CC BY-NC-ND 4.0 · Ann Natl Acad Med Sci 2021; 57(02): 081-093
DOI: 10.1055/s-0041-1726149
Review Article

Evolving Patterns of Cryptosporidiosis: Issues and Implications in the Context of Public Health in India

Bijay Ranjan Mirdha
1   Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India
› Author Affiliations

Abstract

Cryptosporidiosis is one of the major causes of diarrhea in immune-compromised individuals and children besides causing sporadic water-borne, food-borne, and zoonotic outbreaks. In 2016, Cryptosporidium species infection was the fifth leading cause of diarrhea and acute infection causing more than 4.2 million disability-adjusted life years lost besides a decrease in childhood growth. Human cryptosporidiosis is primarily caused by two species/genotype: Cryptosporidium hominis (anthroponotic) and Cryptosporidium parvum (zoonotic) besides other six rare species/genotypes. Transmission intensity, genetic diversity, and occurrence of genetic recombination have shaped the genus Cryptosporidium population structures into palmitic, clonal, and epidemic. Genetic recombination is more in C. parvum compared with C. hominis. Furthermore, parasite–host co-evolution, host adaptation, and geographic segregation have led to the formation of “subtype- families.” Host-adapted subtype-families have distinct geographical distribution and host preferences. Genetic exchanges between subtypes played an important role throughout the evolution of the genus leading to “adaptation introgression” that led to emergence of virulent and hyper-transmissible subtypes. The population structure of C. hominis in India appears to be more complex where both transmission intensity and genetic diversity are much higher. Further, study based on “molecular strain surveillance” has resulted newer insights into the epidemiology and transmission of cryptosporidiosis in India. The identification at the species and genotype levels is essential for the assessment of infection sources in humans and the public health potential of the parasite at large. The results of the study over three decades on cryptosporidiosis in India, in the absence of a national surveillance data, were analyzed highlighting current situation on epidemiology, genetic diversity, and distribution particularly among vulnerable population. Despite creditable efforts, there are still many areas need to be explored; therefore, the intent of this article is to facilitate future research approaches for mitigating the burden associated with this disease.

Notes

*Recipient of Dr. Pran Nath Chhuttani oration.




Publication History

Article published online:
03 May 2021

© 2021. National Academy of Medical Sciences (India). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).

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  • References

  • 1 Tyzzer EE. A sporozoan found in the peptic glands of the common mouse. Proc Soc Exp Biol Med 1907; 5: 12-13
  • 2 Meisel JL, Perera DR, Meligro C, Rubin CE. Overwhelming watery diarrhea associated with a cryptosporidium in an immunosuppressed patient. Gastroenterology 1976; 70 (06) 1156-1160
  • 3 Nime FA, Burek JD, Page DL, Holscher MA, Yardley JH. Acute enterocolitis in a human being infected with the protozoan Cryptosporidium. Gastroenterology 1976; 70 (04) 592-598
