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-
1.
Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE; Child Health Epidemiology Reference Group of WHO and UNICEF, 2012. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 379: 2151–2161.
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2.
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3.
Das SK, Faruque AS, Chisti MJ, Malek MA, Salam MA, Sack DA, 2012. Changing trend of persistent diarrhoea in young children over two decades: observations from a large diarrheal disease hospital in Bangladesh. Acta Paediatr 101: e452–e457.
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4.
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6.
Rahman AE, Moinuddin M, Molla M, Worku A, Hurt L, Kirkwood B, Mohan SB, Mazumder S, Bhutta Z, Raza F, Mrema S, Masanja H, Kadobera D, Waiswa P, Bahl R, Zangenbergh M, Muheh L, 2014. Childhood diarrheal deaths in seven low- and middle-income countries. Bull World Health Organ 92: 664–671.
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Samie A, El Bakri A, Ra'ed Abu Odeh R, 2012. Amoebiasis in the Tropics: Epidemiology and Pathogenesis. Available at: www.intechopen.com. Accessed October 10, 2014.
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Guerrant RL, Gilder TV, Steiner TS, Thielman NM, Slutsker L, Tauxe RV, Hennessy T, Griffin PM, DuPont H, Sack RB, Tarr P, Neill M, Nachamkin I, Reller LB, Osterholm MT, Bennish ML, Pickering LK, 2001. Practice guidelines for the management of infectious diarrhea. CID 32: 231–251.
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9.
Morris AJ, Murray PR, Reller LB, 1996. Contemporary testing for enteric pathogens: the potential for cost, time, and health care savings. J Clin Microbiol 34: 1776–1778.
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10.
Hines J, Nachamkin I, 1996. Effective use of the clinical microbiology laboratory for diagnosing diarrheal diseases. Clin Infect Dis 23: 1292–1301.
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11.
González-Ruiz A, Haque R, Aguirre A, Castañón G, Hall A, Guhl F, Ruiz-Palacios G, Miles MA, Warhurst DC, 1994. Value of microscopy in the diagnosis of dysentery associated with invasive Entamoeba histolytica. J Clin Pathol 47: 236–239.
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Tanyuksel M, Petri WA Jr, 2003. Laboratory diagnosis of amebiasis. Clin Microbiol Rev 16: 713–729.
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13.
Stark FRD, Beebe N, Marriott D, Elli J, Harkness J, 2007. A review of laboratory diagnostic techniques for Entamoeba species. Clin Microbiol Rev 20: 511–532.
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14.
Haque R, Ali IK, Akther S, Petri WA Jr, 1998. Comparison of PCR, isoenzyme analysis, and antigen detection for diagnosis of E. histolytica infection. J Clin Microbiol 36: 449–452.
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15.
Mirelman D, Nuchamowitz Y, Stolarsky T, 1997. Comparison of use of enzyme-linked immunosorbent assay-based kits and PCR amplification of rRNA genes for simultaneous detection of E. histolytica and E. dispar. J Clin Microbiol 35: 2405–2407.
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16.
Roy S, Kabir M, Mondal D, Ali IK, Petri WA Jr, Haque R, 2005. Real-time-PCR assay for diagnosis of E. histolytica infection. J Clin Microbiol 43: 2168–2172.
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Okeke IN, Ojo O, Lamikanra A, Kaper JB, 2003. Etiology of acute diarrhea in adults in southwestern Nigeria. J Clin Microbiol 41: 4525–4530.
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Idowu OA, Rowland SA, 2006. Oral fecal parasites and personal hygiene of food handlers in Abeokuta, Nigeria. Afr Health Sci 6: 160–164.
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20.
Oyerinde JPO, Alonge AA, Adegbite-Hollist AF, Ogunbi O, 1979. The epidemiology of Entamoeba histolytica in a Nigerian urban population. Int J Epidemiol 8: 55–60.
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21.
Ilero Town in Nigeria. Available at: http://www.fallingrain.com/world/NI/00/Ilero.html. Accessed May 20, 2015.
