The effects of co-infection with human parvovirus B19 and Plasmodium falciparum on type and degree of anaemia in Ghanaian children

Asian Pacific Journal of Tropical Biomedicine

Volumn 3, Issue 2, 2013, Pages 129-139

  Duedu, Kwabena Obeng ^a,b   Sagoe, Kwamena William Coleman ^a   Ayeh Kumi, Patrick Ferdinand ^a   Affrim, Raymond Bedu ^c   Adiku, Theophilus ^a  

^a UNIVERSITY OF GHANA   (Ghana)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Princess Marie Louis Children's Hospital   (Ghana)

Author keywords

Anaemia; Children; Ghana; Human parvovirus B19; Malaria

Indexed keywords

VIRUS DNA;

ARTICLE; BLOOD CELL COUNT; CHILD; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE SEVERITY; ERYTHEMA INFECTIOSUM; ETHNIC GROUP; GHANAIAN; HIGH RISK PATIENT; HUMAN; HUMAN PARVOVIRUS B19; INFANT; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MICROCYTIC ANEMIA; MIXED INFECTION; NONHUMAN; NORMOCHROMIC NORMOCYTIC ANEMIA; PARASITE IDENTIFICATION; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PRIORITY JOURNAL; RISK ASSESSMENT; SCHOOL CHILD; SCREENING TEST; ADOLESCENT; ANEMIA; COINFECTION; COMPLICATION; FEMALE; GHANA; ISOLATION AND PURIFICATION; MALARIA, FALCIPARUM; MALE; PARASITOLOGY; PARVOVIRIDAE INFECTIONS; PATHOPHYSIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PREVALENCE; RISK FACTOR; VIROLOGY;

ADOLESCENT; ANEMIA; CHILD; CHILD, PRESCHOOL; COINFECTION; FEMALE; GHANA; HUMANS; INFANT; MALARIA, FALCIPARUM; MALE; PARVOVIRIDAE INFECTIONS; PARVOVIRUS B19, HUMAN; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PREVALENCE; RISK FACTORS;

EID: 84873025590     PISSN: 22211691     EISSN: None     Source Type: Journal    
DOI: 10.1016/S2221-1691(13)60037-4     Document Type: Article

References (101)

