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Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333
2 To whom correspondence should be addressed. E-mail: rsteketee{at}cdc.gov.
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ABSTRACT |
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 TOP ABSTRACT LITERATURE CITED |
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KEY WORDS: • pregnancy • malaria • anemia • intestinal helminths • parasitic diseases
In the developing world, young women, pregnant women, and their infants and children frequently experience a cycle where undernutrition (macronutrient and micronutrient) and repeated infection lead to adverse consequences that can continue from one generation to the next. Infants born prematurely or with low birth weight (LBW) 3 are at increased risk of early death but are also at risk of poor growth and development in childhood and adolescence. The poor growth resulting in underweight and stunting leaves reproductive-age women at risk in their early pregnancies of delivering premature or LBW infants (1). In addition, the micronutrient deficiencies, particularly iron and folate deficiencies (which contribute to anemia), leave the young women at risk of anemia leading to inadequate oxygen-carrying capacity and risk in pregnancy of delivering premature or LBW infants (1). This cycle (Fig. 1) is affected in each age group (infants, children, adolescents and reproductive-age or pregnant women) by prevalent parasitic infections. Of particular note, malaria and hookworm infections are widely prevalent in poor areas and both are recognized as contributing importantly to this cycle (3, 4). Other parasitic infections may be less common or more geographically localized but also contribute to this cycle.
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Preexisting conditions in young nonpregnant women of reproductive age
The health status of young women before pregnancy is a critical determinant of the risks that may ensue during pregnancy. Young women who experience one or more problems, including stunting, low weight, anemia through its multiple causes or chronic infection, will start a pregnancy at great disadvantage. Women who are underweight or stunted, those with anemia from one or more causes (e.g., iron deficiency, malaria, intestinal helminth infection) and those with certain infectious diseases (e.g., malaria) are at increased risk of delivering LBW infants (1, 3, 5, 6). LBW and premature infants have a much increased risk of early child mortality (7– 9) and impaired growth and cognitive development (10, 11).
Parasitic infections, nutrition and pregnancy
Malaria. Malaria infection is endemic across the tropics and subtropics; affects people in more than 90 countries; causes 300–500 million infections each year; and is estimated to lead to approximately 1 million deaths each year, mostly in young children (12, 13). Most infections and the most severe morbidity and mortality are caused by Plasmodium falciparum. The other three human malaria parasites (P. vivax, P. malariae and P. ovale) contribute to fewer infections and to more moderate disease and relatively few deaths (14). Most P. falciparum infections and consequences are in sub-Saharan Africa, but Asia, Southeast Asia and the Americas are also sites of transmission for this parasite. Although a few reports of adverse consequences of P. vivax in pregnancy exist (15), P. falciparum is the only human malaria parasite that is more common in pregnant than in nonpregnant women and is the only human parasite with a clear and substantial adverse effect on pregnancy, nutrition during pregnancy and pregnancy outcome (3, 16, 17).
Erythrocytes infected with P. falciparum congregate in the maternal placental vascular space where the sinusoidal and low pressure blood flow, and possibly parasite adherence to endothelial cells (18), allow parasites to sequester and replicate. An active immune response involving antibody production, cytokine release and a cellular response (principally a basophilic monocytic macrophage response) is frequently observed in malaria-infected placentas (19). The infection and, possibly, aspects of the immune response contribute to poor pregnancy outcomes of prematurity and fetal intrauterine growth retardation (IUGR) (9, 20). These adverse consequences appear to be mediated through several different pathways. The effect on prematurity is not entirely clear, but women with an active parasite infection and a fetus exposed to parasitized maternal erythrocytes (9) may develop an immunologic response that contributes to stimulus of early onset of labor. The effect of malaria on IUGR appears to be basic to the system of nutrient transport to the fetus. High-density or prolonged parasite infection in placental blood and the consequent cellular immune response may require substantial nutrients and thus leave less nutrient (glucose and oxygen) available for passage to the fetus. In addition, histopathologic studies of malaria-infected placentas demonstrate thickening of cytotrophoblastic membranes, which may alter nutrient transport to the fetus (19). Although the details of these biological processes are difficult to study except when the placenta is delivered, the overwhelming evidence of many studies suggests a clear adverse effect of malaria on LBW and prematurity (3, 21).
Malaria also clearly contributes to anemia throughout life and specifically during pregnancy. In a recent review of studies of P. falciparum–related anemia in pregnant women, Guyatt and Snow (22) suggest that approximately 400,000 pregnant women develop moderate or severe anemia (hemoglobin <80 g/L or hematocrit <0.25) each year in sub-Saharan Africa as a result of malaria infection. Studies have shown that maternal anemia contributes independently to LBW through IUGR (19, 23, 24) and to infant mortality (24). Although the specific biological processes are not clearly delineated, the contribution of moderate and severe anemia to poor oxygen transport to the developing fetus is a likely mode of action for anemia's adverse effect on fetal growth. In addition, malaria-associated anemia in the mother likely has important consequences on her outcome whereby already anemic women are at increased risk of severe consequences (e.g., hypotension, shock, death) even with a moderate ante- or postpartum hemorrhage.
