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Frontiers of Medicine

Front. Med.    2010, Vol. 4 Issue (2) : 192-198     DOI: 10.1007/s11684-010-0039-0
Research articles |
Co-infection of HIV and parasites in China: Results from an epidemiological survey in rural areas of Fuyang city, Anhui province, China
Li-Guang TIAN MPH1,Jia-Xu CHEN PhD1,Yu-Chun CAI BM1,Jian GUO MPH1,Xiao-Mei TONG1,Qin LIU DVM1,Xiao-Nong ZHOU PhD1,Tian-Ping WANG PhD2,Xiao-Mei YIN2,Wei-Duo WU2,Li ZHOU2,Feng-Feng WANG2,Zhen-Li WANG MSc2,Guo-Jin CHENG3,Peter STEINMANN PhD4,Lan-Hua LI MSc5,
1.National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, China; 2.Anhui Institute of Parasitic Disease Control, Wuhu 241000, China; 3.Fuyang Center for Disease Control and Prevention, Fuyang 236000, China; 4.National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, China;Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel CH-4000, Switzerland;University of Basel, Basel CH-4000, Switzerland; 5.Weifang Medical University, Weifang 261000, China;
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Abstract The aim of this study was to investigate epidemiological characteristics of co-infection of HIV and intestinal parasites in a HIV/AIDS highly endemic area in China. A cross-sectional survey was carried out in two villages where HIV/AIDS prevalence in residents was over 1%. Stool samples of all residents in the two targeted villages were examined for the presence of intestinal parasites. Blood examination was performed for the HIV infection detection and anemia test. A questionnaire survey was carried out in all residents participating in the study. A total of 769 individuals were enrolled in the investigation, 720 of whom were involved in stool examination of intestinal parasites. The infection rates of parasites in the residents of the targeted villages were as follows: 0.56% for Ascaris lumbricoides, 4.03% for Hookworm, 0.28% for Trichuris trichiura, 0.42% for Clonorchis sinensis, 21.39% for Blastocystis hominis, 3.89% for Giardia lamblia, 1.67% for Entamoeba spp., 4.44% for Cryptosporidium spp., and no infection for Strongyloides stercoralis. The overall infection rate of intestinal worms was 4.72%, intestinal parasite infection rate was 24.31%, the anemia prevalence rate was 34.68%, the co-infection rate of HIV and intestinal helminthes 2.17%, the co-infection rate of HIV and intestinal protozoa 28.26%, of which the co-infection rates of HIV and Blastocystis hominis, and HIV and Cryptosporidium spp. were 19.57% and 13.04%, respectively. A significant difference of Cryptosporidium spp. infection rate was found between HIV-positive group (13.04%) and HIV-negative group (4.70%) (P<0.05). Higher prevalence of anemia (34.68%) occurred in the study villages, particularly in children (>50%) and women (>39%). It was concluded that the infection rate of intestinal protozoa in the residents was higher than that of intestinal helminthes in the local setting, and a same pattern appeared in the co-infection rate of HIV and parasites. An interesting finding is that the infection rate of Cryptosporidium spp. among the HIV-positives was significantly higher than that in the HIV-negatives, and children and women had higher anemia prevalence.
Keywords human immunodeficiency virus (HIV)      acquired immunodeficiency syndrome (AIDS)      co-infection      intestinal parasites      helminthes      protozoa      China      
Issue Date: 05 June 2010
 Cite this article:   
Xiao-Mei TONG,Li-Guang TIAN MPH,Yu-Chun CAI BM, et al. Co-infection of HIV and parasites in China: Results from an epidemiological survey in rural areas of Fuyang city, Anhui province, China[J]. Front. Med., 2010, 4(2): 192-198.
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Xiao-Mei TONG
Yu-Chun CAI BM
Xiao-Nong ZHOU PhD
Tian-Ping WANG PhD
Hotez P J, Bottazzi M E, Franco-Paredes C, Ault S K, Periago M R. The neglected tropical diseases of Latin America and the Caribbean:a review of disease burden and distribution and a roadmap for controland elimination. PLoS Negl Trop Dis, 2008, 2(9): e300

doi: 10.1371/journal.pntd.0000300
Hotez P J, Fenwick A, Kjetland E F. Africa’s 32 cents solutionfor HIV/AIDS. PLoS Negl Trop Dis, 2009, 3(5): e430

doi: 10.1371/journal.pntd.0000430
Shao Y. AIDS epidemic at age 25 and control efforts in China. Retrovirology, 2006, 3: 87

doi: 10.1186/1742-4690-3-87
Newton C R. Interaction between Plasmodium falciparum and human immunodeficiencyvirus type 1 on the central nervous system of African children. J Neurovirol, 2005, 11(Suppl 3): 45―51