1. van Hensbroek MB, Jonker F, Bates I Severe acquired anaemia in Africa: new concepts. Br J Haematol 2011, 10.1111/j.1365-2141.2011.08761.x.
2. Dicko A, Klion AD, Thera MA, Sagara I, Yalcouye D, Niambele MB, et al. The etiology of severe anemia in a village and a periurban area in Mali. Blood 2004, 104:1198-1200.
3. van Hensbroek BM, Calis JC, Phiri KS, Vet R, Munthali F, Kraaijenhagen R, et al. Pathophysiological mechanisms of severe anaemia in Malawian children. PLoS One 2010, 5:e12589.
4. Mishra B, Malhotra P, Ratho RK, Singh MP, Varma S, Varma N Human parvovirus B19 in patients with aplastic anemia. Am J Hematol 2005, 79:166-167.
5. Asobayire FS, Adou P, Davidsson L, Cook JD, Hurrell RF Prevalence of iron deficiency with and without concurrent anemia in population groups with high prevalences of malaria and other infections: a study in Cote d'Ivoire. Am J Clin Nutr 2001, 74:776-782.
6. Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, et al. Epidemiology of plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 2007, 77:88-98.
7. Dreyfuss ML, Stoltzfus RJ, Shrestha JB, Pradhan EK, LeClerq SC, Khatry SK, et al. Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J Nutr 2000, 130:2527-2536.
8. Olsen A, Magnussen P, Ouma JH, Andreassen J, Friis H The contribution of hookworm and other parasitic infections to haemoglobin and iron status among children and adults in western Kenya. Trans R Soc Trop Med Hyg 1998, 92:643-649.
9. Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KK, Sumbele I Malaria and helminth co-infection in children living in a malaria endemic setting of mount Cameroon and predictors of anemia. J Parasitol 2006, 92:1191-1195.
10. Akhwale WS, Lum JK, Kaneko A, Eto H, Obonyo C, Bjorkman A, et al. Anemia and malaria at different altitudes in the western highlands of Kenya. Acta Trop 2004, 91:167-175.
11. van den Broek NR, Letsky EA Etiology of anemia in pregnancy in south Malawi. Am J Clin Nutr 2000, 72:247S-256S.
12. Calis JC, Phiri KS, Faragher EB, Brabin BJ, Bates I, Cuevas LE, et al. Severe anemia in Malawian children. N Engl J Med 2008, 358:888-899.
13. Phiri KS, Calis JC, Faragher B, Nkhoma E, Ng'oma K, Mangochi B, et al. Long term outcome of severe anaemia in Malawian children. PLoS One 2008, 3:e2903.
14. Carraturo A, Catalani V, Ottaviani D, Menichelli P, Rossini M, Terella D, et al. Parvovirus B19 infection and severe anemia in renal transplant recipients. Sci World J 2012, 2012:102829.
15. Winbo A, Sandstrom O, Palmqvist R, Rydberg A Iron-deficiency anaemia, gastric hyperplasia, and elevated gastrin levels due to potassium channel dysfunction in the Jervell and Lange-Nielsen Syndrome. Cardiol Young 2012, 1-10.
16. Rogawski ET, Chaluluka E, Molyneux ME, Feng G, Rogerson SJ, Meshnick SR The effects of malaria and intermittent preventive treatment during pregnancy on fetal anemia in Malawi. Clin Infect Dis 2012, 55(8):1096-1102.
17. Menendez C, Kahigwa E, Hirt R, Vounatsou P, Aponte JJ, Font F, et al. Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet 1997, 350:844-850.
18. Oppenheimer SJ, MacFarlane SB, Moody JB, Bunari O, Williams TE, Harrison C, et al. Iron and infection in infancy-report on field studies in Papua New Guinea: 1. Demographic description and pilot surveys. Ann Trop Paediatr 1984, 4:135-143.
19. Kahigwa E, Schellenberg D, Sanz S, Aponte JJ, Wigayi J, Mshinda H, et al. Risk factors for presentation to hospital with severe anaemia in Tanzanian children: a case-control study. Trop Med Int Health 2002, 7:823-830.