Malaria in early childhood has long been thought to contribute to lasting undernutrition. Recently, in intervention studies with very malaria-specific interventions (e.g., insecticide-treated bed nets), malaria prevention was shown to substantially reduce the frequency of early stunting in children (25), suggesting that malaria contributes directly to stunting and that this is reversible in early childhood. This malaria effect on stunting then contributes further to the cycle noted above where poor nutrition in childhood (e.g., early and recurrent infection with P. falciparum) leads to short and small reproductive-age women who risk a poor pregnancy outcome.
With the development and rapid expansion of the HIV epidemic, particularly in sub-Saharan Africa, investigators have observed the worsening of malaria and its consequences in pregnancy. In malaria-endemic settings, women with HIV infection are at greater risk of having malaria, placental malaria infection and higher-density parasitemias with the infection; both HIV and malaria contribute independently to maternal anemia and LBW infants (26– 30). Although not as clearly documented, the effect of HIV on nutrition has been described for iron, folate, vitamin A and other deficiencies (31– 33), and dual HIV and malaria (or other parasite) infection may have a substantial effect on nutrition.
Treatment of malaria during pregnancy is highly effective in clearing or reducing placental infection, anemia and LBW consequences (3). Because of the high frequency of P. falciparum infection in many African settings, a preemptive approach using intermittent preventive treatment at regularly scheduled antenatal clinic visits and providing insecticide-treated bed nets for each pregnant woman has been shown to be highly effective; this approach was adopted by the Roll Back Malaria partnership and established as policy in a number of countries (3, 25, 34). Studies have shown that additional supplementation of iron (35) and other micronutrients, possibly including vitamin A (36) and folate (37), should be coupled with antimalarial use for anemia and LBW prevention in pregnancy (36).
Intestinal nematodes. Intestinal worm infections are common worldwide but thrive in poor communities in the tropics where poor water supply and poor sanitation are common. The burden of infection is estimated to exceed 1000 million infected persons each for roundworm (Ascaris lumbricoides), hookworm (Ancylostoma duodenal and Necator americanus) and whipworm (Trichuris trichiura) (38, 39). Although acute symptoms of infection are uncommon, numerous studies have shown a consistent association between intestinal nematode infection and diminished food intake and weight loss (40– 42).
Of particular note, hookworm infection causes mechanical laceration and enzymatic damage to the mucosa of the small intestine leading to approximately 0.05 mL/d of blood loss per adult Necatur americanus and approximately 0.25 mL/d per adult Ancyclostoma duodenale (43). The hypochromic microcytic anemia follows chronic infection within 3–5 mo after exposure. These infections may predominate in young and school-age children but their consequences in chronic undernutrition and anemia in reproductive-age women are considerable. Data from the early 1990s suggest that 44 million of the developing world's 124 million pregnant women harbored hookworm infection (44). Although it has been difficult to measure and attribute the LBW and decreased child growth caused by hookworm, recent intervention trials using effective drugs against intestinal helminths showed significant improvements in child weight, weight for age and weight for height (45). The gastrointestinal blood loss, malabsorption and appetite inhibition (46) may further aggravate the iron, zinc and protein-energy deficiencies and the anemia of pregnancy. Intervention studies suggest that even relatively light hookworm infections may decrease fetal growth and weight gain in pregnancy (47).
The World Health Organization recommends four antihelminthic drugs for the control of intestinal nematodes including hookworm and a World Health Organization Informal Consultation suggested that the drugs albendazole, levamisole, mebendazole, pyrantel and praziquantel could be used in strategies designed to improve the health, development and nutritional status of girls and women and that single-dose, oral anthelminthic treatment can also be given to pregnant and lactating women (stressing that these drugs should not be used in the first trimester of pregnancy as a general precautionary measure) (48– 50).
Other parasitic infections. The specific effect of other parasitic infections on nutritional factors affecting pregnancy and pregnancy outcomes is less well documented. The frequency and geographic distribution of some of these infections is great (e.g., schistosomiasis, filariasis, giardiasis) but other infections are more localized or relatively less common in reproductive-age women. Information on many of the specific effects of acute parasite infections during pregnancy or with congenital infection has been reviewed elsewhere (51). Although it is easy to imagine that infection with any of these parasites is not good for the nutritional status of pregnant women, specific data for each of these parasitic diseases are limited. As a consequence—and not because of their importance or the importance of their control in the broader population—the priority placed on these diseases for specific pregnancy-focused intervention strategies is currently lower than the priority for malaria and intestinal helminths. Some of the common parasites are briefly discussed below in this context.