  • 4 Parasites - Cryptosporidium (also known as “Crypto”). Available at: https://www.cdc.gov/parasites/crypto/illness.html
  • 5 Gentile G, Venditti M, Micozzi A. et al. Cryptosporidiosis in patients with hematologic malignancies. Rev Infect Dis 1991; 13 (05) 842-846
  • 6 Blanshard C, Jackson AM, Shanson DC, Francis N, Gazzard BG. Cryptosporidiosis in HIV-seropositive patients. Q J Med 1992; 85 (307-308) 813-823
  • 7 Farthing MJ. Clinical aspects of human cryptosporidiosis. Contrib Microbiol 2000; 6: 50-74
  • 8 Tumwine JK, Kekitiinwa A, Nabukeera N. et al. Cryptosporidium parvum in children with diarrhea in Mulago Hospital, Kampala, Uganda. Am J Trop Med Hyg 2003; 68 (06) 710-715
  • 9 Pandak N, Zeljka K, Cvitkovic A. A family outbreak of cryptosporidiosis: Probable nosocomial infection and person-to-person transmission. Wien Klin Wochenschr 2006; 118 (15/16) 485-487
  • 10 Xiao L, Feng Y. Zoonotic cryptosporidiosis. FEMS Immunol Med Microbiol 2008; 52 (03) 309-323
  • 11 Ryan U, Fayer R, Xiao L. Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology 2014; 141 (13) 1667-1685
  • 12 Robertson LJ, Gjerde BK. Cryptosporidium oocysts: challenging adversaries. ? Trends Parasitol 2007; 23 (08) 344-347
  • 13 Pereira SJ, Ramirez NE, Xiao L, Ward LA. Pathogenesis of human and bovine Cryptosporidium parvum in gnotobiotic pigs. J Infect Dis 2002; 186 (05) 715-718
  • 14 Okhuysen PC, Chappell CL, Crabb JH, Sterling CR, DuPont HL. Virulence of three distinct Cryptosporidium parvum isolates for healthy adults. J Infect Dis 1999; 180 (04) 1275-1281
  • 15 O’Donoghue PJ. Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 1995; 25 (02) 139-195
  • 16 Widmer G, Carmena D, Kváč M. et al. Update on Cryptosporidium spp.: highlights from the Seventh International Giardia and Cryptosporidium Conference. Parasite 2020; 27: 14
  • 17 Cama VA, Ross JM, Crawford S. et al. Differences in clinical manifestations among Cryptosporidium species and subtypes in HIV-infected persons. J Infect Dis 2007; 196 (05) 684-691
  • 18 Ajjampur SS, Sarkar R, Sankaran P. et al. Symptomatic and asymptomatic Cryptosporidium infections in children in a semi-urban slum community in southern India. Am J Trop Med Hyg 2010; 83 (05) 1110-1115
  • 19 Coutinho BP, Oriá RB, Vieira CM. et al. Cryptosporidium infection causes undernutrition and, conversely, weanling undernutrition intensifies infection. J Parasitol 2008; 94 (06) 1225-1232
  • 20 Chalmers RM, Davies AP. Minireview: clinical cryptosporidiosis. Exp Parasitol 2010; 124 (01) 138-146
  • 21 Clark DP. New insights into human cryptosporidiosis. Clin Microbiol Rev 1999; 12 (04) 554-563
  • 22 Mathan MM, Venkatesan S, George R, Mathew M, Mathan VI. Cryptosporidium and diarrhoea in southern Indian children. Lancet 1985; 2 (8465) 1172-1175
  • 23 Fayer R. Cryptosporidium: a water-borne zoonotic parasite. Vet Parasitol 2004; 126 (1-2) 37-56
  • 24 Areeshi M, Dove W, Papaventsis D. et al. Cryptosporidium species causing acute diarrhoea in children in Antananarivo, Madagascar. Ann Trop Med Parasitol 2008; 102 (04) 309-315
  • 25 Yoder JS, Wallace RM, Collier SA, Beach MJ, Hlavsa MC. Centers for Disease Control and Prevention (CDC). Cryptosporidiosis surveillance–United States, 2009-2010. MMWR Surveill Summ 2012; 61 (05) 1-12
  • 26 Health Protection Agency. Available at:www.hpa.org.uk.