20. Lewis DK, Whitty CJ, Walsh AL, Epino H, Broek NR, Letsky EA, et al. Treatable factors associated with severe anaemia in adults admitted to medical wards in Blantyre, Malawi, an area of high HIV seroprevalence. Trans R Soc Trop Med Hyg 2005, 99:561-567.
21. Newton CR, Warn PA, Winstanley PA, Peshu N, Snow RW, Pasvol G, et al. Severe anaemia in children living in a malaria endemic area of Kenya. Trop Med Int Health 1997, 2:165-178.
22. Geelhoed D, Agadzi F, Visser L, Ablordeppey E, Asare K, O'Rourke P, et al. Severe anemia in pregnancy in rural Ghana: a case-control study of causes and management. Acta Obstet Gynecol Scand 2006, 85:1165-1171.
23. Amoa AB, Lavu E, Ray U, Sapuri M, Kariwiga G, Heywood S The aetiology of severe anaemia among antenatal patients of the Port Moresby General Hospital. P N G Med J 2003, 46:143-151.
24. Muir KR, Chilvers CE, Harriss C, Coulson L, Grainge M, Darbyshire P, et al. The role of occupational and environmental exposures in the aetiology of acquired severe aplastic anaemia: a case control investigation. Br J Haematol 2003, 123:906-914.
25. Ahmed F Anaemia in Bangladesh: a review of prevalence and aetiology. Public Health Nutr 2000, 3:385-393.
26. van den Broek N The aetiology of anaemia in pregnancy in West Africa. Trop Doct 1996, 26:5-7.
27. Potter CG, Potter AC, Hatton CS, Chapel HM, Anderson MJ, Pattison JR, et al. Variation of erythroid and myeloid precursors in the marrow and peripheral blood of volunteer subjects infected with human parvovirus (B19). J Clin Invest 1987, 79:1486-1492.
28. Wan Z, Zhi N, Wong S, Keyvanfar K, Liu D, Raghavachari N, et al. Human parvovirus B19 causes cell cycle arrest of human erythroid progenitors via deregulation of the E2F family of transcription factors. J Clin Invest 2010, 120:3530-3544.
29. Young N Hematologic and hematopoietic consequences of B19 parvovirus infection. Semin Hematol 1988, 25:159-172.
30. Carzavec D, Gacina P, Vasilj A, Katovic SK Aplastic crisis induced by human parvovirus B19 as an initial presentation of hereditary spherocytosis. Coll Antropol 2010, 34:619-621.
31. Saarinen UM, Chorba TL, Tattersall P, Young NS, Anderson LJ, Palmer E, et al. Human parvovirus B19-induced epidemic acute red cell aplasia in patients with hereditary hemolytic anemia. Blood 1986, 67:1411-1417.
32. Muir K, Todd WT, Watson WH, Fitzsimons E Viral-associated haemophagocytosis with parvovirus-B19-related pancytopenia. Lancet 1992, 339:1139-1140.
33. Rao SP, Desai N, Miller ST B19 parvovirus infection and transient aplastic crisis in a child with sickle cell anemia. J Pediatr Hematol Oncol 1996, 18:175-177.
34. Yermalovich MA, Hubschen JM, Semeiko GV, Samoilovich EO, Muller CP Human parvovirus B19 surveillance in patients with rash and fever from Belarus. J Med Virol 2012, 84:973-978.
35. Gadage VS, Viswanathan S, Kunal S, Subramanian PG, Gujral S Parvovirus B19 presenting with persistent pancytopenia in a patient of T-ALL post induction chemotherapy diagnosed on bone marrow examination. Indian J Pathol Microbiol 2011, 54:603-605.
36. Tsukada Y, Yokoyama K, Ishida A, Handa M, Mori T, Kizaki M, et al. Erythroid crisis caused by parvovirus B19 transmitted via red blood cell transfusion. Intern Med 2011, 50:2379-2382.
37. Seo JY, Kim HJ, Kim SH Neutropenia in parvovirus B19-associated pure red cell aplasia. Ann Hematol 2011, 90:975-978.
38. Broliden K, Tolfvenstam T, Norbeck O Clinical aspects of parvovirus B19 infection. J Intern Med 2006, 260:285-304.
39. Wen JQ, Zhou N, Li D, Feng HL, Wang H Study on clinical characteristics and follow-up visit of acquired aplastic anemia associated with parvovirus b19 infection. Indian J Pediatr 2012, 79:741-746.
40. Ho M, Webster HK, Looareesuwan S, Supanaranond W, Phillips RE, Chanthavanich P, et al. Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. J Infect Dis 1986, 153:763-771.
