Coinfection with Helminths and HIV-1 in East Asia

  • Katarina SteteEmail author
  • Xiao-Nong Zhou
  • Li-Guang Tian
  • Matthias C. Mueller
Part of the Neglected Tropical Diseases book series (NTD)


As geographic distributions of human immunodeficiency virus-1 (HIV-1) and helminth infections largely overlap in many regions of the world, including the East Asian region, HIV-1/helminth coinfection is a common finding. Both HIV-1 and helminth infections mutually interact on several levels, especially on the level of immunomodulation, which has potential effects on the risk of acquisition and the clinical course of the involved pathogens. In this chapter, we present the epidemiology of HIV-1/helminth coinfection in East Asia and summarize the current knowledge on mutual interaction and its effect on epidemiology, clinical course, and treatment of the respective pathogen.


HIV-1 Helminth infection Coinfection East Asia 


  1. Bentwich Z, Kalinkovich A, Weisman Z (1995) Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunol Today 16:187–191PubMedCrossRefPubMedCentralGoogle Scholar
  2. Borkow G, Bentwich Z (2004) Chronic immune activation associated with chronic helminthic and human immunodeficiency virus infections: role of hyporesponsiveness and anergy. Clin Microbiol Rev 17:1012–1030PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bretscher PA (2014) On the mechanism determining the TH1/TH2 phenotype of an immune response, and its pertinence to strategies for the prevention, and treatment, of certain infectious diseases. Scand J Immunol 79:361–376PubMedPubMedCentralCrossRefGoogle Scholar
  4. Brindley PJ, Sher A (1987) The chemotherapeutic effect of praziquantel against Schistosoma mansoni is dependent on host antibody response. J Immunol Baltim Md 1950 139:215–220Google Scholar
  5. Brooker S, Clements ACA, Bundy DAP (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62:221–261PubMedPubMedCentralCrossRefGoogle Scholar
  6. Brown M, Kizza M, Watera C, Quigley MA, Rowland S, Hughes P et al (2004) Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. J Infect Dis 190:1869–1879PubMedCrossRefPubMedCentralGoogle Scholar
  7. Brown M, Cartledge JD, Miller RF (2006) Dissemination of Strongyloides stercoralis as an immune restoration phenomenon in an HIV-1-infected man on antiretroviral therapy. Int J STD AIDS 17:560–561PubMedCrossRefPubMedCentralGoogle Scholar
  8. Card CM, McLaren PJ, Wachihi C, Kimani J, Plummer FA, Fowke KR (2009) Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4(+)CD25(+)FOXP3(+) regulatory T cells. J Infect Dis 199:1318–1322PubMedCrossRefPubMedCentralGoogle Scholar
  9. Centers for Disease Control, R.O.C. (Taiwan)—Annual Report (2015) [Internet]. Centers for Disease Control, R.O.C. (Taiwan). Verfügbar unter:
  10. Centers of Disease Control, R.O.C. (Taiwan), Statistics of HIV (2015) Statistics of HIV 08/31/2015 [Internet]. Verfügbar unter:
  11. Chenine A-L, Shai-Kobiler E, Steele LN, Ong H, Augostini P, Song R et al (2008) Acute Schistosoma mansoni infection increases susceptibility to systemic SHIV clade C infection in rhesus macaques after mucosal virus exposure. PLoS Negl Trop Dis 2:e265PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chermette R, Bussiéras J, Marionneau J, Boyer E, Roubin C, Prophette B et al (1995) Invasive cysticercosis due to Taenia crassiceps in an AIDS patient. Bull Acad Natl Méd 179:777–780; discussion 780–783Google Scholar
  13. Chevalier MF, Weiss L (2013) The split personality of regulatory T cells in HIV infection. Blood 121:29–37PubMedCrossRefPubMedCentralGoogle Scholar