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22.
Smith B, Li N, Andersen AS, Slotved HC, Krogfelt KA, 2011. Optimising bacterial DNA extraction from faecal samples: comparison of three methods. Open Microbiol J 5: 14–17.
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23.
Verweij JJ, Oostvogel F, Brienen EAT, Nang-Beifubah A, Ziem J, Polderman AM, 2003. Prevalence of E. histolytica and E. dispar in northern Ghana. Trop Med Int Health 8: 1153–1156.
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24.
Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EAT, van Rooyen MAA, van Lieshout L, Poldermanet AM, 2004. Simultaneous detection of E. histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol 42: 1220–1223.
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McElligott JT, Naaktgeboren C, Makuma-Massa H, Summer AP, Deal JL, 2013. Prevalence of intestinal protozoa in communities along the Lake Victoria region of Uganda. Int J Infect Dis 17: 658–659.
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26.
Kebede A, Verweij JJ, Endeshaw T, Messele T, Tasew G, Petros B, Polderman AM, 2004. The use of real-time PCR to identify E. histolytica and E. dispar infections in prisoners and primary-school children in Ethiopia. Ann Trop Med Parasitol 98: 43–48.
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27.
Ayed SB, Abdallah RB, Mousli M, Aoun K, Thellier M, Bouratbine A, 2008. Molecular differentiation of E. histolytica and E. dispar from Tunisian food handlers with amoeba infection initially diagnosed by microscopy. Parasite 15: 65–68.
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29.
Opintan JA, Newman MJ, Ayeh-Kumi PF, Affrim R, Gepi-Attee R, Sevilleja JEAD, Roche JK, Nataro JP, Warren CA, Guerant RL, 2011. Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg 83: 936–943.
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Molecular Detection of the Carriage Rate of Four Intestinal Protozoa with Real-Time Polymerase Chain Reaction: Possible Overdiagnosis of Entamoeba histolytica in Nigeria
Michael A. Efunshile
Michael A. Efunshile
Institute of Medical Microbiology and Infectious Disease Epidemiology, Medical Faculty, University of Leipzig, Leipzig, Germany; Ebonyi State University, Abakaliki, Nigeria; Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital Copenhagen, Denmark; Department of International Health, Immunology, and Microbiology, University of Copenhagen, Denmark; Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark
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Bethrand A. F. Ngwu
Bethrand A. F. Ngwu
Institute of Medical Microbiology and Infectious Disease Epidemiology, Medical Faculty, University of Leipzig, Leipzig, Germany; Ebonyi State University, Abakaliki, Nigeria; Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital Copenhagen, Denmark; Department of International Health, Immunology, and Microbiology, University of Copenhagen, Denmark; Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark
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Jørgen A. L. Kurtzhals
Jørgen A. L. Kurtzhals
Institute of Medical Microbiology and Infectious Disease Epidemiology, Medical Faculty, University of Leipzig, Leipzig, Germany; Ebonyi State University, Abakaliki, Nigeria; Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital Copenhagen, Denmark; Department of International Health, Immunology, and Microbiology, University of Copenhagen, Denmark; Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark
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Sumrin Sahar
Sumrin Sahar
Institute of Medical Microbiology and Infectious Disease Epidemiology, Medical Faculty, University of Leipzig, Leipzig, Germany; Ebonyi State University, Abakaliki, Nigeria; Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital Copenhagen, Denmark; Department of International Health, Immunology, and Microbiology, University of Copenhagen, Denmark; Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark
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Brigitte König
Brigitte König
Institute of Medical Microbiology and Infectious Disease Epidemiology, Medical Faculty, University of Leipzig, Leipzig, Germany; Ebonyi State University, Abakaliki, Nigeria; Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital Copenhagen, Denmark; Department of International Health, Immunology, and Microbiology, University of Copenhagen, Denmark; Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark
