ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Calis JC , van Hensbroek MB , de Haan RJ , Moons P , Brabin BJ , Bates I , 2008. HIV-associated anemia in children: a systematic review from a global perspective. AIDS 22: 1099–1112.
-
2.
Aguilar R , Moraleda C , Quinto L , Renom M , Mussacate L , Macete E , Aguilar JL , Alonso PL , Menendez C , 2012. Challenges in the diagnosis of iron deficiency in children exposed to high prevalence of infections. PLoS One 7: e50584.
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3.
Mir N , Costello C , Luckit J , Lindley R , 1989. HIV-disease and bone marrow changes: a study of 60 cases. Eur J Haematol 42: 339–343.
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4.
Mueller BU , Tannenbaum S , Pizzo PA , 1996. Bone marrow aspirates and biopsies in children with human immunodeficiency virus infection. J Pediatr Hematol Oncol 18: 266–271.
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Meira DG , Lorand-Metze I , Toro AD , Silva MT , Vilela MM , 2005. Bone marrow features in children with HIV infection and peripheral blood cytopenias. J Trop Pediatr 51: 114–119.
-
6.
Esan MO , Jonker FA , Hensbroek MB , Calis JC , Phiri KS , 2012. Iron deficiency in children with HIV-associated anaemia: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg 106: 579–587.
-
7.
Gonzalez R , Ataide R , Naniche D , Menendez C , Mayor A , 2012. HIV and malaria interactions: where do we stand? Expert Rev Anti Infect Ther 10: 153–165.
-
8.
Esan MO , van Hensbroek MB , Nkhoma E , Musicha C , White SA , Ter Kuile FO , Phiri KS , 2013. Iron supplementation in HIV-infected Malawian children with anemia: a double-blind, randomized, controlled trial. Clin Infect Dis 57: 1626–1634.
-
9.
Sacoor C et al. 2013. Profile: manhica health research centre (manhica HDSS). Int J Epidemiol 42: 1309–1318.
-
10.
Gonzalez R , Munguambe K , Aponte J , Bavo C , Nhalungo D , Macete E , Alonso P , Menendez C , Naniche D , 2012. High HIV prevalence in a southern semi-rural area of Mozambique: a community-based survey. HIV Med 13: 581–588.
-
11.
Moraleda C , de Deus N , Serna-Bolea C , Renom M , Quinto L , Macete E , Menendez C , Naniche D , 2014. Impact of HIV exposure on health outcomes in HIV-negative infants born to HIV-positive mothers in sub-Saharan Africa. J Acquir Immune Defic Syndr 65: 182–189.
-
12.
Pedrini M , Moraleda C , Macete E , Gondo K , Brabin BJ , Menendez C , 2015. Clinical, nutritional and immunological characteristics of HIV-infected children in an area of high HIV prevalence. J Trop Pediatr 61: 286–294.
-
13.
WHO , 2006. WHO 2006 Guidelines on ART in Infants and Children in Resource Limited Setting: Towards Universal Access, Recommendations for a Public Health Approach. Geneva, Switzerland: World Health Organization.
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14.
Moraleda C et al. 2017. Anaemia in hospitalised preschool children from a rural area in Mozambique: a case control study in search for aetiological agents. BMC Pediatr 17: 63.
-
15.
Stoltzfus RJ , Dreyfuss ML , 1998. Guidelines for the Use of Iron Supplements to Prevent and Treat Iron Deficiency Anemia. Washington, DC: International Nutritional Anemia Consultative Group (INACG), World Health Organization (WHO), United Nations Childrens Fund (UNICEF).
-
16.
Sapero JJ , Lawless DK , 1953. The MIF stain-preservation technic for the identification of intestinal protozoa. Am J Trop Med Hyg 2: 613–619.
-
17.
Romagosa C , Menendez C , Ismail MR , Quinto L , Ferrer B , Alonso PL , Ordi J , 2004. Polarisation microscopy increases the sensitivity of hemozoin and Plasmodium detection in the histological assessment of placental malaria. Acta Trop 90: 277–284.
-
18.
Heinze G , Schemper M , 2002. A solution to the problem of separation in logistic regression. Stat Med 21: 2409–2419.
-
19.
Salome MA , Grotto HZ , 2002. Human immunodeficiency virus-related anemia of chronic disease: relationship to hematologic, immune, and iron metabolism parameters, and lack of association with serum interferon-gamma levels. AIDS Patient Care STDS 16: 361–365.
-
20.