Schistosomiasis, principally caused by S. haematobium, S. japonicum and S. mansoni, is endemic in 74 countries and infects more than 200 million people worldwide (52). Child growth patterns and school performance are adversely affected by infection but are reversible with therapy. Women of reproductive age may experience genital tract infection with disease in the pelvis affecting the renal system and the genital tract including salpingitis and tubal obstruction with possible ectopic pregnancy. As a systemic disease that causes anemia, schistosomiasis may have consequences similar to those described for hookworm infection. Investigators have demonstrated this blood loss and anemia from S. mansoni, S. japonicum and S. haematobium (53, 54). Some case reports of congenital infection exist and S. haematobium eggs have been recognized in placental blood (55), but other than the anemia noted above, there is little documentation of other widespread pregnancy-associated consequences of schistosomiasis. Because the treatment for schistosomiasis with praziquantel is relatively simple and considered safe at least in the second and third trimester of pregnancy, case management during pregnancy can be considered and would likely have important benefits in endemic settings (49, 50).
Filariasis is endemic in more than 80 countries and an estimated 120 million people are infected (two-thirds of infected people are in India and sub-Saharan Africa) (56). This blood-born parasite leads to local inflammation with lymph node involvement, including in the pelvis and possibly affecting reproductive organs; there is little evidence that it contributes to specific adverse nutritional outcomes (45).
African trypanosomiasis (sleeping sickness caused by Trypanosoma gambiense or T. rhondesiensi) and American trypanosomiasis (Chagas disease caused by T. cruzi) affect substantial populations in their respective continents and can infect women during pregnancy and lead to congenital infection of the newborn. However, other than the general effect of systemic illness on limiting food intake and causing increased energy requirements for coping with the infection, there is no evidence for specific effects on maternal or fetal nutritional status.
Many other parasitic diseases may have acute systemic consequences in infected individuals, which may include pregnant women, but they have no broader documented contribution to nutritional deficiencies during pregnancy. Other reviews of these parasitic infections can be consulted for further information on case identification and management (51, 54, 57, 58).
Micronutrient deficiencies and parasitic infections
The consequences of parasitic infections on human nutrition and the consequences of undernutrition on parasitic infections and their outcomes are clearly intertwined. Recent reviews of micronutrient malnutrition and malarial anemia (59); malnutrition and parasitic helminth infections (4); and malnutrition, infection and immunity (60) suggest a strong link among protein-energy malnutrition, micronutrient deficiency, infection and bad outcomes. Some of the general knowledge regarding interactions among micronutrient deficiency, anemia and infections with parasites are summarized in Table 1. Although these interactions are not specific to pregnancy, the increased demands on micronutrients during pregnancy exacerbate the deficiency and its consequences.
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Intervention opportunities
Because the cycle of infection (Fig. 1) suggests that for many parasitic infections the effect may occur both during pregnancy and well before pregnancy, various opportunities to intervene may exist (82, 83). In general, no one will declare that a drug for parasitic infections is safe during pregnancy. Thus, where possible, priority should be given to treating or preventing infections either before the first pregnancy or between pregnancies. For conditions that are diagnosed during pregnancy or that must be treated or prevented during pregnancy (e.g., anemia, malaria, hookworm), the safety of the treatment must be balanced with the adverse consequences of the disease.
Currently, reproductive health programs encourage public health approaches during pregnancy for anemia, malaria and hookworm prevention and treatment because the substantial adverse consequences outweigh any risk associated with the prevention and treatment. These are meant to be part of routine antenatal care services provided particularly during the second and third trimester of pregnancy when the risk of the drugs for the mother and the developing fetus is thought to be small and the benefits have been clearly documented. In the developing world, relatively few women come for care before quickening, so this preventive management approach is well suited to begin with the first antenatal clinic visit. Because a relatively high proportion of pregnant women attend an antenatal clinic at least once (e.g., Demographic and Health Surveys show that in 30 sub-Saharan African countries with recent surveys, >70% of all pregnant women attended an antenatal clinic at least once in most (22 of 30) counties [61] ; Fig. 2). This strategy of incorporating services within existing antenatal clinic systems is likely to reach a high proportion of at-risk women and could substantially interrupt the cycle of infection, undernutrition and adverse reproductive outcome.
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Approaches to the diagnosis and treatment of less common parasitic diseases presenting as acute infection during pregnancy are likely to be addressed case by case. Recommendations for the management of these acute infections can be found elsewhere (57, 58, 90). Unless the infection threatens the pregnancy, many of the treatments are best postponed to the postpartum period.
