter

counter techniques and use of optical spectrophotometers). However, this analysis has identified a large

number of reports and the strength of statistical associations can be adequately tested.

Estimates of PAR can be defended on the basis of the strong association between severe anemia and maternal

mortality, but not for mild or moderate anemia. The policy implications of this are, first, that some reduction in

maternal mortality should be achievable in developing countries through reduction in severe maternal anemia,

with the greatest effect resulting from reductions in both malaria and nutritional anemias. This conclusion

contrasts with the situation in Western countries, where neither historical review nor review of obstetric literature

identified a plausible contribution of nutritional factors to the decline in maternal mortality (Ronsmans et al.

1999). The size of this effect is likely to be small unless there is a very high prevalence of severe anemia in the

population. However, the evidence is insufficient for or against treatment of iron-deficiency anemia as a

preventive measure for maternal mortality. Second, with good antenatal and obstetric care, most anemia-related

deaths are preventable, and policies to reduce anemia prevalence should not be divorced from efforts to

provide adequate antenatal and delivery facilities for women in developing countries. Putting into operation

nutrition interventions as the magic pill approach will have to compete with budgets allocated for essential

obstetric care. Finally, iron deficiency and malarial anemia should be treated differently from other categories of

risk in maternal health such as height, weight, age, parity, previous history and use of antenatal care services.

Iron-deficiency anemia, like malarial anemia, is in fact a complication, a medical condition that requires

treatment. The broad use of terminology, which clusters together such unrelated criteria, could be detrimental to

effective health care strategies (Rhode 1995).

John Lawson, in his classic annual report in 1954, concluded that it was hoped that maternal (and fetal) loss

from anemia would show a steady decline in the future. In his view, the declining level of Hb in some patientsmeant that they reached a point of no return and would die however they were treated. Fifty years later,

maternal and fetal losses are still unacceptably high, although today we have better ways of preventing women

from reaching that point of no return.

ACKNOWLEDGMENTS

We thank James Bunn for finding the early report by Professor John Lawson and U. Lister (1953-1954), Jean

Taylor for expert secretarial assistance and several colleagues for kindly helping with data sources and

references. DISCUSSION

Participants: Pelletier, Beard, Brabin, Allen, Rasmussen, Habicht, Tielsch, Premji, Oppenheimer, Stoltzfus,

Horton

Dr. Pelletier: Several comments on the Nigerian studies, which report the lowest hemoglobin values. They are

all from around 1960, all from one country, and all with a certain level and type of obstetric care and they are

clearly pulling the risk curve up. So, if you fit various models to that, it turns out the best fit is exponential. I am



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trying to zero in on the mild and moderate range, independent of any sort of very powerful data points that are

pulling it up. There does not seem to be any relationship if you exclude those four studies. So, if we want to look

for a dose-response relationship, we really have to see evidence of it over the entire distribution and be wary of

influential data points, especially because those seem exceptional.

Dr. Beard: Do we have any documentation of the kind or type of obstetric care that was given then relative to

what is available in that part of the world now?Dr. Brabin: I think the obstetrics has improved greatly. I do not think we can ignore those four points. These old

Nigerian studies document the situation with relatively little interference, where women have desperately low

hemoglobin and are dying. These are the only data that exist in the world.

Dr. Pelletier: I am not suggesting we ignore them. It would be, probably, the causal effect of severe anemia.

Dr. Beard: Are you willing to allow those four studies to stay in the analysis?

Dr. Pelletier: Yes, for the purposes of making inferences about severe anemia, but if we start fitting curves they

will begin to have a distorting influence on our judgment. Imagine that it was absolutely horizontal and then it

goes up with severe anemia. If you fit an exponential curve to that, it is going to fit very nicely.

Participant: Are there other sub-Saharan Africa studies of the mid-1960s in your pile of 28 studies? I am just

trying to figure out what the situation would be if you took them all out.