  14. Clerici M, Shearer GM (1993) A TH1→TH2 switch is a critical step in the etiology of HIV infection. Immunol Today 14:107–111PubMedCrossRefPubMedCentralGoogle Scholar
  15. Coordinating Office of the National Survey on the Important Human Parasitic Diseases (2005) A national survey on current status of the important parasitic diseases in human population. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 23(Suppl 5):332–340Google Scholar
  16. Craib KJ, Meddings DR, Strathdee SA, Hogg RS, Montaner JS, O’Shaughnessy MV et al (1995) Rectal gonorrhoea as an independent risk factor for HIV infection in a cohort of homosexual men. Genitourin Med 71:150–154PubMedPubMedCentralGoogle Scholar
  17. Davies SJ, Grogan JL, Blank RB, Lim KC, Locksley RM, McKerrow JH (2001) Modulation of blood fluke development in the liver by hepatic CD4+ lymphocytes. Science 294:1358–1361PubMedCrossRefPubMedCentralGoogle Scholar
  18. Delobel P, Signate A, El Guedj M, Couppie P, Gueye M, Smadja D et al (2004) Unusual form of neurocysticercosis associated with HIV infection. Eur J Neurol 11:55–58PubMedCrossRefPubMedCentralGoogle Scholar
  19. Deschamps MM, Fitzgerald DW, Pape JW, Johnson WD (2000) HIV infection in Haiti: natural history and disease progression. AIDS 14:2515–2521PubMedCrossRefPubMedCentralGoogle Scholar
  20. Doenhoff MJ, Pearson S, Dunne DW, Bickle Q, Lucas S, Bain J et al (1981) Immunological control of hepatotoxicity and parasite egg excretion in Schistosoma mansoni infections: stage specificity of the reactivity of immune serum in T-cell deprived mice. Trans R Soc Trop Med Hyg 75:41–53PubMedCrossRefPubMedCentralGoogle Scholar
  21. Doenhoff MJ, Cioli D, Utzinger J (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis 21:659–667PubMedCrossRefPubMedCentralGoogle Scholar
  22. Domingues C-SB, Waldman EA (2014) Causes of death among people living with AIDS in the pre- and post-HAART Eras in the City of São Paulo, Brazil. PLoS One 9:e114661PubMedPubMedCentralCrossRefGoogle Scholar
  23. Douek DC, Picker LJ, Koup RA (2003) T cell dynamics in HIV-1 infection. Annu Rev Immunol 21:265–304PubMedCrossRefPubMedCentralGoogle Scholar
  24. Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H et al (2011) Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg 84:364–369PubMedPubMedCentralCrossRefGoogle Scholar
  25. Downs JA, van Dam GJ, Changalucha JM, Corstjens PLAM, Peck RN, de Dood CJ et al (2012) Association of schistosomiasis and HIV infection in Tanzania. Am J Trop Med Hyg 87:868–873PubMedPubMedCentralCrossRefGoogle Scholar
  26. Dunne DW, Hassounah O, Musallam R, Lucas S, Pepys MB, Baltz M et al (1983) Mechanisms of Schistosoma mansoni egg excretion: parasitological observations in immunosuppressed mice reconstituted with immune serum. Parasite Immunol 5:47–60PubMedCrossRefPubMedCentralGoogle Scholar
  27. Efraim L, Peck RN, Kalluvya SE, Kabangila R, Mazigo HD, Mpondo B et al (2013) Schistosomiasis and impaired response to antiretroviral therapy among HIV-infected patients in Tanzania. J Acquir Immune Defic Syndr 1999 62:e153–e156CrossRefGoogle Scholar
  28. Elliott AM, Mawa PA, Joseph S, Namujju PB, Kizza M, Nakiyingi JS et al (2003) Associations between helminth infection and CD4+ T cell count, viral load and cytokine responses in HIV-1-infected Ugandan adults. Trans R Soc Trop Med Hyg 97:103–108PubMedCrossRefPubMedCentralGoogle Scholar