Calis JC et al. 2010. Erythropoiesis in HIV-infected and uninfected Malawian children with severe anemia. AIDS 24: 2883–2887.
-
21.
Menendez C , Quinto LL , Kahigwa E , Alvarez L , Fernandez R , Gimenez N , Schellenberg D , Aponte JJ , Tanner M , Alonso PL , 2001. Effect of malaria on soluble transferrin receptor levels in Tanzanian infants. Am J Trop Med Hyg 65: 138–142.
-
22.
Totin D , Ndugwa C , Mmiro F , Perry RT , Jackson JB , Semba RD , 2002. Iron deficiency anemia is highly prevalent among human immunodeficiency virus-infected and uninfected infants in Uganda. J Nutr 132: 423–429.
-
23.
Miller MF , Humphrey JH , Iliff PJ , Malaba LC , Mbuya NV , Stoltzfus RJ ; ZVITAMBO Study Group , 2006. Neonatal erythropoiesis and subsequent anemia in HIV-positive and HIV-negative Zimbabwean babies during the first year of life: a longitudinal study. BMC Infect Dis 6: 1.
-
24.
Gordeuk VR , Delanghe JR , Langlois MR , Boelaert JR , 2001. Iron status and the outcome of HIV infection: an overview. J Clin Virol 20: 111–115.
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25.
WHO , 2016. Guideline: Daily Iron Supplementation in Infants and Children. Geneva, Switzerland: World Health Organization.
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26.
Bebell LM , Gasasira A , Kiggundu M , Dokomajilar C , Kamya MR , Charlebois ED , Havlir D , Rosenthal PJ , Dorsey G , 2007. HIV-1 infection in patients referred for malaria blood smears at government health clinics in Uganda. J Acquir Immune Defic Syndr 46: 624–630.
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Villamor E , Fataki MR , Mbise RL , Fawzi WW , 2003. Malaria parasitaemia in relation to HIV status and vitamin A supplementation among pre-school children. Trop Med Int Health 8: 1051–1061.
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29.
Kalyesubula I , Musoke-Mudido P , Marum L , Bagenda D , Aceng E , Ndugwa C , Olness K , 1997. Effects of malaria infection in human immunodeficiency virus type 1-infected Ugandan children. Pediatr Infect Dis J 16: 876–881.
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Pathophysiology of Anemia in HIV-Infected Children Exposed to Malaria
Cinta Moraleda
Cinta Moraleda
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Ruth Aguilar
Ruth Aguilar
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
CIBER Epidemiology and Public Health (CIBERESP), Barcelona, Spain;
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Manhiça Health Research Center (CISM), Manhiça, Mozambique;
CIBER Epidemiology and Public Health (CIBERESP), Barcelona, Spain;
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Llorenç Quintó
Llorenç Quintó
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
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Tacilta Nhampossa
Tacilta Nhampossa
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Montserrat Renom
Montserrat Renom
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Augusto Nhabomba
Augusto Nhabomba
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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María Ruperez
María Ruperez
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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John J. Aponte
John J. Aponte
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Ariel H. Achtman
Ariel H. Achtman
Walter and Eliza Hall Institute for Medical Research, Victoria, Australia;
Department of Medical Biology, The University of Melbourne, Victoria, Australia;
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Department of Medical Biology, The University of Melbourne, Victoria, Australia;
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María del Mar Mañú Pereira
María del Mar Mañú Pereira
Red Blood Cell Pathology- Centre for Rare Diseases, Vall d’Hebron Research Institute, University Hospital Vall d’Hebron, Barcelona, Spain;
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Louis Schofield
Louis Schofield
Walter and Eliza Hall Institute for Medical Research, Victoria, Australia;
Department of Medical Biology, The University of Melbourne, Victoria, Australia;
Australian Institute of Tropical Health and Medicine, James Cook University, Douglas, Australia;
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Department of Medical Biology, The University of Melbourne, Victoria, Australia;
Australian Institute of Tropical Health and Medicine, James Cook University, Douglas, Australia;
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Pedro L. Alonso
Pedro L. Alonso
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Manhiça Health Research Center (CISM), Manhiça, Mozambique;
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Eusebio Macete
Eusebio Macete
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
National Directorate of Health, Ministry of Health, Maputo, Mozambique