Dr. Pelletier: Actually, I am looking at that curve again and Brabin is right. It is not just those four. It turns out

that eight data points are up there. Seven of the eight are from Nigeria. One is from Guinea. So, they are all

from sub-Saharan Africa. Some of the less extreme points are also from Africa.

Dr. Allen: Were they all the same investigators?

Dr. Brabin: No. There were three different groups of investigators.

Dr. Beard: One of the things that generally concerns me about hospital-based data in resource-poor

environments is what gets you admitted to a hospital. What gets you admitted to a hospital if you show up with a

hemoglobin of 30 or 40 g/L is going to be very different from what gets you admitted if you show up with a

hemoglobin of 60 or 80 g/L. Right? So, it seems to me that the people who are showing up with hemoglobins of

60 or 80 g/L are being admitted primarily for completely other reasons.

Participant: That would tend to diminish the relationship.

Dr. Beard: That would tend to inflate the mortality risk among the moderately anemic because they are selected

for a higher risk profile. I think the question is in the mild-tomoderate range of anemia, what is it that hospital-

based data can tell us in this kind of environment, and how much is selection bias influencing our assessment of

the relationship.

Dr. Habicht: At least down to 60 g/L or so, I do not see any admissions because of hemoglobin. They are all

there for other reasons. Now, is there any reason to believe that those other reasons would be different across

the hemoglobin range? Probably not.Dr. Brabin: Any woman who comes to the hospital whatever her hemoglobin is admitted so that she can deliver

her baby.

Dr. Habicht: I think we need to divide the conversation into different parts. First, do we believe that that excess

risk below 50 g/L is really there? It seems to me that everybody believes that. So, the second question is

whether there is any excess risk above 50 g/L? From these data, if you just took the fitted lines away so you

were not being prejudiced, you would not see a relationship above 50 g/L. This is an underestimate of the true

relationship. If it is a flat line, it is an underestimate because those people are being selected into the hospital

sample because they are likely to die.

Dr. Tielsch: So, you think the comorbidity profile of women with hemoglobin 60 gfL at admission for birth is the

same as for women who have 100 g/L at admission. I suggest that is not probably true, in fact, because we

know that anemia is related to poverty and poor health. So that women who get admitted-who are coming to the

hospital to deliver-and have got an admission hemoglobin of 100 g/L are likely to be healthier.



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Dr. Habicht: Then your conclusion is very clear. Taking that into account-rather than this apparent flat

relationship between hemoglobin and mortality-you then have a positive relationship between hemoglobin and

case fatality above 60 g/L, going up to the right-hand side.

Dr. Tielsch: I cannot figure out what the true relationship is.

Dr. Premji: I wanted to ask Brabin whether he has any clue about the association between malaria and

mortality.Dr. Brabin: I cannot enlighten you. We have done a retrospective analysis of a very large data set from the north

coast of Papua New Guinea and an equally large data set from the highlands of New Guinea. In the malaria-

endemic north coast, for the same level of hemoglobin in the mother at delivery there was a significantly

increased risk of postpartum hemorrhage. This is just a hint that malaria is in some way related to the risk,

because postpartum hemorrhage is associated with mortality. I do not know the mechanism.

Dr. Tielsch: This is outside primagravida-independent of that?

Dr. Brabin: Independent.

Dr. Oppenheimer: I remember seeing a review about maternal mortality in Nigeria in the 1960s and they had a

real problem with anemia and heart failure because they did not have effective rapid-acting diuretics. If they

were transfused, their heart failure got worse. In fact, they were trying to use exchange transfusion to cope with

this problem. So, there was a particular problem of management of severe anemia and heart failure.

Dr. Brabin: The Nigerian studies do give clinical reasons for death, and heart failure is mentioned as one cause

of death. It has been shown in Nigeria that exchange transfusion dramatically reduced the risk of death in these

severely anemic women.