  • 27 Muthusamy D, Rao SS, Ramani S. et al. Multilocus genotyping of Cryptosporidium sp. isolates from human immunodeficiency virus-infected individuals in South India. J Clin Microbiol 2006; 44 (02) 632-634
  • 28 Rao Ajjampur SS, Asirvatham JR, Muthusamy D. et al. Clinical features & risk factors associated with cryptosporidiosis in HIV infected adults in India. Indian J Med Res 2007; 126 (06) 553-557
  • 29 Hijjawi N, Ng J, Yang R, Atoum MF, Ryan U. Identification of rare and novel Cryptosporidium GP60 subtypes in human isolates from Jordan. Exp Parasitol 2010; 125 (02) 161-164
  • 30 Meinhardt PL, Casemore DP, Miller KB. Epidemiologic aspects of human cryptosporidiosis and the role of waterborne transmission. Epidemiol Rev 1996; 18 (02) 118-136
  • 31 Jagai JS, Castronovo DA, Monchak J, Naumova EN. Seasonality of cryptosporidiosis: a meta-analysis approach. Environ Res 2009; 109 (04) 465-478
  • 32 Nath G, Choudhury A, Shukla BN, Singh TB, Reddy DCS. Significance of Cryptosporidium in acute diarrhoea in North-Eastern India. J Med Microbiol 1999; 48 (06) 523-526
  • 33 Ajjampur SS, Sankaran P, Kang G. Cryptosporidium species in HIV-infected individuals in India: an overview. Natl Med J India 2008; 21 (04) 178-184
  • 34 Kulkarni SV, Kairon R, Sane SS. et al. Opportunistic parasitic infections in HIV/AIDS patients presenting with diarrhoea by the level of immunesuppression. Indian J Med Res 2009; 130 (01) 63-66
  • 35 Vignesh R, Balakrishnan P, Shankar EM. et al. High proportion of isosporiasis among HIV-infected patients with diarrhea in southern India. Am J Trop Med Hyg 2007; 77 (05) 823-824
  • 36 Masarat S, Ahmad F, Chisti M, Hamid S, Sofi BA. Prevalence of Cryptosporidium species among HIV positive asymptomatic and symptomatic immigrant population in Kashmir, India. Iran J Microbiol 2012; 4 (01) 35-39
  • 37 Patel SD, Kinariwala DM, Javadekar TB. Clinico-microbiological study of opportunistic infection in HIV seropositive patients. Indian J Sex Transm Dis AIDS 2011; 32 (02) 90-93
  • 38 Gupta S, Narang S, Nunavath V, Singh S. Chronic diarrhoea in HIV patients: prevalence of coccidian parasites. Indian J Med Microbiol 2008; 26 (02) 172-175
  • 39 Gautam H, Bhalla P, Saini S. et al. Epidemiology of opportunistic infections and its correlation with CD4 T-lymphocyte counts and plasma viral load among HIV-positive patients at a tertiary care hospital in India. J Int Assoc Physicians AIDS Care (Chic) 2009; 8 (06) 333-337
  • 40 Ramakrishnan K, Shenbagarathai R, Uma A, Kavitha K, Rajendran R, Thirumalaikolundusubramanian P. Prevalence of intestinal parasitic infestation in HIV/AIDS patients with diarrhea in Madurai City, South India. Jpn J Infect Dis 2007; 60 (04) 209-210
  • 41 Deorukhkar S, Katiyar R, Saini S. et al. The prevalence of intestinal parasitic infections in HIV infected patients in a rural tertiary care hospital of Western Maharashtra. (A 5 year study). J Clin Diagn Res 2011; 5: 210-212
  • 42 Tuli L, Gulati AK, Sundar S, Mohapatra TM. Correlation between CD4 counts of HIV patients and enteric protozoan in different seasons - an experience of a tertiary care hospital in Varanasi (India). BMC Gastroenterol 2008; 8: 36
  • 43 Anand L, Brajachand NG, Dhanachand CH. Cryptosporidiosis in HIV infection. J Commun Dis 1996; 28 (04) 241-244
  • 44 Sharma P, Sharma A, Sehgal R, Malla N, Khurana S. Genetic diversity of Cryptosporidium isolates from patients in North India. Int J Infect Dis 2013; 17 (08) e601-e605
