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-
1.
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, 2006. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411–425.
-
2.
Global Network, 2009. Schistosomiasis Fact Sheet. Available at: http://globalnetwork.org/about-ntds/factsheets. Accessed August 20, 2009.
-
3.
King CH, Dickman K, Tisch DJ, 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 1561–1569.
-
4.
Stephenson L, 1993. The impact of schistosomiasis on human nutrition. Parasitology 107 (Suppl): S107–S123.
-
5.
Nelson M, 1996. Anaemia in adolescent girls: effects on cognitive function and activity. Proc Nutr Soc 55: 359–367.
-
6.
Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21: 386–392.
-
7.
United Nations Administrative Committee on Coordination, Standing Committee on Nutrition, 2000. Fourth Report on the World Nutrition Situation: Nutrition throughout the Life Cycle. Available at: http://www.unscn.org/layout/modules/resources/files/rwns4.pdf. Accessed July 20, 2010.
-
8.
Koukounari A, Estambale BB, Njagi JK, Cundill B, Ajanga A, Crudder C, Otido J, Jukes MC, Clarke SE, Brooker S, 2008. Relationships between anaemia and parasitic infections in Kenyan schoolchildren: a Bayesian hierarchical modelling approach. Int J Parasitol 38: 1663–1671.
-
9.
Tolentino K, Friedman JF, 2007. An update on anemia in less developed countries. Am J Trop Med Hyg 77: 44–51.
-
10.
Friedman JF, Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Wu H, Olveda RM, McGarvey ST, Kurtis JD, 2005. Relationship between Schistosoma japonicum and nutritional status among children and young adults in Leyte, the Philippines. Am J Trop Med Hyg 72: 527–533.
-
11.
Leenstra T, Acosta LP, Langdon GC, Manalo DL, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines. Am J Clin Nutr 83: 371–379.
-
12.
Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2005. Schistosoma japonicum and occult blood loss in endemic villages in Leyte, the Philippines. Am J Trop Med Hyg 72: 115–118.
-
13.
Weiss G, Goodnough LT, 2005. Anemia of chronic disease. N Engl J Med 352: 1011–1023.
-
14.
Malope BI, MacPhail AP, Alberts M, Hiss DC, 2001. The ratio of serum transferrin receptor and serum ferritin in the diagnosis of iron status. Br J Haematol 115: 84–89.
-
15.
Punnonen K, Irjala K, Rajamaki A, 1997. Serum transferrin receptor and its ratio to serum ferritin in the diagnosis of iron deficiency. Blood 89: 1052–1057.
-
16.
Lee EJ, Oh E, Park Y, Lee HK, Kim BK, 2002. Soluble transferrin receptor (sTfR), ferritin, and sTfR/log ferritin index in anemic patients with nonhematologic malignancy and chronic inflammation. Clin Chem 48: 1118–1121.
-
17.
Suominen P, Punnonen K, Rajamaki A, Irjala K, 1998. Serum transferrin receptor and transferrin receptor-ferritin index identify healthy subjects with subclinical iron deficits. Blood 92: 2934–2939.
-
18.
Mast AE, Blinder MA, Gronowski AM, Chumley C, Scott MG, 1998. Clinical utility of soluble transferrin receptor and comparison with serum ferritin in several populations. Clin Chem 44: 45–51.
-
19.
Wish JB, 2006. Assessing iron status: beyond serum ferritin and transferrin saturation. Clin J Am Soc Nephrol 1 (Suppl 1): S4–S8.
-
20.
Ferguson BJ, Skikne BS, Simpson KM, Baynes RD, Cook JD, 1992. Serum transferrin receptor distinguishes the anemia of chronic disease from iron deficiency anemia. J Lab Clin Med 119: 385–390.
-
21.
Ioannou G, Spector J, Scott K, Rockey DC, 2002. Prospective evaluation of a clinical guideline for the diagnosis and management of iron deficiency anemia. Am J Med 113: 281–287.
-
22.
National Kidney Foundation, 2006. Kidney Dialysis Outcome Quality Initiative (KDOQI) Clinical practice guidelines and clinical practice recommendations for anemia in chronic kidney disease. Am J Kidney Dis 47 (Suppl 3): S11–S145.
-
23.
Brugnara C, 2003. Iron deficiency and erythropoiesis: new diagnostic approaches. Clin Chem 49: 1573–1578.
-
24.