  29. Fang G, Burger H, Grimson R, Tropper P, Nachman S, Mayers D et al (1995) Maternal plasma human immunodeficiency virus type 1 RNA level: a determinant and projected threshold for mother-to-child transmission. Proc Natl Acad Sci USA 92:12100–12104PubMedCrossRefPubMedCentralGoogle Scholar
  30. Feitosa G, Bandeira AC, Sampaio DP, Badaró R, Brites C (2001) High prevalence of giardiasis and stronglyloidiasis among HIV-infected patients in Bahia, Brazil. Braz J Infect Dis 5:339–344Google Scholar
  31. Fischer P, Kipp W, Kabwa P, Buttner DW (1995) Onchocerciasis and human immunodeficiency virus in western Uganda: prevalences and treatment with ivermectin. Am J Trop Med Hyg 53:171–178PubMedPubMedCentralGoogle Scholar
  32. Flammer Anikpeh Y, Grimm F, Lindenblatt N, Zinkernagel A (2014) It isn’t always caviar. BMJ Case Rep 2014:bcr2013200078Google Scholar
  33. Fontanet AL, Woldemichael T, Sahlu T, van Dam GJ, Messele T, Rinke de Wit T et al (2000) Epidemiology of HIV and Schistosoma mansoni infections among sugar-estate residents in Ethiopia. Ann Trop Med Parasitol 94:145–155PubMedCrossRefPubMedCentralGoogle Scholar
  34. François A, Favennec L, Cambon-Michot C, Gueit I, Biga N, Tron F et al (1998) Taenia crassiceps invasive cysticercosis: a new human pathogen in acquired immunodeficiency syndrome? Am J Surg Pathol 22:488–492PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gallagher M, Malhotra I, Mungai PL, Wamachi AN, Kioko JM, Ouma JH et al (2005) The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS 19:1849–1855PubMedCrossRefPubMedCentralGoogle Scholar
  36. Glynn JR, Sonnenberg P, Nelson G, Bester A, Shearer S, Murray J (2007) Survival from HIV-1 seroconversion in Southern Africa: a retrospective cohort study in nearly 2000 gold-miners over 10 years of follow-up. AIDS 21:625–632PubMedCrossRefPubMedCentralGoogle Scholar
  37. Gopinath R, Ostrowski M, Justement SJ, Fauci AS, Nutman TB (2000) Filarial infections increase susceptibility to human immunodeficiency virus infection in peripheral blood mononuclear cells in vitro. J Infect Dis 182:1804–1808PubMedCrossRefPubMedCentralGoogle Scholar
  38. Greene BM, Fanning MM, Ellner JJ (1983) Non-specific suppression of antigen-induced lymphocyte blastogenesis in Onchocerca volvulus infection in man. Clin Exp Immunol 52:259–265PubMedPubMedCentralGoogle Scholar
  39. Hira SK, Shroff HJ, Lanjewar DN, Dholkia YN, Bhatia VP, Dupont HL (2003) The natural history of human immunodeficiency virus infection among adults in Mumbai. Natl Med J India 16:126–131PubMedGoogle Scholar
  40. Hotez PJ, Ehrenberg JP (2010) Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region. Adv Parasitol 72:31–53PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118:1311–1321PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, van Dam GJ, Erikstrup C et al (2005) Schistosomiasis and HIV-1 infection in rural Zimbabwe: implications of coinfection for excretion of eggs. J Infect Dis 191:1311–1320PubMedCrossRefGoogle Scholar
  43. Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE (1997) Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 56:515–521PubMedCrossRefGoogle Scholar
  44. Karanja DM, Boyer AE, Strand M, Colley DG, Nahlen BL, Ouma JH et al (1998) Studies on schistosomiasis in western Kenya: II. Efficacy of praziquantel for treatment of schistosomiasis in persons coinfected with human immunodeficiency virus-1. Am J Trop Med Hyg 59:307–311PubMedCrossRefGoogle Scholar
  45. Karp CL, Auwaerter PG (2007) Coinfection with HIV and tropical infectious diseases. II. Helminthic, fungal, bacterial, and viral pathogens. Clin Infect Dis 45:1214–1220Google Scholar