Dr. Beard: Some of us may recall Henry J. Whipple, who won the Nobel Prize in Medicine for looking at the

effects of severe anemia on cardiovascular adaptation and cardiac failure. So, this question of severe anemia,

oxygen transport and cardiovascular adaptation has been around for a really, really long time.

Dr. Stoltzfus: It is remarkable that this hemoglobin mortality risk curve is flat across the wide hemoglobin range

about 60 g/L, given all we expect from other anemia survival curves in nonpregnant adults. I think that reverse

causality is part of all these anemia-survival associations, but the fact is that they are there, even in well-cared-

for populations, even in surgical patients, who are not necessarily suffering from an infectious disease that is

causing their surgery. The fact that this occurs in British data makes it astounding to me that that is absent in

African data. I do not know what to conclude from that.

Dr. Pelletier: Bear in mind that these data points are assembled from 12 different studies. So, the picture is a bit

deceiving. We are used to having a reference group and several groups of increasing severity, and then you

would expect to see something like that. However, this is a meta-analysis. There is lots of stuff going on

between these data points besides different degrees of anemia.

Footnote1 Presented at the Belmont Meeting on Iron Deficiency Anemia: Reexamining the Nature and Magnitude of the

Public Health Problem, held May 21-24, 2000 in Belmont, MD. The proceedings of this conference are

published as a supplement to The Journal of Nutrition. Supplement guest editors were John Beard, The

Pennsylvania State University, University Park, PA and Rebecca Stoltzfus, Johns Hopkins School of Public

Health, Baltimore, MD.

2 This article was commissioned by the World Health Organization (WHO). The views expressed are those of

the authors alone and do not necessarily reflect those of WHO.

3 To whom correspondence and reprint requests should be addressed. Email: [email protected].

Footnote4 Abbreviations: CI, confidence interval; Hb, hemoglobin; HIV, human immunodeficiency virus; PAR, population-

attributable risk.

References26 March 2014 Page 17 of 21 ProQuest


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AuthorAffiliationBernard J. Brabin,3 Mohammad Hakimi* and David Pelletier^

Liverpool School of Tropical Medicine, Liverpool, England and University of Amsterdam, Emma

Kinderziekenhuis, Academic Medical Centre, Amsterdam, Netherlands; *Gadjah Mada University, Yogyakarta,

Indonesia; and Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853

Subject: Case studies; Pregnancy; Anemia; Mortality; Malaria; Iron;MeSH:Acute Disease, Adolescent, Adult, Africa -- epidemiology, Anemia -- epidemiology, Anemia, Iron-Deficiency -- mortality, Asia -- epidemiology, Cause of Death, Chronic Disease, Cross-Sectional Studies,

Female, Folic Acid Deficiency -- mortality, Humans, Latin America -- epidemiology, Longitudinal Studies,

Maternal Mortality, Pregnancy, Pregnancy Complications, Hematologic -- epidemiology, Pregnancy in

Adolescence -- statistics & numerical data, Prevalence, Risk Assessment, Anemia -- mortality (major),

Developing Countries -- statistics & numerical data (major), Pregnancy Complications, Hematologic -- mortality

(major)

Publication title: The Journal of Nutrition

Volume: 131



23/23

Issue: 2S

Supplement: Iron-deficiency Anemia: Reexamining the Nature and...

Pages: 604S-614S; discussion 614S-615S

Number of pages: 12

Publication year: 2001Publication date: Feb 2001

Year: 2001

Publisher:American Institute of Nutrition

Place of publication: Bethesda

Country of publication: United States

Publication subject: Nutrition And Dietetics

ISSN: 00223166CODEN: JONUAI

Source type: Scholarly Journals

Language of publication: English

Document type: Journal Article

Accession number: 11160593

ProQuest document ID: 197424749

Document URL: http://search.proquest.com/docview/197424749?accountid=50268Copyright: Copyright American Institute of Nutrition Feb 2001

Last updated: 2013-01-27

Database: ProQuest Agriculture Journals,ProQuest Nursing & Allied Health Source

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