Tsang VC, Tsang KR, Hancock K, Kelly MA, Wilson BC, Maddison SE, 1983. Schistosoma mansoni adult microsomal antigens, a serologic reagent. I. Systematic fractionation, quantitation, and characterization of antigenic components. J Immunol 130: 1359–1365.
-
25.
Tsang VC, Hancock K, Maddison SE, Beatty AL, Moss DM, 1984. Demonstration of species-specific and cross-reactive components of the adult microsomal antigens from Schistosoma mansoni and S. japonicum (MAMA and JAMA). J Immunol 132: 2607–2613.
-
26.
Gwatkin DR, Rustein S, Johnson K, Pande R, Wagstaff A, 2000. Socio-Economic Differences in Health, Nutrition and Population in Kenya. Washington, DC: HNP/Poverty Thematic Group, The World Bank.
-
27.
Government of Kenya Ministry of Health, 2002. Nutritional and haematologic conditions. Kimathi NA, Micheni JN, Muriithi A, eds. Clinical Guidelines for Diagnosis and Treatment of Common Conditions in Kenya. Nairobi, Kenya: The Regal Press Kenya Ltd., 190–202.
-
28.
Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T, 2003. Hepcidin, a putative mediator of anemia of inflammation, is a type II acute phase protein. Blood 101: 2461–2463.
-
29.
Ganz T, Olbina G, Girelli D, Nemeth E, Westerman M, 2008. Immunoassay for human serum hepcidin. Blood 112: 4292–4297.
-
30.
Weiss G, 2002. Pathogenesis and treatment of anaemia of chronic disease. Blood Rev 16: 87–96.
-
31.
Weiss G, 2002. Iron and immunity: a double-edged sword. Eur J Clin Invest 32 (Suppl 1): 70–78.
-
32.
Means RT Jr, 2003. Recent developments in the anemia of chronic disease. Curr Hematol Rep 2: 116–121.
-
33.
Cartwright GE, 1966. The anemia of chronic disorders. Semin Hematol 3: 351–375.
-
34.
Matzner Y, Levy S, Grossowicz N, Izak G, Hershko C, 1979. Prevalence and causes of anemia in elderly hospitalized patients. Gerontology 25: 113–119.
-
35.
Oppenheimer SJ, Gibson FD, MacFarlane SB, Moody JB, Harrison C, Spencer A, Bunari O, 1986. Iron supplementation increases prevalence and effects of malaria: report on clinical studies in Papua New Guinea. Trans R Soc Trop Med Hyg 80: 603–612.
-
36.
Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra U, Kabole I, Deb S, Othman MK, Kabole FM, 2006. Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet 367: 133–143.
-
37.
Leenstra T, Coutinho HM, Acosta LP, Langdon GC, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Schistosoma japonicum reinfection after praziquantel treatment causes anemia associated with inflammation. Infect Immun 74: 6398–6407.
-
38.
Olson CL, Acosta LP, Hochberg NS, Olveda RM, Jiz M, McGarvey ST, Kurtis JD, Bellinger DC, Friedman JF, 2009. Anemia of inflammation is related to cognitive impairment among children in Leyte, the Philippines. PLoS Negl Trop Dis 10: e533.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1323 | 1186 | 224 |
| Full Text Views | 442 | 6 | 1 |
| PDF Downloads | 155 | 5 | 1 |
Mechanism of Anemia in Schistosoma mansoni–Infected School Children in Western Kenya
Sara E. Butler
Sara E. Butler
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Erick M. Muok
Erick M. Muok
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Susan P. Montgomery
Susan P. Montgomery
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Keziah Odhiambo
Keziah Odhiambo
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Pauline M. N. Mwinzi
Pauline M. N. Mwinzi
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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W. Evan Secor
W. Evan Secor
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Diana M. S. Karanja
Diana M. S. Karanja
Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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A better understanding of the mechanism of anemia associated with Schistosoma mansoni infection might provide useful information on how treatment programs are implemented to minimize schistosomiasis-associated morbidity and maximize treatment impact. We used a cross-sectional study with serum samples from 206 Kenyan school children to determine the mechanisms in S. mansoni-associated anemia. Serum ferritin and soluble transferrin receptor levels were measured by using an enzyme-linked immunosorbent assay. Results suggest that S. mansoni-infected persons are more likely (odds ratio = 3.68, 95% confidence interval = 1.33–10.1) to have levels of serum ferritin (> 100 ng/mL) that are associated with anemia of inflammation (AI) than S. mansoni-uninfected children. Our results suggest that AI is the most common form of anemia in S. mansoni infections. In contrast, the mechanism of anemia in S. mansoni-uninfected children was iron deficiency. Moreover, the prevalence of AI in the study participants demonstrated a significant trend with S. mansoni infection intensity (P < 0.001). Our results are consistent with those observed in S. japonicum-associated anemia.