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National Directorate of Health, Ministry of Health, Maputo, Mozambique
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Clara Menéndez
Clara Menéndez
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain;
Manhiça Health Research Center (CISM), Manhiça, Mozambique;
CIBER Epidemiology and Public Health (CIBERESP), Barcelona, Spain;
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ABSTRACT
Anemia is a common condition in HIV-infected children; however, its pathophysiology and the contribution of frequent causes of anemia such as iron deficiency (ID) and malaria are poorly understood. We carried out an ancillary study on the effect of HIV on anemia as part of a case–control study on risk factors of anemia among Mozambican children aged 1–59 months with documented HIV status. Of them, 390 children were admitted to the hospital with anemia (hemoglobin [Hb] < 11 g/dL), whereas 272 children without anemia (Hb ≥ 11 g/dL) were recruited in the community. We assessed differences by HIV status in the presentation of anemia etiological factors and the effect of HIV infection on the association of each factor with anemia. Among the 99 HIV-infected and 563 uninfected children included, HIV-infected anemic children had an increased risk of undernutrition (P < 0.0001), Epstein–Barr virus infection (P < 0.0001), bacteremia (P = 0.0060), a decreased risk of malaria (P < 0.0001), and a similar risk of ID (P = 0.7371) compared with anemic-uninfected children. HIV-infected children were significantly less likely to have anemia associated with Plasmodium falciparum hyperparasitemia (P = 0.0444) and had a lower prevalence of parasitemia in the bone marrow (BM) (P < 0.0001) than anemic-uninfected children. Levels of BM erythropoiesis and dyserythropoiesis were comparable between groups. These findings suggest that the pathophysiology of anemia among HIV-infected malaria-exposed children is not related to HIV-specific effects. For unclear reasons, HIV-infected children had reduced risk of malaria infection, whereas ID prevalence was comparable in HIV-infected and uninfected children, suggesting that iron supplementation recommendations should not be different in HIV-infected children.
- Supplemental Materials (PDF 642.96 KB)
Author Notes
Financial support: This study was funded by the Agencia de Cooperación Internacional de Las Illes Balears, Spain, and the Fundación Ramón Areces. The Centro de Investigaçaõ em Saúde de Manhiça receives core funding from the Spanish Agency for International Cooperation and Development (AECID). The Walter and Eliza Hall Institute receives Victorian State Government Operational Infrastructure Support and Australian Government NHMRC IRIISS. L. S. received support as an International Research Scholars of the Howard Hughes Medical Institute and from NHMRC program grant #637406. AHA received support from the Victorian Community Foundation-the George Perry Fund.
Authors’ addresses: Cinta Moraleda, ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain, and Pediatric Infectious Diseases Unit, Instituto de investigación Hospital, RiTiP, Hospital Universitario, Universidad Complutense, Madrid, Spain, E-mail: cinta.moraleda@isglobal.org. Ruth Aguilar, Llorenç Quintó, Montserrat Renom, John J. Aponte, and Clara Menéndez, ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain, E-mails: ruth.aguilar@isglobal.org, llorenc.quinto@isglobal.org, montse.renom034@gmail.com, john.aponte@isglobal.org, and clara.menendez@isglobal.org. Tacilta Nhampossa, Augusto Nhabomba, and Eusebio Macete, Manhiça Health Research Center (CISM), Manhiça, Mozambique, E-mails: tacilta.nhampossa@manhica.net, augusto.nhabomba@gmail.com, and eusebio.macete@manhica.net. María Ruperez, London School of Hygiene and Tropical Medicine, London, United Kingdom, E-mail: maria.ruperez@lshtm.ac.uk. Ariel H. Achtman and Louis Schofield, Walter and Eliza Hall Institute for Medical Research, Parkville, Australia, E-mails: arielachtman@hotmail.com and louis.schofield@jcu.edu.au. María del Mar Mañú Pereira, Red Blood Cell Pathology- Centre for Rare Diseases, Vall d’Hebron Research Institute, University Hospital Vall d’Hebron, Barcelona, Spain, E-mail: mar.manu@vhir.org. Pedro L. Alonso, ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain, and Global Malaria Programme, WHO, Geneva, Switzerland, E-mail: alonsop@who.int.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Calis JC , van Hensbroek MB , de Haan RJ , Moons P , Brabin BJ , Bates I , 2008. HIV-associated anemia in children: a systematic review from a global perspective. AIDS 22: 1099–1112.
-
2.
Aguilar R , Moraleda C , Quinto L , Renom M , Mussacate L , Macete E , Aguilar JL , Alonso PL , Menendez C , 2012. Challenges in the diagnosis of iron deficiency in children exposed to high prevalence of infections. PLoS One 7: e50584.
-
3.