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Christen R. Stensvold
Christen R. Stensvold
Institute of Medical Microbiology and Infectious Disease Epidemiology, Medical Faculty, University of Leipzig, Leipzig, Germany; Ebonyi State University, Abakaliki, Nigeria; Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital Copenhagen, Denmark; Department of International Health, Immunology, and Microbiology, University of Copenhagen, Denmark; Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark
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Diarrhea remains the second largest killer of children worldwide, and Nigeria ranks number two on the list of global deaths attributable to diarrhea. Meanwhile, prevalence studies on potentially diarrheagenic protozoa in asymptomatic carriers using molecular detection methods remain scarce in sub-Saharan countries. To overcome sensitivity issues related to microscopic detection and identification of cysts in stool concentrates, real-time polymerase chain reaction (PCR) was used to analyze genomic DNAs extracted from stool samples from 199 healthy school children for Entamoeba histolytica, E. dispar, Giardia intestinalis, and Cryptosporidium. Questionnaires were administered for epidemiological data collection. E. histolytica was not detected in any of the samples, whereas Giardia (37.2%), E. dispar (18.6%), and Cryptosporidium (1%) were found. Most of the children sourced their drinking water from community wells (91%), while the majority disposed of feces in the bush (81.9%). Our study is the first to use real-time PCR to evaluate the epidemiology of E. histolytica, Giardia, and Cryptosporidium in Nigeria where previous studies using traditional diagnostic techniques have suggested higher and lower carriage rates of E. histolytica and Giardia, respectively. It is also the first study to accurately identify the prevalence of common potentially diarrheagenic protozoa in asymptomatic carriers in sub-Saharan Africa.
Author Notes
Authors' addresses: Michael A. Efunshile, Institute of Medical Microbiology and Infectious Disease Epidemiology, University of Leipzig, Leipzig, Germany, and Department of Medical Microbiology and Parasitology, Ebonyi State University, Abakaliki, Ebonyi, Nigeria, E-mail: drefunshile@yahoo.com. Bethrand A. F. Ngwu, Department of Medical Microbiology and Parasitology, Ebonyi State University, Abakaliki, Ebonyi, Nigeria, E-mail: bethfrancis5@yahoo.com. Jørgen A. L. Kurtzhals, Department of Clinical Microbiology, Centre for Medical Parasitology, Copenhagen University Hospital, Copenhagen, Denmark, and Department of International Health, Immunology, and Microbiology, University of Copenhagen, Copenhagen, Denmark, E-mail: joergen.kurtzhals@rh.regionh.dk. Sumrin Sahar, Department of Microbiology and Infection Control, Statens Serum Institute, Copenhagen, Denmark, E-mail: sumrinsahar@yahoo.com. Brigitte König, Institute of Medical Microbiology and Infectious Disease Epidemiology, University of Leipzig, Leipzig, Germany, E-mail: brigitte.koenig@medizin.uni-leipzig.de. Christen R. Stensvold, Department of Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark, E-mail: run@ssi.dk.
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BibTeX
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-
1.
Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE; Child Health Epidemiology Reference Group of WHO and UNICEF, 2012. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 379: 2151–2161.
-
2.
UNICEF, WHO, 2009. Diarrhoea: Why Children are Still Dying and What Can Be Done. New York, NY: United Nations Children's Fund. Available at: http://www.who.int/child_adolescent_health/documents/who. Accessed October 6, 2014.
-
3.
Das SK, Faruque AS, Chisti MJ, Malek MA, Salam MA, Sack DA, 2012. Changing trend of persistent diarrhoea in young children over two decades: observations from a large diarrheal disease hospital in Bangladesh. Acta Paediatr 101: e452–e457.
-
4.
World Health Organization and United Nations Children's Fund, 2013. Ending Preventable Child Deaths from Pneumonia and Diarrhea by 2025. The Integrated Global Action Plan for Pneumonia and Diarrhea (GAPPD). Geneva, Switzerland and New York, NY: World Health Organization and United Nations Children's Fund. Available at: http://apps.who.int/iris/bitstream/10665/79200/1/9789241505239_eng.pdf?ua=1. Accessed October 4, 2014.
