ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2014. WHO | World Malaria Report 2014. Geneva, Switzerland: WHO. Available at: http://www.who.int/malaria/publications/world_malaria_report_2014/en/. Accessed February 27, 2015.
-
2.
Bryce J, Boschi-Pinto C, Shibuya K, Black RE, 2005. WHO estimates of the causes of death in children. Lancet 365: 1147–1152.
-
3.
World Health Organization, 2008. WHO | Worldwide Prevalence of Anaemia 1993–2005. Geneva, Switzerland, WHO. Available at: http://www.who.int/nutrition/publications/micronutrients/anaemia_iron_deficiency/9789241596657/en/. Accessed May 12, 2015.
-
4.
Kassebaum NJ et al. 2014. A systematic analysis of global anemia burden from 1990 to 2010. Blood 123: 615–624.
-
5.
Worwood M, 1997. The laboratory assessment of iron status—an update. Clin Chim Acta 259: 3–23.
-
6.
Stoltzfus RJ, Chwaya HM, Albonico M, Schulze KJ, Savioli L, Tielsch JM, 1997. Serum ferritin, erythrocyte protoporphyrin and hemoglobin are valid indicators of iron status of school children in a malaria-holoendemic population. J Nutr 127: 293–298. Available at: http://jn.nutrition.org/content/127/2/293.short. Accessed November 19, 2015.
-
7.
Sazawal S et al. 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 (London, England) 367: 133–143.
-
8.
Ojukwu JU, Okebe JU, Yahav D, Paul M, 2009. Oral iron supplementation for preventing or treating anaemia among children in malaria-endemic areas. Evid Based Child Health 5: 967–1183 [Review].
-
9.
Okebe JU, Yahav D, Shbita R, Paul M, 2016. Oral iron supplements for children in malaria-endemic areas. Cochrane Database Syst Rev 10: CD006589.
-
10.
World Health Organization, 2011. WHO | Intermittent Iron Supplementation in Preschool and School-Age Children. Geneva, Switzerland: WHO. Available at: http://www.who.int/nutrition/publications/micronutrients/guidelines/guideline_iron_supplementation_children/en/. Accessed November 5, 2015.
-
11.
Roth DE, Black RE, Ojukwu JU, Okebe JU, Yahav D, Paul M, 2010. Commentary on “Oral iron supplementation for preventing or treating anaemia among children in malaria-endemic areas” with a response from the review authors. Evid Based Child Health 5: 1186–1188.
-
12.
Spottiswoode N, Fried M, Drakesmith H, Duffy PE, 2012. Implications of malaria on iron deficiency control strategies. Adv Nutr 3: 570–578.
-
13.
Nyakeriga AM, Troye-Blomberg M, Dorfman JR, Alexander ND, Bäck R, Kortok M, Chemtai AK, Marsh K, Williams TN, 2004. Iron deficiency and malaria among children living on the coast of Kenya. J Infect Dis 190: 439–447.
-
14.
Gwamaka M, Kurtis JD, Sorensen BE, Holte S, Morrison R, Mutabingwa TK, Fried M, Duffy PE, 2012. Iron deficiency protects against severe Plasmodium falciparum malaria and death in young children. Clin Infect Dis 54: 1137–1144.
-
15.
Jonker FAM, Calis JCJ, van Hensbroek MB, Phiri K, Geskus RB, Brabin BJ, Leenstra T, 2012. Iron status predicts malaria risk in Malawian preschool children. PLoS One 7: e42670.
-
16.
Snow RW, Byass P, Shenton FC, Greenwood BM, 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.
-
17.
Gabay C, Kushner I, 1999. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340: 448–454.
-
18.
Tran TN, Eubanks SK, Schaffer KJ, Zhou CY, Linder MC, 1997. Secretion of ferritin by rat hepatoma cells and its regulation by inflammatory cytokines and iron. Blood 90: 4979–4986. Available at: http://www.bloodjournal.org/content/90/12/4979.abstract. Accessed November 19, 2015.