  • 45 Khalil S, Mirdha BR, Paul J, Panda A, Singh Y. Molecular detection and identification of Cryptosporidium viatorum in a human immunodeficiency virus-seropositive patient. J Glob Infect Dis 2018; 10 (01) 28-29
  • 46 Raccurt CP, Brasseur P, Verdier RI. et al. [Human cryptosporidiosis and Cryptosporidium spp. in Haiti]. Trop Med Int Health 2006; 11 (06) 929-934
  • 47 Cama VA, Bern C, Roberts J. et al. Cryptosporidium species and subtypes and clinical manifestations in children, Peru. Emerg Infect Dis 2008; 14 (10) 1567-1574
  • 48 Swathirajan CR, Vignesh R, Pradeep A, Solomon SS, Solomon S, Balakrishnan P. Occurrence of enteric parasitic infections among HIV-infected individuals and its relation to CD4 T-cell counts with a special emphasis on coccidian parasites at a tertiary care centre in South India. Indian J Med Microbiol 2017; 35 (01) 37-40
  • 49 Uppal B, Singh O, Chadha S, Jha AK. A comparison of nested PCR assay with conventional techniques for diagnosis of intestinal cryptosporidiosis in AIDS cases from northern India. J Parasitol Res 2014; 2014: 706105
  • 50 Chen XM, LaRusso NF. Cryptosporidiosis and the pathogenesis of AIDS-cholangiopathy. Semin Liver Dis 2002; 22 (03) 277-289
  • 51 Babiker A, Darbyshire J, Pezzotti P. et al. CASCADE Collaboration. Changes over calendar time in the risk of specific first AIDS-defining events following HIV seroconversion, adjusting for competing risks. Int J Epidemiol 2002; 31 (05) 951-958
  • 52 Soave R, Ma P. Cryptosporidiosis. Traveler’s diarrhea in two families. Arch Intern Med 1985; 145 (01) 70-72
  • 53 Das P, Pal S, Dutta D, Bhattacharya MK, Pal SC. Cryptosporidiosis in Bengali children with acute diarrhoea. Trans R Soc Trop Med Hyg 1987; 81 (02) 241
  • 54 Palit A, Sur D, Mitra KDhar, Saha MR. Asymptomatic cryptosporiosis in a periurban slum setting in Kolkata, India–a pilot study. Jpn J Infect Dis 2005; 58: 110-111
  • 55 Mall AN, Sehagal R, Ganguly NK, Mahajan RC. Cryptosporidiosis in children in Chandigarh. Ind. J Med Res 1987; 86: 722-725
  • 56 Sen D, Sha MR, Nair GB. et al. Etiological spectrum of acute diarrhoea in hospitalised patients in Calcutta. Ind J Med Res; 1985; 286-291
  • 57 Pherwani AV, Bhave SY, Bijm AM, Desai AG. Prevalence of cryptosporidium in children with acute diarrhea. Indian J Pediatr 1989; 56 (01) 133-135
  • 58 Dwivedi KK, Prasad G, Saini S, Mahajan S, Lal S, Baveja UK. Enteric opportunistic parasites among HIV infected individuals: associated risk factors and immune status. Jpn J Infect Dis 2007; 60 (2-3) 76-81
  • 59 Sarkar R, Ajjampur SS, Prabakaran AD. et al. Cryptosporidiosis among children in an endemic semiurban community in southern India: does a protected drinking water source decrease infection?. Clin Infect Dis 2013; 57 (03) 398-406
  • 60 Bera P, Das S, Saha R, Ramachandran VG, Shah D. Cryptos-poridium in children with diarrhea: a hospital-based Study. Indian Pediatr 2014; 51 (11) 906-908
  • 61 Platts-Mills JA, Babji S, Bodhidatta L. et al. MAL-ED Network Investigators. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Glob Health 2015; 3 (09) e564-e575
  • 62 Al-Brikan FA, Salem HS, Beeching N, Hilal N. Multilocus genetic analysis of Cryptosporidium isolates from Saudi Arabia. J Egypt Soc Parasitol 2008; 38 (02) 645-658
  • 63 Xiao L, Ryan UM. Cryptosporidiosis: an update in molecular epidemiology. Curr Opin Infect Dis 2004; 17 (05) 483-490
  • 64 Maikai BV, Umoh JU, Lawal IA, Kudi AC, Ejembi CL, Xiao L. Molecular characterizations of Cryptosporidium, Giardia, and Enterocytozoon in humans in Kaduna State, Nigeria. Exp Parasitol 2012; 131 (04) 452-456