  46. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kim T-S, Cho S-H, Huh S, Kong Y, Sohn W-M, Hwang S-S (2009) A nationwide survey on the prevalence of intestinal parasitic infections in the Republic of Korea, 2004. Korean J Parasitol 47:37PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L et al (2006) Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 20:593–600PubMedCrossRefGoogle Scholar
  49. Kleppa E, Ramsuran V, Zulu S, Karlsen GH, Bere A, Passmore J-AS et al (2014) Effect of female genital schistosomiasis and anti-schistosomal treatment on monocytes, CD4+ T-cells and CCR5 expression in the female genital tract. PLoS One 9:e98593PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kleppa E, Klinge KF, Galaphaththi-Arachchige HN, Holmen SD, Lillebø K, Onsrud M et al (2015) Schistosoma haematobium infection and CD4+ T-cell levels: a cross-sectional study of young South African women. PLoS One 10:e0119326PubMedPubMedCentralCrossRefGoogle Scholar
  51. Klinker H, Tintelnot K, Joeres R, Müller J, Gross U, Schmidt-Rotte H et al (1992) Taenia crassiceps infection in AIDS. Dtsch Med Wochenschr 1946 117:133–138CrossRefGoogle Scholar
  52. Kroidl I, Saathoff E, Maganga L, Makunde WH, Hoerauf A, Geldmacher C et al (2016) Effect of Wuchereria bancrofti infection on HIV incidence in southwest Tanzania: a prospective cohort study. Lancet 388:1912–1920PubMedCrossRefPubMedCentralGoogle Scholar
  53. Kullberg MC, Pearce EJ, Hieny SE, Sher A, Berzofsky JA (1992) Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J Immunol 1950 148:3264–3270Google Scholar
  54. Lanzafame M, Faggian F, Lattuada E, Antolini D, Vento S (2005) Strongyloidiasis in an HIV-1-infected patient after highly active antiretroviral therapy-induced immune restoration. J Infect Dis 191:1027PubMedCrossRefGoogle Scholar
  55. Lawn SD (2004) AIDS in Africa: the impact of coinfections on the pathogenesis of HIV-1 infection. J Infect 48:1–12PubMedCrossRefGoogle Scholar
  56. Lawn SD, Butera ST, Folks TM (2001) Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin Microbiol Rev 14:753–777PubMedPubMedCentralCrossRefGoogle Scholar
  57. Li Y, Ling W, Xu H, Wang M, Wu C (2012) The activation and dynamics of cytokine expression by CD4+ T cells and AIDS progression in HIV-1-infected Chinese individuals. Microb Pathog 53:189–197PubMedCrossRefGoogle Scholar
  58. Lun Z-R, Gasser RB, Lai D-H, Li A-X, Zhu X-Q, Yu X-B et al (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 5:31–41PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lustigman S, Prichard RK, Gazzinelli A, Grant WN, Boatin BA, McCarthy JS, Basanez MG (2012) A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Negl Trop Dis 6:e1582PubMedPubMedCentralCrossRefGoogle Scholar
  60. Maizels RM, Yazdanbakhsh M (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3:733–744PubMedCrossRefGoogle Scholar
  61. Malhotra I, Ouma J, Wamachi A, Kioko J, Mungai P, Omollo A et al (1997) In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J Clin Invest 99:1759–1766PubMedPubMedCentralCrossRefGoogle Scholar
  62. Mazigo HD, Dunne DW, Wilson S, Kinung’hi SM, Pinot de Moira A, Jones FM et al (2014) Co-infection with Schistosoma mansoni and human immunodeficiency virus-1 (HIV-1) among residents of fishing villages of north-western Tanzania. Parasit Vectors 7:587Google Scholar
  63. Means AR, Burns P, Sinclair D, Walson JL (2016) Antihelminthics in helminth-endemic areas: effects on HIV disease progression. Cochrane Database of Syst Rev [Internet].