Author Notes
Financial support: This study was supported in part by an appointment to the Emerging Infectious Diseases Fellowship Program administered by the Association of Public Health Laboratories and funded by a grant from the Schistosomiasis Research Program at the DBL – Institute for Health Research and Development and the Centers for Disease Control and Prevention.
Authors' addresses: Sara E. Butler, Susan P. Montgomery, and W. Evan Secor, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: saebutler@gmail.com, zqu6@cdc.gov, and was4@cdc.gov. Erick M. Muok, Kezia Odhiambo, Pauline M. N. Mwinzi, and Diana M. S. Karanja, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya, E-mails: EMuok@kemricdc.org, kezahinyi@yahoo.com, PMwinzi@kemricdc.org, and DKaranja@kemricdc.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, 2006. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411–425.
-
2.
Global Network, 2009. Schistosomiasis Fact Sheet. Available at: http://globalnetwork.org/about-ntds/factsheets. Accessed August 20, 2009.
-
3.
King CH, Dickman K, Tisch DJ, 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 1561–1569.
-
4.
Stephenson L, 1993. The impact of schistosomiasis on human nutrition. Parasitology 107 (Suppl): S107–S123.
-
5.
Nelson M, 1996. Anaemia in adolescent girls: effects on cognitive function and activity. Proc Nutr Soc 55: 359–367.
-
6.
Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21: 386–392.
-
7.
United Nations Administrative Committee on Coordination, Standing Committee on Nutrition, 2000. Fourth Report on the World Nutrition Situation: Nutrition throughout the Life Cycle. Available at: http://www.unscn.org/layout/modules/resources/files/rwns4.pdf. Accessed July 20, 2010.
-
8.
Koukounari A, Estambale BB, Njagi JK, Cundill B, Ajanga A, Crudder C, Otido J, Jukes MC, Clarke SE, Brooker S, 2008. Relationships between anaemia and parasitic infections in Kenyan schoolchildren: a Bayesian hierarchical modelling approach. Int J Parasitol 38: 1663–1671.
-
9.
Tolentino K, Friedman JF, 2007. An update on anemia in less developed countries. Am J Trop Med Hyg 77: 44–51.
-
10.
Friedman JF, Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Wu H, Olveda RM, McGarvey ST, Kurtis JD, 2005. Relationship between Schistosoma japonicum and nutritional status among children and young adults in Leyte, the Philippines. Am J Trop Med Hyg 72: 527–533.
-
11.
Leenstra T, Acosta LP, Langdon GC, Manalo DL, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines. Am J Clin Nutr 83: 371–379.
-
12.
Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2005. Schistosoma japonicum and occult blood loss in endemic villages in Leyte, the Philippines. Am J Trop Med Hyg 72: 115–118.
-
13.
Weiss G, Goodnough LT, 2005. Anemia of chronic disease. N Engl J Med 352: 1011–1023.
-
14.
Malope BI, MacPhail AP, Alberts M, Hiss DC, 2001. The ratio of serum transferrin receptor and serum ferritin in the diagnosis of iron status. Br J Haematol 115: 84–89.
-
15.
Punnonen K, Irjala K, Rajamaki A, 1997. Serum transferrin receptor and its ratio to serum ferritin in the diagnosis of iron deficiency. Blood 89: 1052–1057.
-
16.
Lee EJ, Oh E, Park Y, Lee HK, Kim BK, 2002. Soluble transferrin receptor (sTfR), ferritin, and sTfR/log ferritin index in anemic patients with nonhematologic malignancy and chronic inflammation. Clin Chem 48: 1118–1121.
-
17.
Suominen P, Punnonen K, Rajamaki A, Irjala K, 1998. Serum transferrin receptor and transferrin receptor-ferritin index identify healthy subjects with subclinical iron deficits. Blood 92: 2934–2939.
-
18.
Mast AE, Blinder MA, Gronowski AM, Chumley C, Scott MG, 1998. Clinical utility of soluble transferrin receptor and comparison with serum ferritin in several populations. Clin Chem 44: 45–51.