  • 65 Opintan JA, Newman MJ, Ayeh-Kumi PF. et al. Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg 2010; 83 (04) 936-943
  • 66 Lorntz B, Soares AM, Moore SR. et al. Early childhood diarrhea predicts impaired school performance. Pediatr Infect Dis J 2006; 25 (06) 513-520
  • 67 Mor SM, Tzipori S. Cryptosporidiosis in children in Sub-Saharan Africa: a lingering challenge. Clin Infect Dis 2008; 47 (07) 915-921
  • 68 Behera B, Mirdha BR, Makharia GK, Bhatnagar S, Dattagupta S, Samantaray JC. Parasites in patients with malabsorption syndrome: a clinical study in children and adults. Dig Dis Sci 2008; 53 (03) 672-679
  • 69 Kang G, Srivastava A, Pulimood AB, Dennison D, Chandy M. Etiology of diarrhea in patients undergoing allogeneic bone marrow transplantation in South India. Transplantation 2002; 73 (08) 1247-1251
  • 70 Weisburger WR, Hutcheon DF, Yardley JH, Roche JC, Hillis WD, Charache P. Cryptosporidiosis in an immunosuppressed renal-transplant recipient with IgA deficiency. Am J Clin Pathol 1979; 72 (03) 473-478
  • 71 Minz M, Udgiri NK, Heer MK, Kashyap R, Malla N. Cryptos-poridiasis in live related renal transplant recipients: a single center experience. Transplantation 2004; 77 (12) 1916-1917
  • 72 Bhadauria D, Goel A, Kaul A. et al. Cryptosporidium infection after renal transplantation in an endemic area. Transpl Infect Dis 2015; 17 (01) 48-55
  • 73 Yadav P, Khalil S, Mirdha BR. Molecular appraisal of intestinal parasitic infection in transplant recipients. Indian J Med Res 2016; 144 (02) 258-263
  • 74 Ghoshal U, Ranjan P, Dey A, Ghoshal UC. Intestinal cryptosporidiosis in renal transplant recipients: prevalence, species detection and comparative evaluation of SSU rRNA and Cryptosporidium oocyst wall protein genes. Indian J Med Microbiol 2018; 36 (02) 247-250
  • 75 Rudrapatna JS, Kumar V, Sridhar H. Intestinal parasitic infections in patients with malignancy. J Diarrhoeal Dis Res 1997; 15 (02) 71-74
  • 76 Sreedharan A, Jayshree RS, Sridhar H. Cryptosporidiosis among cancer patients: an observation. J Diarrhoeal Dis Res 1996; 14 (03) 211-213
  • 77 Zhang N, Yu X, Zhang H. et al. Prevalence and genotyping of Cryptosporidium parvum in gastrointestinal cancer patients. J Cancer 2020; 11 (11) 3334-3339
  • 78 Efstratiou A, Ongerth JE, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2011-2016. Water Res 2017; 114: 14-22
  • 79 Ryan U, Hijjawi N, Xiao L. Foodborne cryptosporidiosis. Int J Parasitol 2018; 48 (01) 1-12
  • 80 Tali A, Addebbous A, Asmama S, Chabaa L, Zougaghi L. Respi-ratory cryptosporidiosis in two patients with HIV infection in a tertiary care hospital in Morocco. Ann Biol Clin (Paris) 2011; 69 (05) 605-608
  • 81 Kourda N, Blel A, Ben Jilani SB, Zermani R. [Gastric cryptosporidiosis revealing a small cell lung carcinoma (Tunisia)]. Bull Soc Pathol Exot 2008; 101 (01) 22-23
  • 82 Kumar H, Singh VB, Meena BL, Agrawal J, Beniwal S, Swami T. Pulmonary cryptosporidiosis in an immunocompetent host treated successfully with nitazoxanide. Lung India 2016; 33 (01) 69-71
  • 83 Shrikhande SN, Chande CA, Shegokar VR, Powar RM. Pul-monary cryptosporidiosis in HIV negative, immunocompromised host. Indian J Pathol Microbiol 2009; 52 (02) 267-268
  • 84 Gatei W, Das P, Dutta P. et al. Multilocus sequence typing and genetic structure of Cryptosporidium hominis from children in Kolkata, India. Infect Genet Evol 2007; 7 (02) 197-205