41. Jones PH, Pickett LC, Anderson MJ, Pasvol G Human parvovirus infection in children and severe anaemia seen in an area endemic for malaria. J Trop Med Hyg 1990, 93:67-70.
42. Wildig J, Cossart Y, Peshu N, Gicheru N, Tuju J, Williams TN, et al. Parvovirus B19 infection and severe anaemia in Kenyan children: a retrospective case control study. BMC Infect Dis 2010, 10:88.
43. Wildig J, Michon P, Siba P, Mellombo M, Ura A, Mueller I, et al. Parvovirus B19 infection contributes to severe anemia in young children in Papua New Guinea. J Infect Dis 2006, 194:146-153.
44. Wildig J, Mueller I, Kiniboro B, Maraga S, Siba P, Cossart Y Seroprevalence of antibodies to parvovirus B19 among children in Papua New Guinea. Am J Trop Med Hyg 2007, 77:354-357.
45. Parsyan A, Kerr S, Owusu-Ofori S, Elliott G, Allain JP Reactivity of genotype-specific recombinant proteins of human erythrovirus B19 with plasmas from areas where genotype 1 or 3 is endemic. J Clin Microbiol 2006, 44:1367-1375.
46. Lortholary O, Eliaszewicz M, Dupont B, Courouce AM Parvovirus B19 infection during acute Plasmodium falciparum malaria. Eur J Haematol 1992, 49:219.
47. Scarlata F, Gianelli E, Miceli S, Galimberti L, Antinori S Acute parvovirus B19 infection and anemia during Plasmodium falciparum malaria. Clin Infect Dis 2002, 35:1449-1451.
48. Urganci N, Arapoglu M, Kayaalp N Plasmodium falciparum malaria with coexisting parvovirus B19 infection. Indian Pediatr 2003, 40:369-370.
49. Gupta R, Singh T Parvovirus B19 co-infection with falciparum malaria: a cause of severe anemia. Haematologica 2005, 90:ECR41.
50. Ingrassia F, Gadaleta A, Maggi P, Pastore G Plasmodium falciparum malaria and Parvovirus B19; a case of acute co-infection. BMC Infect Dis 2010, 10:87.
51. Weiffenbach J, Bald R, Gloning KP, Minderer S, Gartner BC, Weidner A, et al. Serological and virological analysis of maternal and fetal blood samples in prenatal human parvovirus b19 infection. J Infect Dis 2012, 205:782-788.
52. Slavov SN, Kashima S, Silva-Pinto AC, Covas DT Genotyping of human parvovirus B19 among Brazilian patients with hemoglobinopathies. Can J Microbiol 2012, 58:200-205.
53. Puccetti C, Contoli M, Bonvicini F, Cervi F, Simonazzi G, Gallinella G, et al. Parvovirus B19 in pregnancy: possible consequences of vertical transmission. Prenat Diagn 2012, 32(9):897-902.
54. Pedranti MS, Barbero P, Wolff C, Ghietto LM, Zapata M, Adamo MP Infection and immunity for human parvovirus B19 in patients with febrile exanthema. Epidemiol Infect 2012, 140:454-461.
55. Heavey E Parvovirus B19 exposure during pregnancy. Nursing 2012, 42:69.
56. Park SJ, Kim JH, Ha TS, Shin JI Association of parvovirus B19 infection with systemic lupus erythematosus: role of Th1 predominance. J Rheumatol 2011, 38:1221.
57. Lamont RF, Sobel JD, Vaisbuch E, Kusanovic JP, Mazaki-Tovi S, Kim SK, et al. Parvovirus B19 infection in human pregnancy. BJOG 2011, 118:175-186.
58. Koepsell SA, Anderson DR, Radio SJ Parvovirus B19 is a bystander in adult myocarditis. Cardiovasc Pathol 2012, 21(6):476-481.
59. Koehl B, Oualha M, Lesage F, Rambaud C, Canioni D, Hubert P, et al. Fatal parvovirus B19 myocarditis in children and possible dysimmune mechanism. Pediatr Infect Dis J 2012, 31:418-421.
60. Castagna L, Furst S, El Cheikh J, Faucher C, Blaise D Parvovirus B19 as an etiological agent of acute pleuro-pericarditis. Bone Marrow Transplant 2011, 46:317-318.
61. Mogensen TH, Jensen JM, Hamilton-Dutoit S, Larsen CS Chronic hepatitis caused by persistent parvovirus B19 infection. BMC Infect Dis 2010, 10:246.