-
5.
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque ASG, Zaidi AKM, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM, 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.
-
6.
Rahman AE, Moinuddin M, Molla M, Worku A, Hurt L, Kirkwood B, Mohan SB, Mazumder S, Bhutta Z, Raza F, Mrema S, Masanja H, Kadobera D, Waiswa P, Bahl R, Zangenbergh M, Muheh L, 2014. Childhood diarrheal deaths in seven low- and middle-income countries. Bull World Health Organ 92: 664–671.
-
7.
Samie A, El Bakri A, Ra'ed Abu Odeh R, 2012. Amoebiasis in the Tropics: Epidemiology and Pathogenesis. Available at: www.intechopen.com. Accessed October 10, 2014.
-
8.
Guerrant RL, Gilder TV, Steiner TS, Thielman NM, Slutsker L, Tauxe RV, Hennessy T, Griffin PM, DuPont H, Sack RB, Tarr P, Neill M, Nachamkin I, Reller LB, Osterholm MT, Bennish ML, Pickering LK, 2001. Practice guidelines for the management of infectious diarrhea. CID 32: 231–251.
-
9.
Morris AJ, Murray PR, Reller LB, 1996. Contemporary testing for enteric pathogens: the potential for cost, time, and health care savings. J Clin Microbiol 34: 1776–1778.
-
10.
Hines J, Nachamkin I, 1996. Effective use of the clinical microbiology laboratory for diagnosing diarrheal diseases. Clin Infect Dis 23: 1292–1301.
-
11.
González-Ruiz A, Haque R, Aguirre A, Castañón G, Hall A, Guhl F, Ruiz-Palacios G, Miles MA, Warhurst DC, 1994. Value of microscopy in the diagnosis of dysentery associated with invasive Entamoeba histolytica. J Clin Pathol 47: 236–239.
-
12.
Tanyuksel M, Petri WA Jr, 2003. Laboratory diagnosis of amebiasis. Clin Microbiol Rev 16: 713–729.
-
13.
Stark FRD, Beebe N, Marriott D, Elli J, Harkness J, 2007. A review of laboratory diagnostic techniques for Entamoeba species. Clin Microbiol Rev 20: 511–532.
-
14.
Haque R, Ali IK, Akther S, Petri WA Jr, 1998. Comparison of PCR, isoenzyme analysis, and antigen detection for diagnosis of E. histolytica infection. J Clin Microbiol 36: 449–452.
-
15.
Mirelman D, Nuchamowitz Y, Stolarsky T, 1997. Comparison of use of enzyme-linked immunosorbent assay-based kits and PCR amplification of rRNA genes for simultaneous detection of E. histolytica and E. dispar. J Clin Microbiol 35: 2405–2407.
-
16.
Roy S, Kabir M, Mondal D, Ali IK, Petri WA Jr, Haque R, 2005. Real-time-PCR assay for diagnosis of E. histolytica infection. J Clin Microbiol 43: 2168–2172.
-
17.
World Health Organization, 1997. Amebiasis. WHO Wkly Epidemiol Rec 72: 97–100.
-
18.
Okeke IN, Ojo O, Lamikanra A, Kaper JB, 2003. Etiology of acute diarrhea in adults in southwestern Nigeria. J Clin Microbiol 41: 4525–4530.
-
19.
Idowu OA, Rowland SA, 2006. Oral fecal parasites and personal hygiene of food handlers in Abeokuta, Nigeria. Afr Health Sci 6: 160–164.
-
20.
Oyerinde JPO, Alonge AA, Adegbite-Hollist AF, Ogunbi O, 1979. The epidemiology of Entamoeba histolytica in a Nigerian urban population. Int J Epidemiol 8: 55–60.
-
21.
Ilero Town in Nigeria. Available at: http://www.fallingrain.com/world/NI/00/Ilero.html. Accessed May 20, 2015.
-
22.
Smith B, Li N, Andersen AS, Slotved HC, Krogfelt KA, 2011. Optimising bacterial DNA extraction from faecal samples: comparison of three methods. Open Microbiol J 5: 14–17.
