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Zotero
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Friedman JF, Kwena AM, Mirel LB, Kariuki SK, Terlouw DJ, Phillips-Howard PA, Hawley WA, Nahlen BL, Shi YP, ter Kuile FO, 2005. Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. Am J Trop Med Hyg 73: 698–704.
-
16.
Mfonkeu JB, Gouado I, Kuate HF, Zambou O, Combes V, Grau GE, Zollo PH, 2010. Biochemical markers of nutritional status and childhood malaria severity in Cameroon. Br J Nutr 104: 886–892.
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-
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Omodeo-Sale F, Motti A, Basilico N, Parapini S, Olliaro P, Taramelli D, 2003. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood 102: 705–711.
-
20.
Brattig NW, Kowalsky K, Liu X, Burchard GD, Kamena F, Seeberger PH, 2008. Plasmodium falciparum glycosylphosphatidylinositol toxin interacts with the membrane of non-parasitized red blood cells: a putative mechanism contributing to malaria anemia. Microbes Infect 10: 885–891.
-
21.
Awah NW, Troye-Blomberg M, Berzins K, Gysin J, 2009. Mechanisms of malarial anaemia: potential involvement of the Plasmodium falciparum low molecular weight rhoptry-associated proteins. Acta Trop 112: 295–302.
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Stoute JA, 2011. Complement receptor 1 and malaria. Cell Microbiol 13: 1441–1450.
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Howes RE, Battle KE, Satyagraha AW, Baird JK, Hay SI, 2013. G6PD deficiency: global distribution, genetic variants and primaquine therapy. Adv Parasitol 81: 133–201.
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Abanyie FA, McCracken C, Kirwan P, Molloy SF, Asaolu SO, Holland CV, Gutman J, Lamb TJ, 2013. Ascaris co-infection does not alter malaria-induced anaemia in a cohort of Nigerian preschool children. Malar J 12: 1.
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Melo GC, Reyes-Lecca RC, Vitor-Silva S, Monteiro WM, Martins M, Benzecry SG, Alecrim M, Lacerda MV, 2010. Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS ONE 5: e11206.
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Bouyou-Akotet MK, Mawili Mboumba DP, Kendjo E, Mbadinga F, Obiang-Bekale N, Mouidi P, Kombila M, 2013. Anaemia and severe malarial anaemia burden in febrile Gabonese children: a nine-year health facility based survey. J Infect Dev Ctries 7: 983–989.
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Quintero JP, Siqueira AM, Tobon A, Blair S, Moreno A, Arevalo-Herrera M, Lacerda MV, Valencia SH, 2011. Malaria-related anaemia: a Latin American perspective. Mem Inst Oswaldo Cruz 106 (Suppl 1): 91–104.
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Malaria-Related Anemia in Patients from Unstable Transmission Areas in Colombia
Mary Lopez-Perez
Mary Lopez-Perez
Caucaseco Scientific Research Center, Cali, Colombia; Institute of Bioinformatics, University of Georgia, Athens, Georgia; Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia; Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, Georgia; Faculty of Health, Universidad del Valle, Cali, Colombia
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Álvaro Álvarez
Álvaro Álvarez
Caucaseco Scientific Research Center, Cali, Colombia; Institute of Bioinformatics, University of Georgia, Athens, Georgia; Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia; Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, Georgia; Faculty of Health, Universidad del Valle, Cali, Colombia
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Juan B. Gutierrez
Juan B. Gutierrez
Caucaseco Scientific Research Center, Cali, Colombia; Institute of Bioinformatics, University of Georgia, Athens, Georgia; Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia; Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, Georgia; Faculty of Health, Universidad del Valle, Cali, Colombia
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Alberto Moreno
Alberto Moreno
Caucaseco Scientific Research Center, Cali, Colombia; Institute of Bioinformatics, University of Georgia, Athens, Georgia; Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia; Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, Georgia; Faculty of Health, Universidad del Valle, Cali, Colombia
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Sócrates Herrera
Sócrates Herrera
Caucaseco Scientific Research Center, Cali, Colombia; Institute of Bioinformatics, University of Georgia, Athens, Georgia; Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia; Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, Georgia; Faculty of Health, Universidad del Valle, Cali, Colombia
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Myriam Arévalo-Herrera
Myriam Arévalo-Herrera
Caucaseco Scientific Research Center, Cali, Colombia; Institute of Bioinformatics, University of Georgia, Athens, Georgia; Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia; Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, Georgia; Faculty of Health, Universidad del Valle, Cali, Colombia
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Information about the prevalence of malarial anemia in areas of low-malaria transmission intensity, like Latin America, is scarce. To characterize the malaria-related anemia, we evaluated 929 malaria patients from three sites in Colombia during 2011–2013. Plasmodium vivax was found to be the most prevalent species in Tierralta (92%), whereas P. falciparum was predominant in Tumaco (84%) and Quibdó (70%). Although severe anemia (hemoglobin < 7 g/dL) was almost absent (0.3%), variable degrees of non-severe anemia were observed in 36.9% of patients. In Tierralta, hemoglobin levels were negatively associated with days of illness. Moreover, in Tierralta and Quibdó, the number of previous malaria episodes and hemoglobin levels were positively associated. Both Plasmodium species seem to have similar potential to induce malarial anemia with distinct cofactors at each endemic setting. The target age in these low-transmission settings seems shifting toward adolescents and young adults. In addition, previous malaria experience seems to induce protection against anemia development. Altogether, these data suggest that early diagnosis and prompt treatment are likely preventing more frequent and serious malaria-related anemia in Colombia.