Mir N , Costello C , Luckit J , Lindley R , 1989. HIV-disease and bone marrow changes: a study of 60 cases. Eur J Haematol 42: 339–343.
-
4.
Mueller BU , Tannenbaum S , Pizzo PA , 1996. Bone marrow aspirates and biopsies in children with human immunodeficiency virus infection. J Pediatr Hematol Oncol 18: 266–271.
-
5.
Meira DG , Lorand-Metze I , Toro AD , Silva MT , Vilela MM , 2005. Bone marrow features in children with HIV infection and peripheral blood cytopenias. J Trop Pediatr 51: 114–119.
-
6.
Esan MO , Jonker FA , Hensbroek MB , Calis JC , Phiri KS , 2012. Iron deficiency in children with HIV-associated anaemia: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg 106: 579–587.
-
7.
Gonzalez R , Ataide R , Naniche D , Menendez C , Mayor A , 2012. HIV and malaria interactions: where do we stand? Expert Rev Anti Infect Ther 10: 153–165.
-
8.
Esan MO , van Hensbroek MB , Nkhoma E , Musicha C , White SA , Ter Kuile FO , Phiri KS , 2013. Iron supplementation in HIV-infected Malawian children with anemia: a double-blind, randomized, controlled trial. Clin Infect Dis 57: 1626–1634.
-
9.
Sacoor C et al. 2013. Profile: manhica health research centre (manhica HDSS). Int J Epidemiol 42: 1309–1318.
-
10.
Gonzalez R , Munguambe K , Aponte J , Bavo C , Nhalungo D , Macete E , Alonso P , Menendez C , Naniche D , 2012. High HIV prevalence in a southern semi-rural area of Mozambique: a community-based survey. HIV Med 13: 581–588.
-
11.
Moraleda C , de Deus N , Serna-Bolea C , Renom M , Quinto L , Macete E , Menendez C , Naniche D , 2014. Impact of HIV exposure on health outcomes in HIV-negative infants born to HIV-positive mothers in sub-Saharan Africa. J Acquir Immune Defic Syndr 65: 182–189.
-
12.
Pedrini M , Moraleda C , Macete E , Gondo K , Brabin BJ , Menendez C , 2015. Clinical, nutritional and immunological characteristics of HIV-infected children in an area of high HIV prevalence. J Trop Pediatr 61: 286–294.
-
13.
WHO , 2006. WHO 2006 Guidelines on ART in Infants and Children in Resource Limited Setting: Towards Universal Access, Recommendations for a Public Health Approach. Geneva, Switzerland: World Health Organization.
-
14.
Moraleda C et al. 2017. Anaemia in hospitalised preschool children from a rural area in Mozambique: a case control study in search for aetiological agents. BMC Pediatr 17: 63.
-
15.
Stoltzfus RJ , Dreyfuss ML , 1998. Guidelines for the Use of Iron Supplements to Prevent and Treat Iron Deficiency Anemia. Washington, DC: International Nutritional Anemia Consultative Group (INACG), World Health Organization (WHO), United Nations Childrens Fund (UNICEF).
-
16.
Sapero JJ , Lawless DK , 1953. The MIF stain-preservation technic for the identification of intestinal protozoa. Am J Trop Med Hyg 2: 613–619.
-
17.
Romagosa C , Menendez C , Ismail MR , Quinto L , Ferrer B , Alonso PL , Ordi J , 2004. Polarisation microscopy increases the sensitivity of hemozoin and Plasmodium detection in the histological assessment of placental malaria. Acta Trop 90: 277–284.
-
18.
Heinze G , Schemper M , 2002. A solution to the problem of separation in logistic regression. Stat Med 21: 2409–2419.
-
19.
Salome MA , Grotto HZ , 2002. Human immunodeficiency virus-related anemia of chronic disease: relationship to hematologic, immune, and iron metabolism parameters, and lack of association with serum interferon-gamma levels. AIDS Patient Care STDS 16: 361–365.
-
20.
Calis JC et al. 2010. Erythropoiesis in HIV-infected and uninfected Malawian children with severe anemia. AIDS 24: 2883–2887.
-
21.
Menendez C , Quinto LL , Kahigwa E , Alvarez L , Fernandez R , Gimenez N , Schellenberg D , Aponte JJ , Tanner M , Alonso PL , 2001. Effect of malaria on soluble transferrin receptor levels in Tanzanian infants. Am J Trop Med Hyg 65: 138–142.
-
22.