-
23.
Verweij JJ, Oostvogel F, Brienen EAT, Nang-Beifubah A, Ziem J, Polderman AM, 2003. Prevalence of E. histolytica and E. dispar in northern Ghana. Trop Med Int Health 8: 1153–1156.
-
24.
Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EAT, van Rooyen MAA, van Lieshout L, Poldermanet AM, 2004. Simultaneous detection of E. histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol 42: 1220–1223.
-
25.
McElligott JT, Naaktgeboren C, Makuma-Massa H, Summer AP, Deal JL, 2013. Prevalence of intestinal protozoa in communities along the Lake Victoria region of Uganda. Int J Infect Dis 17: 658–659.
-
26.
Kebede A, Verweij JJ, Endeshaw T, Messele T, Tasew G, Petros B, Polderman AM, 2004. The use of real-time PCR to identify E. histolytica and E. dispar infections in prisoners and primary-school children in Ethiopia. Ann Trop Med Parasitol 98: 43–48.
-
27.
Ayed SB, Abdallah RB, Mousli M, Aoun K, Thellier M, Bouratbine A, 2008. Molecular differentiation of E. histolytica and E. dispar from Tunisian food handlers with amoeba infection initially diagnosed by microscopy. Parasite 15: 65–68.
-
28.
Santos FLN, de Souza Gonçalves M, Soares NM, 2011. Validation and utilization of PCR for differential diagnosis and prevalence determination of E. histolytica/E. dispar in Salvador City, Brazil. Braz J Infect Dis 15: 119–125.
-
29.
Opintan JA, Newman MJ, Ayeh-Kumi PF, Affrim R, Gepi-Attee R, Sevilleja JEAD, Roche JK, Nataro JP, Warren CA, Guerant RL, 2011. Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg 83: 936–943.
-
30.
Gupta SS, Singh O, Shukla S, Raj MK, 2009. Acute fulminant necrotizing amoebic colitis: a rare and fatal complication of amebiasis: a case report. Cases J 2: 6557–6561.
-
31.
Wanke C, Butler T, Islam M, 1988. Epidemiologic and clinical features of invasive amebiasis in Bangladesh: a case-control comparison with other diarrheal diseases and postmortem findings. Am J Trop Med Hyg 38: 335–341.
-
32.
Roy S, Kabir M, Mondal D, Ali IK, Petri WA Jr, Haque R, 2005. Real-time-PCR assay for diagnosis of Entamoeba histolytica infection. Clin Microbiol 43: 2168–2172.
-
33.
Visser LG, Verweij JJ, Van Esbroeck M, Edeling WM, Clerinx J, Polderman AM, 2006. Diagnostic methods for differentiation of Entamoeba histolytica and Entamoeba dispar in carriers: performance and clinical implications in a non-endemic setting. Int J Med Microbiol 296: 397–403.
-
34.
Cegielski JP, Ortega YR, McKee S, Madden JF, Gaido L, Schwartz DA, Manji K, Jorgensen AF, Miller SE, Pulipaka UP, Msengi AE, Mwakyusa DH, Sterling CR, Reller LB, 1999. Cryptosporidium, Enterocytozoon, and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis 28: 314–321.
-
35.
Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, Akiyoshi DE, Tzipori S, 2005. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg 73: 921–925.
-
36.
Houpt ER, Bushen OY, Sam NE, Kohli A, Asgharpour A, Ng CT, Calfee DP, Guerrant RL, Maro V, Ole-Nguyaine S, Shao JF, 2005. Short report: asymptomatic Cryptosporidium hominis infection among human immunodeficiency virus-infected patients in Tanzania. Am J Trop Med Hyg 73: 520–522.
-
37.
Esteban JG, Aguirre C, Flores A, Strauss W, Angles R, Mas-Coma S, 1998. High Cryptosporidium prevalences in healthy Aymara children from the northern Bolivian Altiplano. Am J Trop Med Hyg 58: 50–55.
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