  64. Mkhize-Kwitshana ZL, Taylor M, Jooste P, Mabaso ML, Walzl G (2011) The influence of different helminth infection phenotypes on immune responses against HIV in co-infected adults in South Africa. BMC Infect Dis 11:273PubMedPubMedCentralCrossRefGoogle Scholar
  65. Modjarrad K, Vermund SH (2010) Effect of treating co-infections on HIV-1 viral load: a systematic review. Lancet Infect Dis 10:455–463PubMedPubMedCentralCrossRefGoogle Scholar
  66. Morgan D, Malamba SS, Maude GH, Okongo MJ, Wagner HU, Mulder DW et al (1997) An HIV-1 natural history cohort and survival times in rural Uganda. AIDS 11:633–640PubMedCrossRefGoogle Scholar
  67. Muok EMO, Simiyu EW, Ochola EA, Ng’ang’a ZW, Secor WE, Karanja DMS et al (2013) Association between CD4+ T-lymphocyte counts and fecal excretion of Schistosoma mansoni eggs in patients coinfected with S. mansoni and human immunodeficiency virus before and after initiation of antiretroviral therapy. Am J Trop Med Hyg 89:42–45PubMedPubMedCentralCrossRefGoogle Scholar
  68. Mwanakasale V, Vounatsou P, Sukwa TY, Ziba M, Ernest A, Tanner M (2003) Interactions between Schistosoma haematobium and human immunodeficiency virus type 1: the effects of coinfection on treatment outcomes in rural Zambia. Am J Trop Med Hyg 69:420–428PubMedCrossRefGoogle Scholar
  69. Nielsen NO, Simonsen PE, Magnussen P, Magesa S, Friis H (2006) Cross-sectional relationship between HIV, lymphatic filariasis and other parasitic infections in adults in coastal northeastern Tanzania. Trans R Soc Trop Med Hyg 100:543–550PubMedCrossRefPubMedCentralGoogle Scholar
  70. Nielsen NO, Friis H, Magnussen P, Krarup H, Magesa S, Simonsen PE (2007) Co-infection with subclinical HIV and Wuchereria bancrofti, and the role of malaria and hookworms, in adult Tanzanians: infection intensities, CD4/CD8 counts and cytokine responses. Trans R Soc Trop Med Hyg 101:602–612PubMedCrossRefPubMedCentralGoogle Scholar
  71. Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P et al (2009) Strongyloidiasis—the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg 103:967–972PubMedCrossRefPubMedCentralGoogle Scholar
  72. Paboriboune P, Phoumindr N, Borel E, Sourinphoumy K, Phaxayaseng S, Luangkhot E et al (2014) Intestinal parasitic infections in HIV-infected patients, Lao People’s Democratic Republic. PLoS One 9:e91452PubMedPubMedCentralCrossRefGoogle Scholar
  73. Panic G, Duthaler U, Speich B, Keiser J (2014) Repurposing drugs for the treatment and control of helminth infections. Int J Parasitol Drugs Drug Resist 4:185–200PubMedPubMedCentralCrossRefGoogle Scholar
  74. Piot P, Quinn TC (2013) Response to the AIDS pandemic—a global health model. N Engl J Med 368:2210–2218PubMedPubMedCentralCrossRefGoogle Scholar
  75. Prepared by Special Preventive Programme: FACTSHEET on HIV/AIDS Situation in Hong Kong (2014) [Internet]. Verfügbar unter:
  76. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F et al (2000) Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 342:921–929PubMedCrossRefPubMedCentralGoogle Scholar
  77. Ran B, Shao Y, Guo Y, Yimiti Y, Aji T, Jia J et al (2015) Surgical treatment of hepatic cystic echinococcosis in patients co-infected with HIV/AIDS. J Helminthol 90:1–4Google Scholar
  78. Report to UNAIDS—HIV/AIDS Trends in Japan (2015) [Internet]. Verfügbar unter:
  79. Sabah AA, Fletcher C, Webbe G, Doenhoff MJ (1985) Schistosoma mansoni: reduced efficacy of chemotherapy in infected T-cell-deprived mice. Exp Parasitol 60:348–354PubMedCrossRefPubMedCentralGoogle Scholar
  80. Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, Gottstein B (1997) Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 130:320–323PubMedCrossRefPubMedCentralGoogle Scholar