Author Notes
Financial support: This work was sponsored and conducted in sites affiliated with the Centro Latino Americano de Investigación en Malaria sponsored by The National Institute of Allergy and Infectious Diseases/International Centers of Excellence for Malaria Research (NIAID/ICEMR) Grant 1U19AI089702, Colciencias Grants 360-2011, 458-2012, and 719-2013, and Colombian Presidential Agency of International Cooperation Grant 045-2013. A.M. was supported by NIAID Grants R21AI094402-01 and R21AI095718-01.
Authors' addresses: Mary Lopez-Perez, Álvaro Álvarez, Sócrates Herrera, and Myriam Arévalo-Herrera, Caucaseco Scientific Research Center, Cali, Colombia, E-mails: marlopez@inmuno.org, aalvarez@inmuno.org, sherrera@inmuno.org, and marevalo@inmuno.org. Juan B. Gutierrez, Institute of Bioinformatics, University of Georgia, Athens, GA, E-mail: jgutierr@uga.edu. Alberto Moreno, Emory Vaccine Center, Yerkes National Primate Research Center and Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, GA, E-mail: camoren@emory.edu.
Reprint requests: Myriam Arévalo-Herrera, Caucaseco Scientific Research Center, Carrera 37-2Bis No. 5E-08, Cali, Colombia, E-mail: marevalo@inmuno.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
WHO, 2013. World Malaria Report 2013. Geneva, Switzerland: WHO, 284.
-
2.
Perkins DJ, Were T, Davenport GC, Kempaiah P, Hittner JB, Ong'echa JM, 2011. Severe malarial anemia: innate immunity and pathogenesis. Int J Biol Sci 7: 1427–1442.
-
3.
Milner DA Jr, Montgomery J, Seydel KB, Rogerson SJ, 2008. Severe malaria in children and pregnancy: an update and perspective. Trends Parasitol 24: 590–595.
-
4.
Blair S, Alvarez G, Campuzano G, 1997. Relación entre anemia y malaria en una población rural de Colombia. Bol Dir Malariol Saneam Amb 37: 7–13.
-
5.
Caicedo O, Ramirez O, Mourao MP, Ziade J, Perez P, Santos JB, Quinones F, Alecrim MG, Arevalo-Herrera M, Lacerda MV, Herrera S, 2009. Comparative hematologic analysis of uncomplicated malaria in uniquely different regions of unstable transmission in Brazil and Colombia. Am J Trop Med Hyg 80: 146–151.
-
6.
Echeverri M, Tobon A, Alvarez G, Carmona J, Blair S, 2003. Clinical and laboratory findings of Plasmodium vivax malaria in Colombia, 2001. Rev Inst Med Trop Sao Paulo 45: 29–34.
-
7.
Zamora F, Ramirez O, Vergara J, Arevalo-Herrera M, Herrera S, 2005. Hemoglobin levels related to days of illness, race, and Plasmodium species in Colombian patients with uncomplicated malaria. Am J Trop Med Hyg 73: 50–54.
-
8.