62. Danda D, Naina HV, Abraham M, Mathew AJ, Badika AK, Mathew J Parvovirus B19 serology in early inflammatory polyarthritis-experience from a tertiary core teaching hospital in South India. J Indian Med Assoc 2010, 108:677-678. 681.
63. Bozzola E, Krzysztofiak A, Cortis E Neurological impairment and arthritis in an immunocompetent child with human parvovirus B19 chronic infection. Infez Med 2010, 18:187-190.
64. Bock CT, Klingel K, Kandolf R Human parvovirus B19-associated myocarditis. N Engl J Med 2010, 362:1248-1249.
65. Adda J, Machado S, Eberst E, Roubille C, Macia JC, Roubille F Parvovirus B19 infection and acute myocarditis. Intern Med 2010, 49:79.
66. Yang SH, Lin LW, Fang YJ, Cheng AL, Kuo SH Parvovirus B19 infection-related acute hepatitis after rituximab-containing regimen for treatment of diffuse large B-cell lymphoma. Ann Hematol 2012, 91:291-294.
67. Sun L, Zhang JC Acute fulminant hepatitis with bone marrow failure in an adult due to parvovirus B19 infection. Hepatology 2012, 55:329-330.
68. Compston LI, Li C, Sarkodie F, Owusu-Ofori S, Opare-Sem O, Allain JP Prevalence of persistent and latent viruses in untreated patients infected with HIV-1 from Ghana, West Africa. J Med Virol 2009, 81:1860-1868.
69. Candotti D, Etiz N, Parsyan A, Allain JP Identification and characterization of persistent human erythrovirus infection in blood donor samples. J Virol 2004, 78:12169-12178.
70. Yeats J, Daley H, Hardie D Parvovirus B19 infection does not contribute significantly to severe anaemia in children with malaria in Malawi. Eur J Haematol 1999, 63:276-277.
71. Parsyan A, Addo-Yobo E, Owusu-Ofori S, Akpene H, Sarkodie F, Allain JP Effects of transfusion on human erythrovirus B19-susceptible or -infected pediatric recipients in a genotype 3-endemic area. Transfusion 2006, 46:1593-1600.
72. Lewis SM, Bain BJ, Bates I, Dacie JV Dacie and Lewis practical haematology 2006, Churchill Livingstone/Elsevier, Philadelphia.
73. Manning A, Willey SJ, Bell JE, Simmonds P Comparison of tissue distribution, persistence, and molecular epidemiology of parvovirus B19 and novel human parvoviruses PARV4 and human bocavirus. J Infect Dis 2007, 195:1345-1352.
74. Lefrere J-J, Servant-Delmas A, Candotti D, Mariotti M, Thomas I, Brossard Y, et al. Persistent B19 infection in immunocompetent individuals: implications for transfusion safety. Blood 2005, 106:2890-2895.
75. Cassinotti P, Burtonboy G, Fopp M, Siegl G Evidence for persistence of human parvovirus B19 DNA in bone marrow. J Med Virol 1997, 53:229-232.
76. Eis-Hubinger AM, Reber U, Abdul-Nour T, Glatzel U, Lauschke H, Putz U Evidence for persistence of parvovirus B19 DNA in livers of adults. J Med Virol 2001, 65:395-401.
77. Schenk T, Enders M, Pollak S, Hahn R, Huzly D High prevalence of human parvovirus B19 DNA in myocardial autopsy samples from subjects without myocarditis or dilative cardiomyopathy. J Clin Microbiol 2009, 47:106-110.
78. Heegaard ED, Brown KE Human parvovirus B19. Clin Microbiol Rev 2002, 15:485-505.
79. Commey JO, Dekyem P Childhood deaths from anaemia in Accra, Ghana. West Afr J Med 1995, 14:101-104.
80. Macro ICF Nutrition of children and women in Ghana: A new look at data from the 2008 Ghana Demographic and Health Survey 2010, Claverton, Maryland, USA.
81. Klinkenberg E, McCall PJ, Wilson MD, Akoto AO, Amerasinghe FP, Bates I, et al. Urban malaria and anaemia in children: a cross-sectional survey in two cities of Ghana. Trop Med Int Health 2006, 11:578-588.
82. Alberta Minister of the Environment, ICF Consulting Exploring the potential for an air emissions trading system for Alberta: lessons learned from exsisting trading regimes-final report 2002, ICF Consulting, Alberta.