Because many of the infections and nutritional consequences are chronic, the intervention strategies must consider opportunities for diagnosis and management or preemptive prevention before pregnancy. This is particularly true for anemia and the intestinal helminths; many women enter a pregnancy with these as preexisting conditions. Opportunities to engage young, nonpregnant women for preventive health efforts will be important but are not a reality in many developing countries. An opportunity certainly exists for women attending school but because education is not universally available and the poorest women are least likely to attend school and most likely to be exposed to the diseases, strategies to reach the women at greatest risk must consider other community-based options (44).
Future research needs
Because intervention programs are always best applied from a sound scientific basis of understanding of the disease, its consequences, its points of attack and the ability to introduce the interventions into existing programs, public health professionals have ongoing needs for research in all of the parasitic infections noted above. A review of research needs on the interactions of certain parasitic diseases (malaria, schistosomiasis, amebiasis, giardiasis, ascariasis and hookworm) and nutrition in humans was discussed approximately 20 y ago (91). Although some work has been done to clarify some of the questions, other questions remain unanswered. Further information is needed today on macro- and micronutrients during pregnancy and on interactions between them and parasitic diseases. A clear example of the needs are seen in the editorial on anemia and pregnancy in sub-Saharan Africa (5), where the problem is enormous. Our understanding has evolved, yet we still do not have clarity on a strategy and effective delivery methods for a package of micronutrient supplement coupled with malaria prevention and other parasitic or bacterial disease treatment or prevention.
For malaria and intestinal helminths and their contributions to anemia, existing information on the adverse consequences of infection before and during pregnancy provides sufficient justification for active programs. However, few programs fully implement these proven strategies and further knowledge is required to
For the other parasitic diseases, especially those with wide geographic distribution, additional studies are needed to
Overall, as evidenced by the information reviewed here, relatively little information exists on 1) the specific interaction in pregnancy between parasitic diseases and deficiencies in general nutrition and micronutrients, or 2) the benefit and role for linked infection prevention/treatment and general nutrition/micronutrients supplementation. Because of the clear links among poverty, undernutrition and infection, a systematic evaluation is needed of both macronutrient and micronutrient deficiencies and the benefits of supplementation in combination with systematic treatment or prevention for the infectious diseases, especially the parasitic diseases mentioned. This systematic approach should focus on the at-risk population of pregnant women but should also consider these issues in young children, adolescent girls and women between pregnancies. The approach should address both biological interactions (e.g., among micronutrients, malaria, other parasites, anemia and adverse outcomes) and programmatic interactions, where commonalities in service delivery opportunities might allow for joint delivery of interventions.
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FOOTNOTES |
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3 Abbreviations used: IUGR, intrauterine growth retardation; LBW, low birth weight.
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LITERATURE CITED |
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TOPABSTRACTLITERATURE CITED |
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1. Stephenson, L. S., Latham, M. C. & Ottesen, E. A. (2000) Global malnutrition. Parasitology 121: S5–S22.
2. Administrative Committee on Coordination/Sub Committee in Nutrition. (ACC/SCN) (2000) Fourth Report on the World Nutrition Situation. ACC/SCN, Geneva, Switzerland.
3. Steketee, R. W., Nahlen, B. L., Parise, M. E. & Menendez, C. (2001) The burden of malaria in pregnancy in malaria-endemic areas. Am. J. Trop. Med. Hyg. 64 (Suppl. 1–2), 28–35.[Abstract]
4. Stephenson, L. S., Latham, M. C. & Ottesen, E. A. (2000) Malnutrition and parasitic helminth infections. Parasitology 121 (Suppl.), S23–S38.
5. Van den Broek, N. (2001) Anaemia in pregnancy in sub-Saharan countries. Eur. J. Obstet. Gynecol. Reprod. Biol. 96: 4–6.[Medline]
6. Shulman, C. E., Dorman, E. K., Cutts, F., Kawuondo, K., Bulmer, J. N., Peshu, N. & Marsh, K. (2001) Malaria in pregnancy: adverse effects on haemoglobin levels and birthweight in primigravidae and multigravidae. Trop. Med. Int. Health 6: 1–9.[Medline]
7. McCormick, M. C. (1985) The contribution of low birth weight to infant mortality and childhood mortality. N. Engl. J. Med. 312: 82–90.[Abstract]
8. Greenwood, A. M., Armstrong, J. R. M., Byass, P., Snow, R. W. & Greenwood, B. M. (1992) Malaria chemoprophylaxis, birth weight and child survival. Trans. R. Soc. Trop. Med. Hyg. 86: 483–485.[Medline]
9. Steketee, R. W., Wirima, J. J., Hightower, A. W., Slutsker, L., Heymann, D. L. & Breman, J. G. (1996) The effect of malaria and malaria prevention in pregnancy on offspring birth weight, prematurity, and intrauterine growth retardation in rural Malawi. Am. J. Trop. Med. Hyg. 55 (Suppl. 1), 33–41.