-
19.
Wessells KR, Hess SY, Ouédraogo ZP, Rouamba N, Ouédraogo J-B, Brown KH, 2014. Asymptomatic malaria infection affects the interpretation of biomarkers of iron and vitamin A status, even after adjusting for systemic inflammation, but does not affect plasma zinc concentrations among young children in Burkina Faso. J Nutr 144: 2050–2058.
-
20.
Shipton D, 2004. Association between haemoglobin level and susceptibility to malaria: a study of Gambian children. MSc diss., London School of Hygiene and Tropical Medicine.
-
21.
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.
-
22.
Senn N et al. 2012. Intermittent preventive treatment for malaria in Papua New Guinean infants exposed to Plasmodium falciparum and P. vivax: a randomized controlled trial. PLoS Med 9: e1001195.
-
23.
Müller I, Bockarie M, Alpers M, Smith T, 2003. The epidemiology of malaria in Papua New Guinea. Trends Parasitol 19: 253–259.
-
24.
Schultz L et al. 2010. Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J 9: 336.
-
25.
Rosenberg R, 2007. Plasmodium vivax in Africa: hidden in plain sight? Trends Parasitol 23: 193–196.
-
26.
Genton B, D’Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Müller I, 2008. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: e127.
-
27.
Lin E et al. 2010. Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PLoS One 5: e9047.
-
28.
Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, Lampah DA, Price RN, 2008. Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5: e128.
-
29.
Alexandre MA, Ferreira CO, Siqueira AM, Magalhães BL, Mourão MPG, Lacerda MV, Alecrim MGC, 2010. Severe Plasmodium vivax malaria, Brazilian Amazon. Emerg Infect Dis 16: 1611–1614.
-
30.
Schellenberg D, Cisse B, Menendez C, 2006. The IPTi Consortium: research for policy and action. Trends Parasitol 22: 296–300.
-
31.
Reed RB, Stuart HC, 1959. Patterns of growth in height and weight from birth to eighteen years of age. Pediatrics 24: 904–921.
-
32.
World Health Organization, 2011. WHO | Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Geneva, Switzerland: WHO. Available at: http://www.who.int/vmnis/indicators/haemoglobin/en/. Accessed March 14, 2015.
-
33.
Orkin SH, Nathan DG, 2009. Nathan and Oski’s Hematology of Infancy and Childhood, Vol. 1. Philadelphia, PA: Elsevier Health Sciences.
-
34.
Müller I, Genton B, Rare L, Kiniboro B, Kastens W, Zimmerman P, Kazura J, Alpers M, Smith TA, 2009. Three different Plasmodium species show similar patterns of clinical tolerance of malaria infection. Malar J 8: 158.
-
35.
StataCorp, 2013. Stata Statistical Software: Release 13. College Station, TX: StataCorp LP.
-
36.
Rasmussen K, 2001. Is there a causal relationship between iron deficiency or iron-deficiency anemia and weight at birth, length of gestation and perinatal mortality? J Nutr 131:590S–601S; discussion 601S–603S.
-
37.