  • 85 Yadav P, Mirdha BR, Makharia GK, Chaudhry R. Multilocus sequence typing of Cryptosporidium hominis from northern India. Indian J Med Res 2017; 145 (01) 102-111
  • 86 Cacciò SM. Molecular epidemiology of human cryptosporidiosis. Parassitologia 2005; 47 (02) 185-192
  • 87 Alves M, Matos O, Antunes F. Multilocus PCR-RFLP analysis of Cryptosporidium isolates from HIV-infected patients from Portugal. Ann Trop Med Parasitol 2001; 95 (06) 627-632
  • 88 Cacciò S, Pinter E, Fantini R, Mezzaroma I, Pozio E. Human infection with Cryptosporidium felis: case report and literature review. Emerg Infect Dis 2002; 8 (01) 85-86
  • 89 Ong CS, Eisler DL, Alikhani A. et al. Novel cryptosporidium genotypes in sporadic cryptosporidiosis cases: first report of human infections with a cervine genotype. Emerg Infect Dis 2002; 8 (03) 263-268
  • 90 Leoni F, Gallimore CI, Green J, McLauchlin J. Characterisation of small double stranded RNA molecule in Cryptosporidium hominis, Cryptosporidium felis and Cryptosporidium meleagridis. Parasitol Int 2006; 55 (04) 299-306
  • 91 Hussain G, Roychoudhury S, Singha B, Paul J. Incidence of Cryptosporidium andersoni in diarrheal patients from southern Assam, India: a molecular approach. Eur J Clin Microbiol Infect Dis 2017; 36 (06) 1023-1032
  • 92 Abe N, Matsubayashi M, Kimata I, Iseki M. Subgenotype analysis of Cryptosporidium parvum isolates from humans and animals in Japan using the 60-kDa glycoprotein gene sequences. Parasitol Res 2006; 99 (03) 303-305
  • 93 O’Connor RM, Wanyiri JW, Cevallos AM, Priest JW, Ward HD. Cryptosporidium parvum glycoprotein gp40 localizes to the sporozoite surface by association with gp15. Mol Biochem Parasitol 2007; 156 (01) 80-83
  • 94 Alves M, Matos O, Antunes F. Microsatellite analysis of Cryptosporidium hominis and C. parvum in Portugal: a preliminary study. J Eukaryot Microbiol 2003; 50 (Suppl. 01) 529-530
  • 95 Ajjampur SS, Liakath FB, Kannan A. et al. Multisite study of cryptosporidiosis in children with diarrhea in India. J Clin Microbiol 2010; 48 (06) 2075-2081
  • 96 Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 2010; 124 (01) 80-89
  • 97 Gatei W, Barrett D, Lindo JF, Eldemire-Shearer D, Cama V, Xiao L. Unique Cryptosporidium population in HIV-infected persons, Jamaica. Emerg Infect Dis 2008; 14 (05) 841-843
  • 98 Chalmers RM, Hadfield SJ, Jackson CJ, Elwin K, Xiao L, Hunter P. Geographic linkage and variation in Cryptosporidium hominis. Emerg Infect Dis 2008; 14 (03) 496-498
  • 99 Sulaiman IM, Hira PR, Zhou L. et al. Unique endemicity of cryptosporidiosis in children in Kuwait. J Clin Microbiol 2005; 43 (06) 2805-2809
  • 100 Trotz-Williams LA, Martin DS, Gatei W. et al. Genotype and subtype analyses of Cryptosporidium isolates from dairy calves and humans in Ontario. Parasitol Res 2006; 99: 346-52
  • 101 Valenzuela O, González-Díaz M, Garibay-Escobar A. et al. Molecular characterization of Cryptosporidium spp. in children from Mexico. PLoS One 2014; 9 (04) e96128
  • 102 Alves M, Xiao L, Antunes F, Matos O. Distribution of Cryptosporidium subtypes in humans and domestic and wild ruminants in Portugal. Parasitol Res 2006; 99 (03) 287-292
  • 103 Lucca Pd, De Gaspari EN, Bozzoli LM, Funada MR, Silva SO, Iuliano W, Soares RM. Molecular characterization of Cryptosporidium spp. from HIV infected patients from an urban area of Brazil. Rev Inst Med Trop Sao Paulo 2009; 51 (06) 341-343
  • 104 Bushen OY, Kohli A, Pinkerton RC. et al. Heavy cryptosporidial infections in children in northeast Brazil: comparison of Cryptosporidium hominis and Cryptosporidium parvum. Trans R Soc Trop Med Hyg 2007; 101 (04) 378-384