10. McCormick, M. C., Brooks-Gunn, J., Workman-Daniels, K., Turner, J. & Peckham, G. J. (1992) The health and developmental status of very low-birth-weight children at school age. JAMA 267: 2204–2208.
11. Teplin, S. W., Burchinal, M., Johnson-Martin, N., Humphry, R. A. & Kraybill, E. N. (1991) Neurodevelopmental, health, and growth status at age 6 years of children with birth weights less than 1001 grams. J. Pediatr. 118: 768–777.[Medline]
12. Breman, J. G. (2001) The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am. J. Trop. Med. Hyg. 64 (Suppl. 1–2), 1–11.[Abstract]
13. Murphy, S. C. & Breman, J. G. (2001) Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am. J. Trop. Med. Hyg. 64 (Suppl. 1–2), 57–67.
14. Mendis, K., Sina, B. J., Marchesini, P. & Carter, R. (2001) The neglected burden of Plasmodium vivax malaria. Am. J. Trop. Med. Hyg. 64 (Suppl. 1–2), 97–106.
15. Nosten, F., McGready, R., Simpson, J. A., Thwa, K. L., Balkan, S., Cho, T., Hkirijaroen, L., Looareesuwan, S. & White, N. J. (1999) Effects of Plasmodium vivax malaria in pregnancy. Lancet 354: 546–549.[Medline]
16. Brabin, B. J. (1991) The risks and severity of malaria in pregnant women. World Health Organization Applied Field Research in malaria Reports, No.1. WHO, Geneva, Switzerland.
17. McGregor, I. A., Wilson, M. E. & Billewicz, W. Z. (1983) Malaria infection of the placenta in The Gambia, West Africa: its incidence and relationship to stillbirth, birth weight, and placental weight. Trans. R. Soc. Trop. Med. Hyg. 77: 232–244.[Medline]
18. Beeson, J. G., Reeder, J. C., Rogerson, S. J. & Brown, G. V. (2001) Parasite adhesion and immune evasion in placental malaria. Trends Parasitol. 17: 331–337.[Medline]
19. Ismail, M. R., Ordi, J., Menendez, C., Ventura, P. J., Aponte, J. J., Kahigwa, E., Hirt, R., Cardesa, A. & Alonso, P. L. (2000) Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Hum. Pathol. 31: 85–93.[Medline]
20. Menendez, C., Ordi, J., Ismail, M. R., Ventura, P. J., Aponte, J. J., Kahigwa, E., Font, F. & Alonso, P. L. (2000) The impact of placental malaria on gestational age and birth weight. J. Infect. Dis. 181: 1740–1745.[Medline]
21. Garner, P. & Brabin, B. (1994) A review of randomized controlled trials of routine antimalarial drug prophylaxis during pregnancy in endemic malarious areas. Bull. World Health Organ. 72: 89–99.[Medline]
22. Guyatt, H. L. & Snow, R. W. (2001) The epidemiology and burden of Plasmodium falciparum-related anemia among pregnant women in sub-Saharan Africa. Am. J. Trop. Med. Hyg. 64 (Suppl.1–2), 36–44.
23. Brabin, B. & Piper, C. (1997) Anaemia-and malaria-attributable low birth weight in two populations in Papua New Guinea. Ann. Hum. Biol. 24: 547–555.[Medline]
24. Verhoeff, F. H., Brabin, B. J., Chimsuku, L., Kazembe, P. & Broadhead, R. L. (2000) Malaria in pregnancy and its consequences for the infant in rural Malawi. Ann. Trop. Med. Parasitol. 93 (Suppl. 1), S25–S33.
25. ter Kuile, F. O., Terlouw, D. J., Kariuki, S. K., Phillips-Howard, P. A., Mirel, L. B., Hawley, W. A., Friedman, J. F., Shi, Y. P., Kolczak, M. S., Lal, A. A., Vulule, J. M. & Nahlen, B. L. (2003) Impact of permethrin-treated bednets on malaria, anemia and growth in infants in an area of intense perennial malaria transmission in western Kenya. Am. J. Trop. Med. Hyg., in press.
26. van Eijk, A. M., Ayisi, J. G., ter Kuile, F. O., Misore, A., Otieno, J., Kolczak, M. S., Kager, P., Steketee, R. W. & Nahlen, B. L. (2001) Human immunodeficiency virus infection and malaria as risk factors for third trimester anemia in asymptomatic pregnant Kenyan women. Am. J. Trop. Med. Hyg. 65: 623–630.[Abstract]
27. Steketee, R. W., Wirima, J. J., Bloland, P. B., Chilima, B., Mermin, J. H., Chitsulo, L. & Breman, J. G. (1996) Impairment of a pregnant woman's acquired ability to limit Plasmodium falciparum by infection with human immunodeficiency virus type–1. Am. J. Trop. Med. Hyg. 55 (Suppl. 1), 42–49.