Totin D , Ndugwa C , Mmiro F , Perry RT , Jackson JB , Semba RD , 2002. Iron deficiency anemia is highly prevalent among human immunodeficiency virus-infected and uninfected infants in Uganda. J Nutr 132: 423–429.
-
23.
Miller MF , Humphrey JH , Iliff PJ , Malaba LC , Mbuya NV , Stoltzfus RJ ; ZVITAMBO Study Group , 2006. Neonatal erythropoiesis and subsequent anemia in HIV-positive and HIV-negative Zimbabwean babies during the first year of life: a longitudinal study. BMC Infect Dis 6: 1.
-
24.
Gordeuk VR , Delanghe JR , Langlois MR , Boelaert JR , 2001. Iron status and the outcome of HIV infection: an overview. J Clin Virol 20: 111–115.
-
25.
WHO , 2016. Guideline: Daily Iron Supplementation in Infants and Children. Geneva, Switzerland: World Health Organization.
-
26.
Bebell LM , Gasasira A , Kiggundu M , Dokomajilar C , Kamya MR , Charlebois ED , Havlir D , Rosenthal PJ , Dorsey G , 2007. HIV-1 infection in patients referred for malaria blood smears at government health clinics in Uganda. J Acquir Immune Defic Syndr 46: 624–630.
-
27.
Villamor E , Fataki MR , Mbise RL , Fawzi WW , 2003. Malaria parasitaemia in relation to HIV status and vitamin A supplementation among pre-school children. Trop Med Int Health 8: 1051–1061.
-
28.
Greenberg AE , Nsa W , Ryder RW , Medi M , Nzeza M , Kitadi N , Baangi M , Malanda N , Davachi F , Hassig SE , 1991. Plasmodium falciparum malaria and perinatally acquired human immunodeficiency virus type 1 infection in Kinshasa, Zaire. A prospective, longitudinal cohort study of 587 children. N Engl J Med 325: 105–109.
-
29.
Kalyesubula I , Musoke-Mudido P , Marum L , Bagenda D , Aceng E , Ndugwa C , Olness K , 1997. Effects of malaria infection in human immunodeficiency virus type 1-infected Ugandan children. Pediatr Infect Dis J 16: 876–881.
-
30.
Colebunders R et al. 1990. Incidence of malaria and efficacy of oral quinine in patients recently infected with human immunodeficiency virus in Kinshasa, Zaire. J Infect 21: 167–173.
-
31.
Flateau C , Le Loup G , Pialoux G , 2011. Consequences of HIV infection on malaria and therapeutic implications: a systematic review. Lancet Infect Dis 11: 541–556.
-
32.
Meyers TM , Pettifor JM , Gray GE , Crewe-Brown H , Galpin JS , 2000. Pediatric admissions with human immunodeficiency virus infection at a regional hospital in Soweto, South Africa. J Trop Pediatr 46: 224–230.
-
33.
Dignam JJ , Zhang Q , Kocherginsky M , 2012. The use and interpretation of competing risks regression models. Clin Cancer Res 18: 2301–2308.
-
34.
Ismail MR , Ordi J , Menendez C , Ventura PJ , Aponte JJ , Kahigwa E , Hirt R , Cardesa A , Alonso PL , 2000. Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Hum Pathol 31: 85–93.
-
35.
Dow A et al. 2012. Effects of cotrimoxazole prophylactic treatment on adverse health outcomes among HIV-exposed, uninfected infants. Pediatr Infect Dis J 31: 842–847.
-
36.
Spivak JL , Barnes DC , Fuchs E , Quinn TC , 1989. Serum immunoreactive erythropoietin in HIV-infected patients. JAMA. 261: 3104–3107.
-
37.
Macdougall LG , Moodley G , Eyberg C , Quirk M , 1982. Mechanisms of anemia in protein-energy malnutrition in Johannesburg. Am J Clin Nutr 35: 229–235.
-
38.
Vernazza PL , Pfister LA , Siegl G , Cassinotti P , 1996. High seroprevalence of parvovirus B19 among patients infected with human immunodeficiency virus. Clin Infect Dis 22: 198–199.
-
39.
LaMonte AC , Paul ME , Read JS , Frederick MM , Erdman DD , Han LL , Anderson LJ , 2004. Persistent parvovirus B19 infection without the development of chronic anemia in HIV-infected and -uninfected children: the women and infants transmission study. J Infect Dis 189: 847–851.
-
40.
Menendez C , Fleming AF , Alonso PL , 2000. Malaria-related anaemia. Parasitol Today 16: 469–476.
-
41.
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