  • 105 Waldron LS, Ferrari BC, Power ML. Glycoprotein 60 diversity in C. hominis and C. parvum causing human cryptosporidiosis in NSW, Australia. Exp Parasitol 2009; 122 (02) 124-127
  • 106 Jex AR, Ryan UM, Ng J, Campbell BE, Xiao L, Stevens M, Gasser RB. Specific and genotypic identification of Cryptosporidium from a broad range of host species by nonisotopic SSCP analysis of nuclear ribosomal DNA. Electrophoresis 2007; 28 (16) 2818-2825
  • 107 Ng J, Eastwood K, Durrheim D, Massey P, Walker B, Armson A, Ryan U. Evidence supporting zoonotic transmission of Cryptosporidium in rural New South Wales. Exp Parasitol 2008; 119 (01) 348-356
  • 108 Ng J, MacKenzie B, Ryan U. Longitudinal multi-locus molecular characterisation of sporadic Australian human clinical cases of cryptosporidiosis from 2005 to 2008. Exp Parasitol 2010; 125 (04) 348-356
  • 109 O’Brien E, McInnes L, Ryan U. Cryptosporidium GP60 genotypes from humans and domesticated animals in Australia, North America and Europe. Exp Parasitol 2008; 118: 118-121
  • 110 Guyot K, Follet-Dumoulin A, Lelièvre E. et al. Molecular characterization of Cryptosporidium isolates obtained from humans in France. J Clin Microbiol 2001; 39 (10) 3472-3480
  • 111 Zintl A, Proctor AF, Read C. Dewaal T, Shanaghy N, Fanning S, Mulcahy G. The prevalence of Cryptosporidium species and subtypes in human faecal samples in Ireland. Epidemiol Infect 2009; 137 (02) 270-277
  • 112 Leav BA, Mackay MR, Anyanwu A. et al. Analysis of sequence diversity at the highly polymorphic Cpgp40/15 locus among Cryptosporidium isolates from human immunodeficiency virus-infected children in South Africa. Infect Immun 2002; 70 (07) 3881-3890
  • 113 Adamu H, Petros B, Zhang G, Kassa H, Amer S, Ye J, Feng Y, Xiao L. Distribution and clinical manifestations of Cryptosporidium species and subtypes in HIV/AIDS patients in Ethiopia. PLoS Negl Trop Dis 2014; 8 (04) e2831
  • 114 Molloy SF, Tanner CJ, Kirwan P. et al. Sporadic Cryptosporidium infection in Nigerian children: risk factors with species identification. Epidemiol Infect 2011; 139 (06) 946-954
  • 115 Alyousefi NA, Mahdy MA, Mahmud R, Lim YA. Factors associated with high prevalence of intestinal protozoan infections among patients in Sana’a City, Yemen. PLoS One 2011; 6 (07) e22044
  • 116 Nyamwange CI, Mkoji G, Mpoke S, Nyandieka HS. Cryptosporidiosis and its genotypes among children attending MOI teaching and referral hospital in Eldoret, Kenya. East Afr Med J 2012; 89 (01) 11-19
  • 117 Iqbal J, Khalid N, Hira PR. Cryptosporidiosis in Kuwaiti children: association of clinical characteristics with Cryptosporidium species and subtypes. J Med Microbiol 2011; 60 (Pt 5) 647-652
  • 118 Rao Ajjampur SS, Asirvatham JR, Muthusamy D. et al. Clinical features & risk factors associated with cryptosporidiosisin HIV infected adults in India. Indian J Med Res 2007; 126 (06) 553-557
  • 119 Yadav P, Khalil S, Mirdha BR. Molecular appraisal of intestinalparasitic infection in transplant recipients. Indian J Med Res 2016; 144 (02) 258-263
  • 120 Das P, Roy SS, MitraDhar K. et al. Molecular characterization of Cryptosporidium spp. from children in Kolkata, India. J Clin Microbiol 2006; 44 (11) 4246-4249
  • 121 Del Chierico F, Onori M, Di Bella S. et al. Cases of cryptosporidiosis co-infections in AIDS patients: a correlation between clinical presentation and GP60 subgenotype lineages from aged formalin-fixed stool samples. Ann Trop Med Parasitol 2011; 105 (05) 339-349