Calicivirus and Giardia lamblia are Associated with Diarrhea in Human Immunodeficiency Virus-Seropositive Patients from Southeast Brazil

Ana Carolina M. Gonçalves University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Yvone B. Gabbay University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Joana D’arc Mascarenhas University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Marcela B. Yassaka University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Luciana C. Moran University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Valéria D. Fraga University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Edna Castro University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Célia Franco University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Ricardo Luiz D. Machado University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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Andréa Regina B. Rossit University Center of Rio Preto (UNIRP), São José do Rio Preto, São Paulo; Virology Section, Evandro Chagas Institute, Ananindeua, Pará; Center for Microorganism Investigations, Department of Dermatology, Parasitic and Infectious Diseases, Medicine School in São José do Rio Preto (FAMERP), São Paulo; Infectious and Parasitic Diseases Service of Hospital de Base, Regional Medicine School in São José do Rio Preto (FUNFARME), São José do Rio Preto, São Paulo, Brazil

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To study enteropathogens, 100 fecal samples were collected from a Brazilian human immunodeficiency virus (HIV)-seropositive population, with or without diarrhea. Giardia lamblia and calicivirus were significantly associated with diarrhea as were severe immunosuppression and the presence of at least one enteropathogen. No sample was positive for rotavirus and only one asymptomatic individual carried the astrovirus. We concluded that there is a great diversity of pathogens and opportunistic infections in the studied population, with a high prevalence of mixed colonization/infection. Our findings pave the way for future molecular studies related to the expression of virulence factors and to the possibility of pathogen–pathogen interactions, especially between G. lamblia and calicivirus. These findings are relevant to the improvement of therapies and controlling diarrhea in the HIV-seropositive population.

Author Notes

Reprint requests: Andréa Regina B. Rossit, Center for Microorganism Investigation, Av. Brigadeiro Faria Lima, 5416, Vila São Pedro, 15090-000, São José do Rio Preto, SP-Brazil, Tel/Fax: +55 17 32015909, E-mail: andrea@famerp.br.
  • 1

    UNAIDS, 2007. AIDS Epidemic Update 2007 – Latin America Regional Summary. Available at: http://www.unAIDS.org. Accessed July 15, 2008.

    • PubMed
    • Export Citation
  • 2

    Brasília, Ministry of Health, 2007. Brazil, Ministry of Health, Health Surveillance Department, National DST/AIDS Program. Bulletin Epidemiological of Sexually Transmitted Disease Program/AIDS. Available at: http://www.aids.gov.br. Accessed July 18, 2008.

    • PubMed
    • Export Citation
  • 3

    Motta MEFA, Silva GAP, 2002. Diarréia por parasitas. Rev Bras Saúde Matern Infant 2 :117–127.

  • 4

    Brink AK, Mahé C, Watera C, Lugada E, Gilks C, Whitworth J, French N, 2002. Diarrhea, CD4 counts and enteric infections in a community-based cohort of HIV adults in Uganda. J Infect 45 :99–106.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Cimerman S, Cimerman B, Lewi DS, 1999. Prevalence of intestinal parasitic infections in patients with acquired immunodeficiency syndrome in Brazil. Int J Infect Dis 3 :203–206.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Castro KG, Ward JW, Slutsker L, Buehler JW, Jaffe HW, Berkelman RL, 1992. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR Recomm Rep 41 :1–19.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Rossit AR, Almeida MT, Nogueira CA, Oliveira JG, Barbosa DM, Moscardini AC, Mascarenhas JD, Gabbay JB, Marques FR, Cardoso LV, Cavasini CE, Machado RL, 2007. Bacterial, yeast, parasitic, and viral enteropathogens in HIV-infected children from São Paulo State, Southeastern Brazil. Diagn Microbiol Infect Dis 57 :59–66.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Bauer AW, Kirby WM, Sherris JC, Turck M, 1966. Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45 :493–496.