doi: 10.1080/13550280500511881
Clerici M, Giorgi J V, Chou C C, Gudeman V K, Zack J A, Gupta P, Ho H N, Nishanian P G, Berzofsky J A, Shearer G M. Cell-mediated immune response to human immunodeficiency virus (HIV)type 1 in seronegative homosexual men with recent sexual exposureto HIV-1. J Infect Dis, 1992, 165(6): 1012―1019
Barcellini W, Rizzardi G P, Borghi M O, Fain C, Lazzarin A, Meroni P L. TH1 and TH2 cytokine productionby peripheral blood mononuclear cells from HIV-infected patients. AIDS, 1994, 8(6): 757―762

doi: 10.1097/00002030-199406000-00006
Clerici M, Lucey D R, Berzofsky J A, Pinto L A, Wynn T A, Blatt S P, Dolan M J, Hendrix C W, Wolf S F, Shearer G M. Restoration of HIV-specific cell-mediated immune responses by interleukin-12in vitro. Science, 1993, 262(5140): 1721―1724
Graziosi C, Pantaleo G, Gantt K R, Fortin J P, Demarest J F, Cohen O J, Sékaly R P, Fauci A S. Lack of evidence for the dichotomy of TH1 and TH2 predominance inHIV-infected individuals. Science, 1994, 265(5169): 248―252

doi: 10.1126/science.8023143
Bentwich Z, Weisman Z, Moroz C, Bar-Yehuda S, Kalinkovich A. Immunedysregulation in Ethiopian immigrants in Israel: relevance to helminthinfections? Clin Exp Immunol, 1996, 103(2): 239―243

doi: 10.1046/j.1365-2249.1996.d01-612.x
Gopinath R, Ostrowski M, Justement S J, Fauci A S, Nutman T B. Filarial infections increase susceptibility to human immunodeficiencyvirus infection in peripheral blood mononuclear cells in vitro. J Infect Dis, 2000, 182(6): 1804―1808
Harms G, Feldmeier H. HIVinfection and tropical parasitic diseases- deleterious interactionsin both directions? Trop Med Int Health, 2002, 7(6): 479―488

doi: 10.1046/j.1365-3156.2002.00893.x
Karanja D M, Colley D G, Nahlen B L, Ouma J H, Secor W E. Studies onschistosomiasis in western Kenya: I. Evidence for immune-facilitatedexcretion of schistosome eggs from patients with Schistosoma mansoniand human immunodeficiency virus coinfections. Am J Trop Med Hyg, 1997, 56(5): 515―521
Tawill S A, Gallin M, Erttmann K D, Kipp W, Bamuhiiga J, Büttner D W. Impaired antibody responsesand loss of reactivity to Onchocerca volvulus antigens by HIV-seropositive onchocerciasis patients. Trans R Soc Trop Med Hyg, 1996, 90(1): 85―89

doi: 10.1016/S0035-9203(96)90488-5
Corbett E L, Steketee R W, ter Kuile F O, Latif A S, Kamali A, Hayes R J. HIV-1/AIDS and the controlof other infectious diseases in Africa. Lancet, 2002, 359(9324): 2177―2187

doi: 10.1016/S0140-6736(02)09095-5
Tian L G, Steinmann P, Chen J X, Chen S H, Zhou X N. HIV/AIDS,parasites and co-infections: publication patterns in China. Parasit Vec, 2009, 2: e31

doi: 10.1186/1756-3305-2-31
Tian L G, Zhou X N. Intestinalparasitic infections neglected in the HIV/AIDS patients. Zhong Guo Ji Sheng Chong Xue Yu Ji Sheng ChongBing Za Zhi, 2008, 26(5): 376―381 (in Chinese)
Borkow G, Teicher C, Bentwich Z. Helminth-HIV coinfection:should we deworm? PLoS Negl Trop Dis, 2007, 1(3): e160

doi: 10.1371/journal.pntd.0000160
Unicef U N U. WHO. Iron deficiency anemia:assessment, prevention, and control. A guide for programme managers. Geneva, WHO, 2001
Katz N, Chaves A, Pellegrino J. A simple device for quantitativestool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo, 1972, 14(6): 397―400
Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H. A modified agar plate methodfor detection of Strongyloides stercoralis. Am J Trop Med Hyg, 1991, 45(4): 518―521
Singer B H, Ryff C D. Neglectedtropical diseases, neglected data sources, and neglected issues. PLoS Negl Trop Dis, 2007, 1(2): e104

doi: 10.1371/journal.pntd.0000104
Xu L Q, Chen Y D, Sun F H. A national survey on current status ofthe important parasitic diseases in human population. Zhong Guo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, 2005, 23(5): 332―340 (in Chinese)
Cheng H, Qian X, Cao G H, Chen C K, Gao Y N, Jiang Q W. Study on thc seropositive prevalence of human immunodeficiencyvirus in a village residents living in rural region of central China. Zhong Hua Liu Xing Bing Xue Za Zhi, 2004, 25(4): 317―321 (in Chinese)
Xu L F, Wang J, Wang K X, Li C P. Cryptosporidium Infection among Students in Anhui Province. Zhong Guo Xue Xiao Wei Sheng, 2003, 24(4): 347―348 (in Chinese)
Wan G Q, Liu X, Wang L L, Liao F, Zhao C L, Fu B, Chen X X, Li G P, Zhao Z P, Zhen T M. Present condition and characteristicsof human intestinal parasites in Shandong Province. Zhong Guo Xue Xi Chong Bing Fang Zhi Za Zhi, 2006, 18(5): 381―383 (in Chinese)
Escobedo A A, Núñez F A. Prevalence of intestinal parasites in Cuban acquired immunodeficiencysyndrome (AIDS) patients. Acta Trop, 1999, 72(1): 125―130