28. Parise, M. E., Ayisi, J. G., Nahlen, B. L., Schultz, L. H. J., Roberts, J. M., Misore, A., Muga, R., Oloo, A. J. & Steketee, R. W. (1998) Efficacy of sulfadoxine-pyrimethamine for prevention of placental malaria in an area of Kenya with a high prevalence of malaria and human immunodeficiency virus infection. Am. J. Trop. Med. Hyg. 59: 813–822.[Abstract]
29. Verhoeff, F. H., Brabin, B. J., Hart, C. A., Chimsuku, L., Kazembe, P. & Broadhead, R. L. (1999) Increased prevalence of malaria in HIV–infected pregnant women and its implications for malaria control. Trop. Med. Int. Health 4: 5–12.[Medline]
30. Corbett, E. L., Steketee, R. W., ter Kuile, F. O., Latif, A. S., Kamali, A. & Hayes, J. (2002) HIV–1/AIDS and the control of other infectious diseases in Africa. Lancet 359: 2177–2187.[Medline]
31. Friis, H., Gomo, E., Koestel, P., Ndhlovu, P., Nyazema, N., Krarup, H. & Michaelsen, K. F. (2001) HIV and other predictors of serum folate, serum ferritin, and hemoglobin in pregnancy: a cross-sectional study in Zimbabwe. Am. J. Clin. Nutr. 73: 1066–1073.
32. Friis, H., Gomo, E., Koestel, P., Ndhlovu, P., Nyazema, N., Krarup, H. & Michaelsen, K. F. (2001) HIV and other predictors of serum beta-carotene and retinol in pregnancy: a cross-sectional study in Zimbabwe. Am. J. Clin. Nutr. 73: 1058–1065.
33. Friis, H. & Michaelsen, K. F. (1998) Micronutrients and HIV infection: a review. Eur. J. Clin. Nutr. 52: 157–163.[Medline]
34. Nahlen, B. L. (2000) Rolling back malaria in pregnancy. N. Engl. J. Med. 343: 651–652.
35. Mahomed, K. (2000) Iron supplementation in pregnancy. Cochrane Database Syst. Rev. 2: CD000117.
36. Dreyfuss, M. L., Stoltzfus, R. J., Shrestha, J. B., Pradhan, E. K., LeClerq, S. C., Khatry, S. K., Shrestha, S. R., Katz, J., Aolbonico, M. & West, K. P., Jr. (2000) Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J. Nutr. 130: 2527–2536.
37. Mahomed, K. (2000) Iron and folate supplementation in pregnancy. Cochrane Database Syst. Rev. 2: CD001135.
38. Crompton, D. W. T. (1999) How much human helminthiasis is there in the world? J. Parasitol. 85: 397–403.[Medline]
39. Crompton, D. W. T. (2000) The public health importance of hookworm disease. Parasitology 121: S39–S50.
40. Latham, M. C., Stephenson, L. S., Kurz, K. M. & Kinoti, S. N. (1990) Metrifonate or praziquantel treatment improves physical fitness and appetite of Kenyan schoolboys with Schistosoma haematobium and hookworm infections. Am. J. Trop. Med. Hyg. 43: 170–179.
41. Stephenson, L. S., Latham, M. C., Adams, E. J., Kinoti, S. K. & Pertet, A. (1993) Weight gain of Kenyan school children infected with hookworm, Trichuris trichiura, Ascaris lumbricoides is improved following once- or twice-yearly treatment with albendazole. J. Nutr. 123: 656–665.
42. Hadju, V., Stephenson, L. S., Abadi, K., Mohammed, H. O., Bowman, D. D. & Parker, R. S. (1996) Improvements in appetite and growth in helminth-infected schoolboys three and seven weeks after a single dose of pyrantel pamoate. Parasitology 113: 497–504.
43. MacLeod, C. L. (1988) Intestinal nematode infections. In: Parasitic Infections in Pregnancy and the Newborn (MacLeod, C. L., ed.), pp. 192–215. Oxford University Press, New York.
44. World Health Organization. (1994) Report of the WHO Informal Consultation on Hookworm Infection and Anaemia in Girls and Women, Geneva. WHO/CDS/IPI/95.1. WHO, Geneva, Swizerland.
45. Beach, M. J., Streit, T. B., Addiss, D. G., Prospere, R., Roberts, J. M. & Lammie, P. J. (1999) Assessment of combined ivermectin and albendazole for treatment of intestinal helminth and Wuchereria bancrofti infections in Haitian schoolchildren. Am. J. Trop. Med. Hyg. 60: 479–486.[Abstract]
46. Cline, B. L., Little, M. D., Bartholomew, R. K. & Halsey, N. A. (1984) Larvicidal activity of albendazole against Necator americanus in human volunteers. Am. J. Trop. Med. Hyg. 33: 387–394.