-
19.
Wish JB, 2006. Assessing iron status: beyond serum ferritin and transferrin saturation. Clin J Am Soc Nephrol 1 (Suppl 1): S4–S8.
-
20.
Ferguson BJ, Skikne BS, Simpson KM, Baynes RD, Cook JD, 1992. Serum transferrin receptor distinguishes the anemia of chronic disease from iron deficiency anemia. J Lab Clin Med 119: 385–390.
-
21.
Ioannou G, Spector J, Scott K, Rockey DC, 2002. Prospective evaluation of a clinical guideline for the diagnosis and management of iron deficiency anemia. Am J Med 113: 281–287.
-
22.
National Kidney Foundation, 2006. Kidney Dialysis Outcome Quality Initiative (KDOQI) Clinical practice guidelines and clinical practice recommendations for anemia in chronic kidney disease. Am J Kidney Dis 47 (Suppl 3): S11–S145.
-
23.
Brugnara C, 2003. Iron deficiency and erythropoiesis: new diagnostic approaches. Clin Chem 49: 1573–1578.
-
24.
Tsang VC, Tsang KR, Hancock K, Kelly MA, Wilson BC, Maddison SE, 1983. Schistosoma mansoni adult microsomal antigens, a serologic reagent. I. Systematic fractionation, quantitation, and characterization of antigenic components. J Immunol 130: 1359–1365.
-
25.
Tsang VC, Hancock K, Maddison SE, Beatty AL, Moss DM, 1984. Demonstration of species-specific and cross-reactive components of the adult microsomal antigens from Schistosoma mansoni and S. japonicum (MAMA and JAMA). J Immunol 132: 2607–2613.
-
26.
Gwatkin DR, Rustein S, Johnson K, Pande R, Wagstaff A, 2000. Socio-Economic Differences in Health, Nutrition and Population in Kenya. Washington, DC: HNP/Poverty Thematic Group, The World Bank.
-
27.
Government of Kenya Ministry of Health, 2002. Nutritional and haematologic conditions. Kimathi NA, Micheni JN, Muriithi A, eds. Clinical Guidelines for Diagnosis and Treatment of Common Conditions in Kenya. Nairobi, Kenya: The Regal Press Kenya Ltd., 190–202.
-
28.
Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T, 2003. Hepcidin, a putative mediator of anemia of inflammation, is a type II acute phase protein. Blood 101: 2461–2463.
-
29.
Ganz T, Olbina G, Girelli D, Nemeth E, Westerman M, 2008. Immunoassay for human serum hepcidin. Blood 112: 4292–4297.
-
30.
Weiss G, 2002. Pathogenesis and treatment of anaemia of chronic disease. Blood Rev 16: 87–96.
-
31.
Weiss G, 2002. Iron and immunity: a double-edged sword. Eur J Clin Invest 32 (Suppl 1): 70–78.
-
32.
Means RT Jr, 2003. Recent developments in the anemia of chronic disease. Curr Hematol Rep 2: 116–121.
-
33.
Cartwright GE, 1966. The anemia of chronic disorders. Semin Hematol 3: 351–375.
-
34.
Matzner Y, Levy S, Grossowicz N, Izak G, Hershko C, 1979. Prevalence and causes of anemia in elderly hospitalized patients. Gerontology 25: 113–119.
-
35.
Oppenheimer SJ, Gibson FD, MacFarlane SB, Moody JB, Harrison C, Spencer A, Bunari O, 1986. Iron supplementation increases prevalence and effects of malaria: report on clinical studies in Papua New Guinea. Trans R Soc Trop Med Hyg 80: 603–612.
-
36.
Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra U, Kabole I, Deb S, Othman MK, Kabole FM, 2006. Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet 367: 133–143.
-
37.
Leenstra T, Coutinho HM, Acosta LP, Langdon GC, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Schistosoma japonicum reinfection after praziquantel treatment causes anemia associated with inflammation. Infect Immun 74: 6398–6407.
-
38.
Olson CL, Acosta LP, Hochberg NS, Olveda RM, Jiz M, McGarvey ST, Kurtis JD, Bellinger DC, Friedman JF, 2009. Anemia of inflammation is related to cognitive impairment among children in Leyte, the Philippines. PLoS Negl Trop Dis 10: e533.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1323 | 1186 | 224 |
| Full Text Views | 442 | 6 | 1 |
| PDF Downloads | 155 | 5 | 1 |