Arevalo-Herrera M, Quinones ML, Guerra C, Cespedes N, Giron S, Ahumada M, Pineros JG, Padilla N, Terrientes Z, Rosas A, Padilla JC, Escalante AA, Beier JC, Herrera S, 2012. Malaria in selected non-Amazonian countries of Latin America. Acta Trop 121: 303–314.
-
9.
Chaparro P, Padilla J, Vallejo AF, Herrera S, 2013. Characterization of a malaria outbreak in Colombia in 2010. Malar J 12: 330.
-
10.
Guerra CA, Gikandi PW, Tatem AJ, Noor AM, Smith DL, Hay SI, Snow RW, 2008. The limits and intensity of Plasmodium falciparum transmission: implications for malaria control and elimination worldwide. PLoS Med 5: e38.
-
11.
Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, Temperley WH, Kabaria CW, Tatem AJ, Manh BH, Elyazar IR, Baird JK, Snow RW, Hay SI, 2010. The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis 4: e774.
-
12.
Rodriguez JC, Uribe GA, Araujo RM, Narvaez PC, Valencia SH, 2011. Epidemiology and control of malaria in Colombia. Mem Inst Oswaldo Cruz 106 (Suppl 1): 114–122.
-
13.
Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti, Elyazar I, Bangs MJ, Maguire JD, Baird JK, 2007. Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in northeastern Indonesian Papua. Am J Trop Med Hyg 77: 984–991.
-
14.
Idro R, Aloyo J, Mayende L, Bitarakwate E, John CC, Kivumbi GW, 2006. Severe malaria in children in areas with low, moderate and high transmission intensity in Uganda. Trop Med Int Health 11: 115–124.
-
15.
Friedman JF, Kwena AM, Mirel LB, Kariuki SK, Terlouw DJ, Phillips-Howard PA, Hawley WA, Nahlen BL, Shi YP, ter Kuile FO, 2005. Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. Am J Trop Med Hyg 73: 698–704.
-
16.
Mfonkeu JB, Gouado I, Kuate HF, Zambou O, Combes V, Grau GE, Zollo PH, 2010. Biochemical markers of nutritional status and childhood malaria severity in Cameroon. Br J Nutr 104: 886–892.
-
17.
Langhorne J, Ndungu FM, Sponaas AM, Marsh K, 2008. Immunity to malaria: more questions than answers. Nat Immunol 9: 725–732.
-
18.
Totino PR, Magalhaes AD, Silva LA, Banic DM, Daniel-Ribeiro CT, Ferreira-da-Cruz M de F, 2010. Apoptosis of non-parasitized red blood cells in malaria: a putative mechanism involved in the pathogenesis of anaemia. Malar J 9: 350.
-
19.
Omodeo-Sale F, Motti A, Basilico N, Parapini S, Olliaro P, Taramelli D, 2003. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood 102: 705–711.
-
20.
Brattig NW, Kowalsky K, Liu X, Burchard GD, Kamena F, Seeberger PH, 2008. Plasmodium falciparum glycosylphosphatidylinositol toxin interacts with the membrane of non-parasitized red blood cells: a putative mechanism contributing to malaria anemia. Microbes Infect 10: 885–891.
-
21.
Awah NW, Troye-Blomberg M, Berzins K, Gysin J, 2009. Mechanisms of malarial anaemia: potential involvement of the Plasmodium falciparum low molecular weight rhoptry-associated proteins. Acta Trop 112: 295–302.
-
22.
Stoute JA, 2011. Complement receptor 1 and malaria. Cell Microbiol 13: 1441–1450.
-
23.
Howes RE, Battle KE, Satyagraha AW, Baird JK, Hay SI, 2013. G6PD deficiency: global distribution, genetic variants and primaquine therapy. Adv Parasitol 81: 133–201.
-
24.
Carmona-Fonseca J, Uscategui R, Correa A, 2009. Intestinal parasitoses in children living in malarious zones of Colombia. Iatreia 22: 27–46.
-
25.
Abanyie FA, McCracken C, Kirwan P, Molloy SF, Asaolu SO, Holland CV, Gutman J, Lamb TJ, 2013. Ascaris co-infection does not alter malaria-induced anaemia in a cohort of Nigerian preschool children. Malar J 12: 1.
-
26.
Melo GC, Reyes-Lecca RC, Vitor-Silva S, Monteiro WM, Martins M, Benzecry SG, Alecrim M, Lacerda MV, 2010. Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS ONE 5: e11206.