83. Adjuik M, Agnamey P, Babiker A, Borrmann S, Brasseur P, Cisse M, et al. Amodiaquine-artesunate versus amodiaquine for uncomplicated Plasmodium falciparum malaria in African children: a randomised, multicentre trial. Lancet 2002, 359:1365-1372.
84. Okrah J, Traore C, Pale A, Sommerfeld J, Muller O Community factors associated with malaria prevention by mosquito nets: an exploratory study in rural Burkina Faso. Trop Med Int Health 2002, 7:240-248.
85. Cisse B, Sokhna C, Boulanger D, Milet J, Bael H, Richardson K, et al. Seasonal intermittent preventive treatment with artesunate and sulfadoxine-pyrimethamine for prevention of malaria in Senegalese children: a randomised, placebo-controlled, double-blind trial. Lancet 2006, 367:659-667.
86. Bhattarai A, Ali AS, Kachur SP, Martensson A, Abbas AK, Khatib R, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med 2007, 4:e309.
87. Grabowsky M, Nobiya T, Selanikio J Sustained high coverage of insecticide-treated bednets through combined Catch-up and Keep-up strategies. Trop Med Int Health 2007, 12:815-822.
88. Adjei GO, Darkwah AK, Goka BQ, Bart-Plange C, Alifrangis ML, Kurtzhals JA, et al. Parents' perceptions, attitudes and acceptability of treatment of childhood malaria with artemisinin combination therapies in Ghana. Ghana Med J 2009, 43:99-106.
89. Dodoo AN, Fogg C, Asiimwe A, Nartey ET, Kodua A, Tenkorang O, et al. Pattern of drug utilization for treatment of uncomplicated malaria in urban Ghana following national treatment policy change to artemisinin-combination therapy. Malar J 2009, 8:2.
90. Killeen GF, Tami A, Kihonda J, Okumu FO, Kotas ME, Grundmann H, et al. Cost-sharing strategies combining targeted public subsidies with private-sector delivery achieve high bednet coverage and reduced malaria transmission in Kilombero Valley, Southern Tanzania. BMC Infect Dis 2007, 7:121.
91. Okiro EA, Hay SI, Gikandi PW, Sharif SK, Noor AM, Peshu N, et al. The decline in paediatric malaria admissions on the coast of Kenya. Malaria Journal 2007, 6:151.
92. Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, et al. Changes in malaria indices between 1999 and 2007 in the Gambia: a retrospective analysis. Lancet 2008, 372:1545-1554.
93. O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 2008, 372:1555-1562.
94. Owusu-Agyei S, Asante KP, Adjuik M, Adjei G, Awini E, Adams M, et al. Epidemiology of malaria in the forest-savanna transitional zone of Ghana. Malar J 2009, 8:220.
95. Schellenberg D, Schellenberg JR, Mushi A, Savigny D, Mgalula L, Mbuya C, et al. The silent burden of anaemia in Tanzanian children: a community-based study. Bull World Health Organ 2003, 81:581-590.
96. Premji Z, Hamisi Y, Shiff C, Minjas J, Lubega P, Makwaya C Anaemia and Plasmodium falciparum infections among young children in an holoendemic area, Bagamoyo, Tanzania. Acta Trop 1995, 59:55-64.
97. Candotti D, Danso K, Parsyan A, Dompreh A, Allain JP Maternal-fetal transmission of human parvovirus B19 genotype 3. J Infect Dis 2006, 194:608-611.
98. Compston LI, Sarkobie F, Li C, Candotti D, Opare-Sem O, Allain JP Multiplex real-time PCR for the detection and quantification of latent and persistent viral genomes in cellular or plasma blood fractions. J Virol Methods 2008, 151:47-54.
99. Hoffbrand AV, Moss PAH, Pettit JE Essential haematology 2006, Blackwell Pub, Oxford.
100. Breman JG The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg 2001, 64:1-11.
101. Ballou WR, Reed JL, Noble W, Young NS, Koenig S Safety and immunogenicity of a recombinant parvovirus B19 vaccine formulated with MF59C.1. J Infect Dis 2003, 187:675-678.