Jopling J, Henry E, Wiedmeier SE, Christensen RD, 2009. Reference ranges for hematocrit and blood hemoglobin concentration during the neonatal period: data from a multihospital health care system. Pediatrics 123: e333–e337.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 345 | 240 | 48 |
| Full Text Views | 361 | 11 | 1 |
| PDF Downloads | 104 | 7 | 1 |
Hemoglobin Levels and the Risk of Malaria in Papua New Guinean Infants: A Nested Cohort Study
Patrick Lombardo
Patrick Lombardo
Institute of Family Medicine, University of Lausanne, Lausanne, Switzerland;
Search for other papers by Patrick Lombardo in
Current site
Google Scholar
PubMed
Search for other papers by Patrick Lombardo in
Current site
Google Scholar
PubMed
Paul Vaucher
Paul Vaucher
School of Health Sciences Fribourg, University of Applied Sciences Western Switzerland (HES-SO), Fribourg, Switzerland;
University Center of Legal Medicine, University Hospital Lausanne (CHUV), Lausanne, Switzerland;
Search for other papers by Paul Vaucher in
Current site
Google Scholar
PubMed
University Center of Legal Medicine, University Hospital Lausanne (CHUV), Lausanne, Switzerland;
Search for other papers by Paul Vaucher in
Current site
Google Scholar
PubMed
Patricia Rarau
Patricia Rarau
Papua New Guinea Institute of Medical Research, Vector Borne Diseases Unit, Madang, Papua New Guinea;
Search for other papers by Patricia Rarau in
Current site
Google Scholar
PubMed
Search for other papers by Patricia Rarau in
Current site
Google Scholar
PubMed
Ivo Mueller
Ivo Mueller
Division of Population Health and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia;
Search for other papers by Ivo Mueller in
Current site
Google Scholar
PubMed
Search for other papers by Ivo Mueller in
Current site
Google Scholar
PubMed
Bernard Favrat
Bernard Favrat
Department of Ambulatory Care and Community Medicine, University of Lausanne, Lausanne, Switzerland
Search for other papers by Bernard Favrat in
Current site
Google Scholar
PubMed
Search for other papers by Bernard Favrat in
Current site
Google Scholar
PubMed
Nicolas Senn
Nicolas Senn
Institute of Family Medicine, University of Lausanne, Lausanne, Switzerland;
Department of Ambulatory Care and Community Medicine, University of Lausanne, Lausanne, Switzerland
Search for other papers by Nicolas Senn in
Current site
Google Scholar
PubMed
Department of Ambulatory Care and Community Medicine, University of Lausanne, Lausanne, Switzerland
Search for other papers by Nicolas Senn in
Current site
Google Scholar
PubMed
Studies are available that assess the risk of malaria in accordance to the body’s iron store and the systematic iron supplementation of preschool children. However, only a few studies evaluated the temporal association between hemoglobin and malaria and their results are opposing. A total of 1,650 3-month-old Papua New Guinean infants were enrolled in this study and followed-up for 12 months. The risk of malaria was assessed in all children every 3 months and with each episode of fever. The incidence of clinical malaria between 3 and 15 months of age was 249 cases per 1,000 infants per year. After adjustment for potential confounding factors, a decrease of 1 g/dL of hemoglobin was associated with a nonsignificant increase of 11% for risk of malaria infection (hazard ratio, 1.11, 95% confidence interval; CI, 0.99–1.25, P = 0.076). Only children with severe anemia (hemoglobin < 8.0 g/dL) at baseline were at higher risk of malaria infection (hazard ratio, 1.72, 95% CI, 1.08–2.76, P = 0.023) during the follow-up year compared with the control group (Hemoglobin > 10.0 g/dL). This association was not statistically significant if only clinical malaria episodes were taken into account (hazard ratio, 1.42, 95% CI, 0.77–2.61, P = 0.26). Our study suggests that infants with lower hemoglobin levels are not protected against malaria infection. Further research that examines the risk of malaria in relation to both hemoglobin and iron store levels would be important to better understand this complex interaction.