47. Torlesse, H. & Hodges, M. (2001) Albendazole therapy and reduced decline in haemoglobin concentration during pregnancy. Sierra Leone. Trans. R. Soc. Trop. Med. Hyg. 95: 195–201.[Medline]
48. World Health Organization. (1996) Report of the WHO Informal Consultation on the use of Chemotherapy for the Control of Morbidity due to Soil-transmitted Nematodes in Humans (WHO/CTD/SIP/96.2) WHO, Geneva, Switzerland.
49. World Health Organization. (1999) Monitoring Helminth Control Programs (WHO/CDS/CPC/SIP/99.3). WHO, Geneva, Switzerland.
50. World Health Organization. (1998) Report of the WHO Informal Consultation on Schistosomiasis Control (WHO/CDS/CPC/SIP/99.2) WHO, Geneva, Switzerland.
51. MacLeod, C. L. (ed) . (1988) Parasitic Infections in Pregnancy and the Newborn. Oxford University Press, New York.
52. World Health Organization. Schistosomiasis. http://www.who.int/ctd/schisto/burdens.htm (accessed Dec. 1, 2000).
53. Farid, Z., Bassily, S., Schulert, A. R., Raasch, F., Zeind, A. S., El Rooby, A. S. & Sherif, M. (1967) Blood loss in chronic Schistosoma mansoni infection in Egyptian farmers. Trans. R. Soc. Trop. Med. Hyg. 61: 621–625.[Medline]
54. Stephenson, L. S. (1987) Impact of Helminth Infections on Human Nutrition. Taylor and Francis Ltd, London and Philadelphia.
55. Renaud, R., Brettes, P., Carrie, J., Castanier, C., Renaud, L., Chesnet, Y., Doucet, J. & Loubiere, R. (1971) Bilharziasis of the internal female genital organs. Rev. Fr. Gynecol. Obstet. 66: 1–18.[Medline]
56. World Health Organization. Eliminating Lymphatic Filariassis. http://www.who.int/ctd/filariasis/disease_status/burdens.html (accessed Dec. 1, 2000).
57. Lee, R. V. (1982) Parasitic Infestations. In: Medical complications during pregnancy (Burrow, G. N. & Ferris, T. F., eds.), pp. 386–404. 2nd ed. Saunders Co. Philadelphia, PA.
58. Gilbert, G. L. (1991) infectious disease in pregnancy and the newborn infant. Harwood Academic Publ, GmbH, Chur, Switzerland.
59. Nussenblatt, V. & Semba, R. D. (2002) Micronutrient malnutrition and the pathogenesis of malarial anemia. Acta Trop. 82: 321–327.[Medline]
60. Scrimshaw, N. S. & Sangiovanni, J. P. (1997) Synergism of nutrition, infection, and immunity: an overview. Am. J. Clin. Nutr. 66: 464S–477S.
61. DHS+. Selected Statistics in DHS Surveys. DHS+ Dimensions Newsletter 2:12. Available at http://www.measuredhs.com/pubs/pdf/NL22/NL22.pdf (accessed Dec. 3, 2000).
62. Pedersen, S., Saeed, I., Friis, H. & Michaelsen, K. F. (2001) Effect of iron deficiency on Trichuris suis and Ascaris suum infections in pigs. Parasitology 122: 589–598.[Medline]
63. Olsen, A., Nawiri, J. & Friis, H. (2000) The impact of iron supplementation on reinfection with intestinal helminths and Schistosoma mansoni in western Kenya. Trans. R. Soc. Trop. Med. Hyg. 94: 493–499.[Medline]
64. Pedersen, S., Saeed, I., Jensen, S. K., Michaelsen, K. F. & Friis, H. (2001) Marginal vitamin A deficiency in pigs experimentally infected with Trichuris suis: a model for vitamin A inadequacy in children. Trans. R. Soc. Trop. Med. Hyg. 95: 557–565.[Medline]
65. Kaestel, P., Lewis, F. J., Willingham, A. L., Bogh, H. O., Eriksen, L., Michaelsen, K. F., Sandstrom, B., Hoy, C. E. & Friis, H. (1999) Schistosoma japonicum infection and serum and tissue concentrations of retinol and zinc in pigs. Ann. Trop. Med. Parasitol. 93: 489–499.[Medline]
66. Friis, H., Andersen, C. B., Vennervald, B. J., Christensen, N. O. & Pakkenberg, B. (1998) The use of stereological method to estimate the volume of Schistosoma mansoni granulomas: the effect of zinc deficiency. Ann. Trop. Med. Parasitol. 92: 785–792.[Medline]
67. Friis, H., Ndhlovu, P., Mduluza, T., Kaondera, K., Sandstrom, B., Michaelsen, K. F., Vennervald, B. J. & Christensen, N. O. (1997) The impact of zinc supplementation on Schistosoma mansoni reinfection rate and intensities: a randomized, controlled trial among rural Zimbabwean school children. Eur. J. Clin. Nutr. 51: 33–37.[Medline]
68. Baek, J., Simonsen, P. E., Friis, H. & Christensen, N. O. (1996) Zinc deficiency and host response to helminth infection: Echinostoma caproni infections in CBA mice. J. Helminthol. 70: 7–12.[Medline]
69. Beard, J. L. (2000) Effectiveness and strategies of iron supplementation during pregnancy. Am. J. Clin. Nutr. 71: 1288S–1294S.