  81. Sangaré LR, Herrin BR, Herrin BR, John-Stewart G, Walson JL (2011) Species-specific treatment effects of helminth/HIV-1 co-infection: a systematic review and meta-analysis. Parasitology 138:1546–1558PubMedPubMedCentralCrossRefGoogle Scholar
  82. Sanya RE, Muhangi L, Nampijja M, Nannozi V, Nakawungu PK, Abayo E et al (2015) Schistosoma mansoni and HIV infection in a Ugandan population with high HIV and helminth prevalence. Trop Med Int Health 20:1201–1208PubMedPubMedCentralCrossRefGoogle Scholar
  83. Sauce D, Larsen M, Fastenackels S, Pauchard M, Ait-Mohand H, Schneider L et al (2011) HIV disease progression despite suppression of viral replication is associated with exhaustion of lymphopoiesis. Blood 117:5142–5151PubMedPubMedCentralCrossRefGoogle Scholar
  84. Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H et al (2013) Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis 7:e2288PubMedPubMedCentralCrossRefGoogle Scholar
  85. Schmiedel Y, Mombo-Ngoma G, Labuda LA, Janse JJ, de Gier B, Adegnika AA et al (2015) An CD4+CD25hiFOXP3+ regulatory T cells and cytokine responses in human schistosomiasis before and after treatment with Praziquantel. PLoS Negl Trop Dis 9:e0003995PubMedPubMedCentralCrossRefGoogle Scholar
  86. Serpa JA, Moran A, Goodman JC, Giordano TP, White AC (2007) Neurocysticercosis in the HIV era: a case report and review of the literature. Am J Trop Med Hyg 77:113–117PubMedCrossRefPubMedCentralGoogle Scholar
  87. Shapira-Nahor O, Kalinkovich A, Weisman Z, Greenberg Z, Nahmias J, Shapiro M et al (1998) Increased susceptibility to HIV-1 infection of peripheral blood mononuclear cells from chronically immune-activated individuals. AIDS 12:1731–1733PubMedPubMedCentralGoogle Scholar
  88. Siddappa NB, Hemashettar G, Shanmuganathan V, Semenya AA, Sweeney ED, Paul KS et al (2011) Schistosoma mansoni enhances host susceptibility to mucosal but not intravenous challenge by R5 Clade C SHIV. PLoS Negl Trop Dis 5:e1270PubMedPubMedCentralCrossRefGoogle Scholar
  89. Steinmann P, Zhou X-N, Du Z-W, Jiang J-Y, Wang L-B, Wang X-Z et al (2007) Occurrence of Strongyloides stercoralis in Yunnan Province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis 1:e75PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sudomo M, Chayabejara S, Duong S, Hernandez L, Wu W-P, Bergquist R (2010) Elimination of lymphatic filariasis in Southeast Asia. Adv Parasitol 72:205–233CrossRefGoogle Scholar
  91. Suguimoto SP, Techasrivichien T, Musumari PM, El-saaidi C, Lukhele BW, Ono-Kihara M et al (2014) Changing patterns of HIV epidemic in 30 years in East Asia. Curr HIV/AIDS Rep 11:134–145PubMedCrossRefPubMedCentralGoogle Scholar
  92. Tafatatha T, Taegtmeyer M, Ngwira B, Phiri A, Kondowe M, Piston W et al (2015) Human immunodeficiency virus, antiretroviral therapy and markers of lymphatic filariasis infection: a cross-sectional study in rural Northern Malawi. PLoS Negl Trop Dis 9:e0003825PubMedPubMedCentralCrossRefGoogle Scholar
  93. Tawill SA, Gallin M, Erttmann KD, Kipp W, Bamuhiiga J, Büttner DW (1996) Impaired antibody responses and loss of reactivity to Onchocerca volvulus antigens by HIV-seropositive onchocerciasis patients. Trans R Soc Trop Med Hyg 90:85–89PubMedCrossRefPubMedCentralGoogle Scholar
  94. Tian L-G, Steinmann P, Chen J-X, Chen S-H, Zhou X-N (2009) HIV/AIDS, parasites and co-infections: publication patterns in China. Parasit Vectors 2:31PubMedPubMedCentralCrossRefGoogle Scholar
  95. Tian L-G, Chen J-X, Wang T-P, Cheng G-J, Steinmann P, Wang F-F et al (2012) Co-infection of HIV and intestinal parasites in rural area of China. Parasit Vectors 5:36PubMedPubMedCentralCrossRefGoogle Scholar