  • 9

    Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, van der Noordaa J, 1990. Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28 :495–503.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    das Dôres de Paula Cardoso D, Fiaccadori FS, Borges de Lima Dias e Souza M, Bringel Martins RM, Gagliardi Leite JP, 2002. Detection and genotyping of astroviruses from children with acute gastroenteritis from Goiânia, Goiás, Brazil. Med Sci Monit 8 :CR624–CR628.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Noel JS, Lee TW, Kurtz JB, Glass RI, Monroe SS, 1995. Typing of human astroviruses from clinical isolates by enzyme immuno-assay and nucleotide sequencing. J Clin Microbiol 33 :797–801.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Jiang X, Huang PW, Zhong WM, Farkas T, Cubitt DW, Matson DO, 1999. Design and evaluation of a primer pair that detects both Norwalk- and Sapporo-like caliciviruses by RT-PCR. J Virol Methods 83 :145–154.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Pereira HG, Azeredo RS, Leite Barth OM, Sutmoller F, de Farias V, Vidal MN, 1983. Comparison of polyacrylamide gel electrophoresis (PAGE), immuno-electron microscopy (IEM) and enzyme immunoassay (EIA) for the rapid diagnosis of rotavirus infection in children. Mem Inst Oswaldo Cruz 78 :483–490.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Gassama A, Sow PS, Fall F, Camara P, Philippe H, Guéye-N’diaye A, Seng R, Samb B, M’Boup S, Germani Y, Aidara-Kane A, 2001. Ordinary and opportunistic enteropathogens associated with diarrhea in Senegalese adults in relation to human immunodeficiency virus serostatus. Int J Infect Dis 5 :192–198.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Galli L, de Martino M, Tovo PA, Gabiano C, Zappa M, Giaquinto C, Tulisso S, Vierucci A, Guerra M, Marchisio P, 1995. Onset of clinical signs in children with HIV-1 perinatal infection. Ital Reg HIV Infect Child 9 :455–461.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Kakai R, Bwayo JJ, Wamola IA, Ndinya-Achola JO, Plummer FA, 1995. Effect of human immunodeficiency virus on local immunity in children with diarrhea. East Afr Med J 72 :699–702.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Onyemelukwe GC, Musa BO, 2002. CD4+ and CD8+ lymphocytes and clinical features of HIV seropositive Nigerians on presentation. Afr J Med Sci 31 :229–233.

  • 18

    Attili SV, Gulati AK, Singh VP, Varma DV, Rai M, Sundar S, 2006. Diarrhea, CD4 counts and enteric infections in a hospital-based cohort of HIV-infected patients around Varanasi, India. BMC Infect Dis 6 :39.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Prasad KN, Nag VL, Dhole TN, Ayyagari A, 2000. Identification of enteropathogens in HIV-positive patients with diarrhea in Northern India. J Health Popul Nutr 18 :23–26.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Cárcamo C, Hooton T, Wener MH, Weiss NS, Gilman R, Arevalo J, Carrasco J, Seas C, Caballero M, Holmes KK, 2005. Etiologies and manifestations of persistent diarrhea in adults with HIV-1 infection: a case-control study in Lima, Peru. J Infect Dis 191 :11–19.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Campos LC, Franzolin MR, Trabulsi LR, 2004. Diarrheagenic Escherichia coli categories among the traditional entero E. coli O serogroups: a review. Mem Inst Oswaldo Cruz 99 :545–552.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Aidar-Ugrinovich L, Blanco J, Blanco M, Blanco JE, Leomil L, Dahbi G, Onuma DL, Silveira WD, Pestana de Castro AF, 2007. Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in São Paulo, Brazil. Int J Food Microbiol 115 :297–306.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Wolk M, Valinsky L, Sompolinsky D, Sechter I, Schmidt H, Tetry S, Agmon V, 2004. Endemic occurrence of infections by multi-drug-resistant Escherichia coli of four unique serotypes in the elderly population of Israel. FEMS Microbiol Lett 239 :249–254.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Jones GL, Warren RE, Skidmore SJ, Davies VA, Gibreel T, Upton M, 2008. Prevalence and distribution of plasmid-mediated quinolone resistance genes in clinical isolates of Escherichia coli lacking extended-spectrum β-lactamase. J Antimicrob Chemother 62 :1245–1251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Kownhar H, Shankar EM, Rajan R, Vengatesan A, Rao UA, 2007. Prevalence of Campylobacter jejuni and enteric bacterial pathogens among hospitalized HIV infected versus non-HIV infected patients with diarrhoea in Southern India. Scand J Infect Dis 39 :862–866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Pfaller MA, 1994. Epidemiology and control of fungal infections. Clin Infect Dis 19 :S8–S13.