doi: 10.1016/S0001-706X(98)00091-6
Li C P, Wang J. Epidemiologyinvestigation of Blastocystis hominis in Huainan areas. Di Si Jun Yi Da XueXue Bao, 2002, 23(16): 1480―1482 (in Chinese)
Tian C L, He D X, Wan X L. A clinical survey on Blastocystis hominis. YingYong Yu Fang Yi Xue, 2006, 12(6): 348―350 (in Chinese)
Steinmann P, Du Z W, Wang L B, Wang X Z, Jiang J Y, Li L H, Marti H, Zhou X N, Utzinger J. Extensivemultiparasitism in a village of Yunnan province, People’s Republicof China, revealed by a suite of diagnostic methods. Am J Trop Med Hyg, 2008, 78(5): 760―769
Su Z L, Su S L, Wu Z F, Miao H, Miao Y, Xie Q J, Zhang Q S. Survey epidemiologyof Blastocystis hominis infectionin Ganzhou. Zhong Guo Bing Yuan Sheng WuXue Za Zhi, 2008, 3(2): 142―143 (in Chinese)
Zhang H W, Yan Q Y, He L J, Su Y P, Li W, Xue C G, Wang D. Survey on asymptomtic Blastocystis hominis and its PCR identification. Yi Yao Lun Tan Za Zhi, 2006, 27(1): 32―36 (in Chinese)
Li L H, Zhang X P, Lv S, Zhang L, Yoshikawa H, Wu Z, Steinmann P, Utzinger J, Tong X M, Chen S H, Zhou X N. Cross-sectional surveys and subtype classification of human Blastocystis isolates from four epidemiologicalsettings in China. Parasitol Res, 2007, 102(1): 83―90

doi: 10.1007/s00436-007-0727-0
Li L H, Zhou X N, Du Z W, Wang X Z, Wang L B, Jiang J Y, Yoshikawa H, Steinmann P, Utzinger J, Wu Z, Chen J X, Chen S H, Zhang L. Molecular epidemiology ofhuman Blastocystis in a villagein Yunnan province, China. Parasitol Int, 2007, 56(4): 281―286

doi: 10.1016/j.parint.2007.06.001
Zhang X P, Li L H, Zhu Q, Fu Y H, Ma X J, Lv S, Hong G B, He Y Y, Wang Z Y, Ma X B. Investigation on the infectionof Blastocystis hominis in variouspopulations in Shanghai, China. Zhong GuoBing Yuan Sheng Wu Xue Za Zhi, 2008, 3(9): 693―710 (in Chinese)
Xu L F, Li C P, Zhang R B. Study on characteristic of Cryptosporidium infection among studentsin Anhui province, China. Zhong Guo JiSheng Chong Bing Fang Zhi Za Zhi, 2005, 18(4): 265―267 (in Chinese)
Zhu M S, Song M H. Survey on Cryptoporidium among students of middle schoolin Shiyan city. Zhong Guo Xue Xiao WeiSheng, 2007, 28(6): 549 (in Chinese)
Zhou H F, Yan J L, Li J Y. Current status of the important parasiticsiseases in Luwan district. Re Dai Yi XueZa Zhi, 2006, 6(1): 1203―1204 (in Chinese)
Wang H Y, Rong J Q, Wu G P. Investigation on cryptosporidiosis insome southern areas of Guizhou province. Re Dai Yi Xue Za Zhi, 2006, 6(6): 717―718 (in Chinese)
Zhang J X, Liu P Y, He D L, Wu X H. A survey on parasitic infection in Qumalai count, Qinghai province. Re Dai Bing Yu Ji Sheng Chong Xue, 2007, 5(2): 116 (in Chinese)
Tzipori S, Widmer G. Ahundred-year retrospective on cryptosporidiosis. Trends Parasitol, 2008, 24(4): 184―189

doi: 10.1016/
Tumwine J K, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, Akiyoshi D E, Tzipori S. Cryptosporidiosisand microsporidiosis in ugandan children with persistent diarrheawith and without concurrent infection with the human immunodeficiencyvirus. Am J Trop Med Hyg, 2005, 73(5): 921―925
Arikan S, Ergüven S, Akyön Y, Günalp A. Cryptosporidiosis in immunocompromised patients in aTurkish university hospital. Acta MicrobiolImmunol Hung, 1999, 46(1): 33―40

doi: 10.1556/AMicr.46.1999.1.4
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