- Supplemental Materials (PDF 109 KB)
Author Notes
Authors’ addresses: Patrick Lombardo and Nicolas Senn, Institute of Family Medicine, University of Lausanne, Lausanne, Switzerland, E-mails: patrick@lombardo.com and nicolas.senn@hospvd.ch. Paul Vaucher, School of Health Sciences Fribourg, University of Applied Sciences Western Switzerland, Fribourg, Switzerland. E-mail: paul.vaucher@hefr.ch. Patricia Rarau, Papua New Guinea Institute of Medical Research, Vector Borne Diseases Unit, Madang, Papua New Guinea, E-mail: patricia.rarau@gmail.com. Ivo Mueller, Division of Population Health and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia, E-mail: ivomueller@fastmail.fm. Bernard Favrat, Department of Ambulatory Care and Community Medicine, University of Lausanne, Lausanne, Switzerland, E-mail: bernard.favrat@chuv.ch.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2014. WHO | World Malaria Report 2014. Geneva, Switzerland: WHO. Available at: http://www.who.int/malaria/publications/world_malaria_report_2014/en/. Accessed February 27, 2015.
-
2.
Bryce J, Boschi-Pinto C, Shibuya K, Black RE, 2005. WHO estimates of the causes of death in children. Lancet 365: 1147–1152.
-
3.
World Health Organization, 2008. WHO | Worldwide Prevalence of Anaemia 1993–2005. Geneva, Switzerland, WHO. Available at: http://www.who.int/nutrition/publications/micronutrients/anaemia_iron_deficiency/9789241596657/en/. Accessed May 12, 2015.
-
4.
Kassebaum NJ et al. 2014. A systematic analysis of global anemia burden from 1990 to 2010. Blood 123: 615–624.
-
5.
Worwood M, 1997. The laboratory assessment of iron status—an update. Clin Chim Acta 259: 3–23.
-
6.
Stoltzfus RJ, Chwaya HM, Albonico M, Schulze KJ, Savioli L, Tielsch JM, 1997. Serum ferritin, erythrocyte protoporphyrin and hemoglobin are valid indicators of iron status of school children in a malaria-holoendemic population. J Nutr 127: 293–298. Available at: http://jn.nutrition.org/content/127/2/293.short. Accessed November 19, 2015.
-
7.
Sazawal S et al. 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 (London, England) 367: 133–143.
-
8.
Ojukwu JU, Okebe JU, Yahav D, Paul M, 2009. Oral iron supplementation for preventing or treating anaemia among children in malaria-endemic areas. Evid Based Child Health 5: 967–1183 [Review].
-
9.
Okebe JU, Yahav D, Shbita R, Paul M, 2016. Oral iron supplements for children in malaria-endemic areas. Cochrane Database Syst Rev 10: CD006589.
-
10.
World Health Organization, 2011. WHO | Intermittent Iron Supplementation in Preschool and School-Age Children. Geneva, Switzerland: WHO. Available at: http://www.who.int/nutrition/publications/micronutrients/guidelines/guideline_iron_supplementation_children/en/. Accessed November 5, 2015.
-
11.
Roth DE, Black RE, Ojukwu JU, Okebe JU, Yahav D, Paul M, 2010. Commentary on “Oral iron supplementation for preventing or treating anaemia among children in malaria-endemic areas” with a response from the review authors. Evid Based Child Health 5: 1186–1188.
-
12.
Spottiswoode N, Fried M, Drakesmith H, Duffy PE, 2012. Implications of malaria on iron deficiency control strategies. Adv Nutr 3: 570–578.
-
13.
Nyakeriga AM, Troye-Blomberg M, Dorfman JR, Alexander ND, Bäck R, Kortok M, Chemtai AK, Marsh K, Williams TN, 2004. Iron deficiency and malaria among children living on the coast of Kenya. J Infect Dis 190: 439–447.
-
14.
Gwamaka M, Kurtis JD, Sorensen BE, Holte S, Morrison R, Mutabingwa TK, Fried M, Duffy PE, 2012. Iron deficiency protects against severe Plasmodium falciparum malaria and death in young children. Clin Infect Dis 54: 1137–1144.
-
15.
Jonker FAM, Calis JCJ, van Hensbroek MB, Phiri K, Geskus RB, Brabin BJ, Leenstra T, 2012. Iron status predicts malaria risk in Malawian preschool children. PLoS One 7: e42670.
-
16.