70. Allen, L. H. (2000) Anemia and iron deficiency: effects on pregnancy outcome. Am. J. Clin. Nutr. 71: 1280S–1284S.
71. United Nations Administrative Committee on Coordination/Subcommittee on Nutrition. (1991) Controlling iron deficiency. Nutrition policy discussion paper No. 9. WHO, Geneva, Switzerland.
72. Institute of Medicine. (1993) Iron Deficiency Anemia: Recommended Guidelines for the Prevention, Detection, and Management Among US Children and Women of Childbearing Age. National Academy Press, Washington, DC.
73. Bailey, L. B. (2000) New standard for dietary folate intake in pregnant women. Am. J. Clin. Nutr. 71: 1304S–1307S.
74. Scholl, T. O. & Johnson, W. G. (2000) Folic acid: influence on the outcome of pregnancy. Am. J. Clin. Nutr. 71: 1295S–1303S.
75. McNulty, H., Cuskelly, G. J. & Ward, M. (2000) Response of red blood cell folate to intervention: implications for folate recommendations for the prevention of neural tube defects. Am. J. Clin. Nutr. 71: 1308S–1311S.
76. World Health Organization. (2000) WHO Expert Committee on Malaria 20th Report. Technical Report Series No. 892. WHO. Geneva, Switzerland.
77. Azais-Braesco, V. & Pascal, G. (2000) Vitamin A in pregnancy: requirements and safety limits. Am. J. Clin. Nutr. 71: 1325S–1333S.
78. World Health Organization. (1998) Safe Vitamin A Dosage During Pregnancy and Lactation. Recommendations and Report from a Consultation. Micronutrient Series (WHO.NUT/98.4) WHO Geneva, Switzerland.
79. World Health Organization. (1996) Trace elements in human nutrition and health. WHO, Geneva, Switzerland.
80. Viteri, F. E. (1997) Iron supplementation for the control of iron deficiency in populations at risk. Nutr. Rev. 55: 195–209.[Medline]
81. King, J. C. (2000) Determinants of maternal zinc status during pregnancy. Am. J. Clin. Nutr. 71: 1334S–1343S.
82. Mora, J. O. & Nestel, P. S. (2000) Improving prenatal nutrition in developing countries: strategies, prospects, and challenges. Am. J. Clin. Nutr. 71: 1353S–1363S.
83. Mora, O. (2002) Iron supplementation: overcoming technical and practical barriers. J. Nutr. 132: 853S–855S.
84. Oppenheimer, S. J. (2001) Iron and its relation to immunity and infectious disease. J. Nutr. 131: 616S–633S.
85. Snow, R. W., Byass, P., Shenton, F. C. & Greenwood, B. M. (1991) The relationship between anthropometric measurements and measurements of iron status and susceptibility to malaria in Gambian children. Trans. R. Soc. Trop. Med. Hyg. 85: 584–589.[Medline]
86. Keusch, G. T. (1990) Micronutrients and susceptibility to infection. Ann. N. Y. Acad. Sci. 587: 181–188.[Medline]
87. Menendez, C., Kahigwa, E., Hirt, R., Vounatsou, P., Aponte, J. J., Font, F., Acosta, C. J., Schellenberg, D. M., Galindo, C. M., Kimario, J., Urassa, H., Brabvin, B., Smith, T. A., Kitua, A. Y., Tanner, M. & Alonso, P. L. (1997) Randomized placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet 350: 844–850.[Medline]
88. Verhoef, H., West, C. E., Nzyuko, S. M., de Vogel, S., van der Valk, R., Wanga, M. A., Kuijsten, A., Veenemans, J. & Kok, F. J. (2002) Intermittent administration of iron and sulfadoxine-pyrimethamine to control anemia in Kenyan children: a randomised controlled trial. Lancet 360: 908–914.[Medline]
89. International Nutritional Anemia Consultative Group (INACG). (1998) Safety of Iron Supplementation Programs in Malaria Endemic Regions. ILSI Press, Washington. DC.
90. Horton, J. (2000) Albendazole: a review of anthelminthic efficacy and safety in humans. Parasitology 121: S133–S146.
91. Latham, M. C. (1982) Needed research on the interactions of certain parasitic diseases and nutrition in humans. Rev. Infect. Dis. 4: 896–900.[Medline]
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