  96. Torgerson PR, Keller K, Magnotta M, Ragland N (2010) The global burden of alveolar echinococcosis. PLoS Negl Trop Dis 4:e722PubMedPubMedCentralCrossRefGoogle Scholar
  97. UNAIDS (2013) FactsheetGoogle Scholar
  98. UNAIDS (2015a) China AIDS Response Progress Report [Internet]. Available at:
  99. UNAIDS (2015b) HIV/AIDS Control in the Republic of Korea 2011 [Internet]. Available at:
  100. Viney ME, Brown M, Omoding NE, Bailey JW, Gardner MP, Roberts E et al (2004) Why does HIV infection not lead to disseminated strongyloidiasis? J Infect Dis 190:2175–2180PubMedCrossRefPubMedCentralGoogle Scholar
  101. Walson JL, Stewart BT, Sangaré L, Mbogo LW, Otieno PA, Piper BKS et al (2010) Prevalence and correlates of helminth co-infection in Kenyan HIV-1 infected adults. PLoS Negl Trop Dis 4:e644PubMedPubMedCentralCrossRefGoogle Scholar
  102. Wammes LJ, Mpairwe H, Elliott AM, Yazdanbakhsh M (2014) Helminth therapy or elimination: epidemiological, immunological, and clinical considerations. Lancet Infect Dis 14:1150–1162PubMedCrossRefPubMedCentralGoogle Scholar
  103. Webb EL, Mawa PA, Ndibazza J, Kizito D, Namatovu A, Kyosiimire-Lugemwa J et al (2011) Effect of single-dose anthelmintic treatment during pregnancy on an infant’s response to immunisation and on susceptibility to infectious diseases in infancy: a randomised, double-blind, placebo-controlled trial. Lancet 377:52–62PubMedPubMedCentralCrossRefGoogle Scholar
  104. WHO (2009) Report of an informal working group on urogenital schistosomiasis and HIV transmission. Geneva: World Health OrganizationGoogle Scholar
  105. Wiwanitkit V (2001) Intestinal parasitic infections in Thai HIV-infected patients with different immunity status. BMC Gastroenterol 1:3PubMedPubMedCentralCrossRefGoogle Scholar
  106. World Health Organization, Savioli L, Daumerie D, Herausgeber (2013) Sustaining the drive to overcome the global impact of neglected tropical diseases: second WHO report on neglected tropical diseases. World Health Organization, GenevaGoogle Scholar
  107. Yang G-J, Liu L, Zhu H-R, Griffiths SM, Tanner M, Bergquist R et al (2014) China’s sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis 14:881–892PubMedCrossRefPubMedCentralGoogle Scholar
  108. Zanussi S, Simonelli C, D’Andrea M, Caffau C, Clerici M, Tirelli U et al (1996) CD8+ lymphocyte phenotype and cytokine production in long-term non-progressor and in progressor patients with HIV-1 infection. Clin Exp Immunol 105:220–224PubMedPubMedCentralCrossRefGoogle Scholar
  109. Zhang L, Chow EPF, Jing J, Zhuang X, Li X, He M et al (2013) HIV prevalence in China: integration of surveillance data and a systematic review. Lancet Infect Dis 13:955–963PubMedCrossRefPubMedCentralGoogle Scholar
  110. Zheng Q, Vanderslott S, Jiang B, Xu L-L, Liu C-S, Huo L-L et al (2013) Research gaps for three main tropical diseases in the People’s Republic of China. Infect Dis Poverty 2:15PubMedPubMedCentralCrossRefGoogle Scholar
  111. Zhou X-N, Bergquist R, Leonardo L, Yang G-J, Yang K, Sudomo M et al (2010) Schistosomiasis japonica control and research needs. Adv Parasitol 72:145–178PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Katarina Stete
    • 1
    Email author
  • Xiao-Nong Zhou
    • 2
  • Li-Guang Tian
    • 2
  • Matthias C. Mueller
    • 1
  1. 1.Division of Infectious Diseases, Department of Medicine II, University Medical Center Freiburg, Faculty of MedicineUniversity of FreiburgFreiburgGermany
  2. 2.National Institute of Parasitic Diseases, Chinese Center for Disease Control and PreventionShanghaiPeople’s Republic of China

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