Snow RW, Byass P, Shenton FC, Greenwood BM, 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.
-
17.
Gabay C, Kushner I, 1999. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340: 448–454.
-
18.
Tran TN, Eubanks SK, Schaffer KJ, Zhou CY, Linder MC, 1997. Secretion of ferritin by rat hepatoma cells and its regulation by inflammatory cytokines and iron. Blood 90: 4979–4986. Available at: http://www.bloodjournal.org/content/90/12/4979.abstract. Accessed November 19, 2015.
-
19.
Wessells KR, Hess SY, Ouédraogo ZP, Rouamba N, Ouédraogo J-B, Brown KH, 2014. Asymptomatic malaria infection affects the interpretation of biomarkers of iron and vitamin A status, even after adjusting for systemic inflammation, but does not affect plasma zinc concentrations among young children in Burkina Faso. J Nutr 144: 2050–2058.
-
20.
Shipton D, 2004. Association between haemoglobin level and susceptibility to malaria: a study of Gambian children. MSc diss., London School of Hygiene and Tropical Medicine.
-
21.
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.
-
22.
Senn N et al. 2012. Intermittent preventive treatment for malaria in Papua New Guinean infants exposed to Plasmodium falciparum and P. vivax: a randomized controlled trial. PLoS Med 9: e1001195.
-
23.
Müller I, Bockarie M, Alpers M, Smith T, 2003. The epidemiology of malaria in Papua New Guinea. Trends Parasitol 19: 253–259.
-
24.
Schultz L et al. 2010. Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J 9: 336.
-
25.
Rosenberg R, 2007. Plasmodium vivax in Africa: hidden in plain sight? Trends Parasitol 23: 193–196.
-
26.
Genton B, D’Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Müller I, 2008. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: e127.
-
27.
Lin E et al. 2010. Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PLoS One 5: e9047.
-
28.
Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, Lampah DA, Price RN, 2008. Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5: e128.
-
29.
Alexandre MA, Ferreira CO, Siqueira AM, Magalhães BL, Mourão MPG, Lacerda MV, Alecrim MGC, 2010. Severe Plasmodium vivax malaria, Brazilian Amazon. Emerg Infect Dis 16: 1611–1614.
-
30.
Schellenberg D, Cisse B, Menendez C, 2006. The IPTi Consortium: research for policy and action. Trends Parasitol 22: 296–300.
-
31.
Reed RB, Stuart HC, 1959. Patterns of growth in height and weight from birth to eighteen years of age. Pediatrics 24: 904–921.
-
32.
World Health Organization, 2011. WHO | Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Geneva, Switzerland: WHO. Available at: http://www.who.int/vmnis/indicators/haemoglobin/en/. Accessed March 14, 2015.
-
33.
Orkin SH, Nathan DG, 2009. Nathan and Oski’s Hematology of Infancy and Childhood, Vol. 1. Philadelphia, PA: Elsevier Health Sciences.
-
34.
Müller I, Genton B, Rare L, Kiniboro B, Kastens W, Zimmerman P, Kazura J, Alpers M, Smith TA, 2009. Three different Plasmodium species show similar patterns of clinical tolerance of malaria infection. Malar J 8: 158.
-
35.
StataCorp, 2013. Stata Statistical Software: Release 13. College Station, TX: StataCorp LP.
-
36.
Rasmussen K, 2001. Is there a causal relationship between iron deficiency or iron-deficiency anemia and weight at birth, length of gestation and perinatal mortality? J Nutr 131:590S–601S; discussion 601S–603S.
-
37.
Jopling J, Henry E, Wiedmeier SE, Christensen RD, 2009. Reference ranges for hematocrit and blood hemoglobin concentration during the neonatal period: data from a multihospital health care system. Pediatrics 123: e333–e337.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 345 | 240 | 48 |
| Full Text Views | 361 | 11 | 1 |
| PDF Downloads | 104 | 7 | 1 |