-
27.
Crawley J, 2004. Reducing the burden of anemia in infants and young children in malaria-endemic countries of Africa: from evidence to action. Am J Trop Med Hyg 71: 25–34.
-
28.
Ehrhardt S, Burchard GD, Mantel C, Cramer JP, Kaiser S, Kubo M, Otchwemah RN, Bienzle U, Mockenhaupt FP, 2006. Malaria, anemia, and malnutrition in african children–defining intervention priorities. J Infect Dis 194: 108–114.
-
29.
Bouyou-Akotet MK, Mawili Mboumba DP, Kendjo E, Mbadinga F, Obiang-Bekale N, Mouidi P, Kombila M, 2013. Anaemia and severe malarial anaemia burden in febrile Gabonese children: a nine-year health facility based survey. J Infect Dev Ctries 7: 983–989.
-
30.
Quintero JP, Siqueira AM, Tobon A, Blair S, Moreno A, Arevalo-Herrera M, Lacerda MV, Valencia SH, 2011. Malaria-related anaemia: a Latin American perspective. Mem Inst Oswaldo Cruz 106 (Suppl 1): 91–104.
-
31.
MinSalud, 2010. Guía de Atención Clínica de Malaria. Bogotá, Colombia: Ministerio de la Protección Social, 132.
-
32.
Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K, 2004. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol 42: 5636–5643.
-
33.
WHO, 2011. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Vitamin and Mineral Nutrition Information System. Available at: http://www.who.int/vmnis/indicators/haemoglobin.pdf. Accessed May 2014.
-
34.
Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG, 2009. Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42: 377–381.
-
35.
Gonzalez LM, Vega J, Ramirez J, Bedoya G, Carmona-Fonseca J, Maestre A, 2012. Relationship between Duffy blood groups genotypes and malaria infection in different ethnic groups of Choco-Colombia. Colomb Med 43: 189–195.
-
36.
Herrera S, Gomez A, Vera O, Vergara J, Valderrama-Aguirre A, Maestre A, Mendez F, Wang R, Chitnis CE, Yazdani SS, Arevalo-Herrera M, 2005. Antibody response to Plasmodium vivax antigens in Fy-negative individuals from the Colombian Pacific coast. Am J Trop Med Hyg 73: 44–49.
-
37.
Tobon-Castano A, Giraldo-Castro C, Blair S, 2012. Prognostic value of clinical and parasitological signs for severe malaria in patients from Colombia. Biomedica 32 (Suppl 1): 79–94.
-
38.
McQueen PG, McKenzie FE, 2004. Age-structured red blood cell susceptibility and the dynamics of malaria infections. Proc Natl Acad Sci USA 101: 9161–9166.
-
39.
Cromer D, Stark J, Davenport MP, 2009. Low red cell production may protect against severe anemia during a malaria infection–insights from modeling. J Theor Biol 257: 533–542.
-
40.
McQueen PG, McKenzie FE, 2008. Host control of malaria infections: constraints on immune and erythropoeitic response kinetics. PLoS Comput Biol 4: e1000149.
-
41.
Fernandes AA, Carvalho LJ, Zanini GM, Ventura AM, Souza JM, Cotias PM, Silva-Filho IL, Daniel-Ribeiro CT, 2008. Similar cytokine responses and degrees of anemia in patients with Plasmodium falciparum and Plasmodium vivax infections in the Brazilian Amazon region. Clin Vaccine Immunol 15: 650–658.
-
42.
Caicedo O, Villamor E, Forero Y, Ziade J, Perez P, Quinones F, Arevalo-Herrera M, Herrera S, 2010. Relation between vitamin B12 and folate status, and hemoglobin concentration and parasitemia during acute malaria infections in Colombia. Acta Trop 114: 17–21.
-
43.
Uscategui RM, Correa AM, 2007. Nutritional status of children with malaria in northwest Colombia. Biomedica 27: 559–570.
-
44.
Arevalo-Herrera M, Forero-Pena DA, Rubiano K, Gomez-Hincapie J, Martinez NL, Lopez-Perez M, Castellanos A, Cespedes N, Palacios R, Onate JM, Herrera S, 2014. Plasmodium vivax sporozoite challenge in malaria-naive and semi-immune Colombian volunteers. PLoS ONE 9: e99754.
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