  • 27

    Colombo AL, Branchini ML, Geiger D, Schimidt AL, Pignatari AC, Fischman O, 1996. Gastrointestinal translocation as a possible source of candidemia in an AIDS patient. Rev Inst Med Trop Sao Paulo 38 :197–200.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Muñoz P, Sánchez-Somolinos M, Alcalá L, rodríguez-Crèixems M, Peláez T, Bouza E, 2005. Candida krusei fungaemia: antifungal susceptibility and clinical presentation of an uncommon entity during 15 years in a single general hospital. J Antimicrob Chemother 55 :188–193.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Krause R, Reisinger EC, 2005. Candida and antibiotic-associated diarrhea. Clin Microbiol Infect 11 :1–2.

  • 30

    Kaltenbach G, Heitz D, 2004. Antibiotic-associated diarrhea in the elderly. Rev Med Interne 25 :46–53.

  • 31

    Same-Ekobo A, Lohoue J, Mbassi A, 1997. A clinical and biological study of parasitic and fungal diarrhea in immunosuppressed patients in an urban and suburban area of Yaoundé. Sante 7 :349–354.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Anand L, Dhanachand C, Brajachand N, 1998. Prevalence and epidemiologic characteristics of opportunistic and non-opportunistic intestinal parasitic infections in HIV positive patients in Manipur. J Commun Dis 30 :19–22.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Therizol-Ferly PM, Tagliante-Saracino J, Kone M, Konan A, Ouhon J, Assoumou A, Aka K, Assale G, 1989. Chronic diarrhea and parasitosis in adults suspected of AIDS in the Ivory Coast. Bull Soc Pathol Exot Filiales 82 :690–693.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Ferreira MS, Xavier MP, Fumian TM, Victoria M, Oliveira SA, Pena LH, Leite JP, Miagostovich MP, 2008. Acute gastroenteritis cases associated with noroviruses infection in the State of Rio de Janeiro. J Med Virol 80 :338–344.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Borges AM, Teixeira JM, Costa PS, Giugliano LG, Fiaccadori FS, Franco RC, Brito WM, Leite JP, Cardoso DD, 2006. Detection of calicivirus from fecal samples from children with acute gastroenteritis in the West Central region of Brazil. Mem Inst Oswaldo Cruz 101 :721–724.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Monica B, Ramani S, Banerjee I, Primrose B, Iturriza-Gomara M, Gallimore CI, Brown DW, M F, Moses PD, Gray JJ, Kang G, 2007. Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J Med Virol 79 :544–551.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Dove W, Cunliffe NA, Gondwe JS, Broadhead RL, Molyneux ME, Nakagomi O, Hart CA, 2005. Detection and characterization of human caliciviruses in hospitalized children with acute gastro-enteritis in Blantyre, Malawi. J Med Virol 77 :522–527.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Grohmann GS, Glass RI, Pereira HG, Monroe SS, Hightower AW, Weber R, Bryan RT, 1993. Enteric viruses and diarrhea in HIV-infected patients. Enteric Opportunistic Infections Working Group. N Engl J Med 329 :14–20.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    González GG, Pujol FH, Liprandi F, Deibis L, Ludert JE, 1998. Prevalence of enteric viruses in human immunodeficiency virus seropositive patients in Venezuela. J Med Virol 55 :288–292.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Rodriguez-Guillen L, Vizzi E, Alcala AC, Pujol FH, Liprandi F, Ludert JE, 2005. Calicivirus infection in human immunodeficiency virus seropositive children and adults. J Clin Virol 33 :104–109.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Cardoso LV, Marques FR, Cavasini CE, Almeida MC, Bassi NA, Gongóra DV, Maia IL, Rossit AR, Machado RL, 2004. Correlation of intestinal parasitic pathogens in HIV-seropositive adult with and without diarrhea in Northeast region of São Paulo State, Brazil. Rev Panam Infect 6 :8–11.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Moura H, Fernandes O, Viola JP, Silva SP, Passos RH, Lima DB, 1989. Enteric parasites and HIV infection: occurrence in AIDS patients in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 84 :527–533.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Feitosa G, Bandeira AC, Sampaio DP, Badaró R, Brites C, 2001. High prevalence of giardiasis and strongyloidiasis among HIV-infected patients in Bahia, Brazil. Braz J Infect Dis 5 :339–344.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Dwivedi KK, Prasad G, Saini S, Mahajan S, Lal S, Baveja UK, 2007. Enteric opportunistic parasites among HIV infected individuals: associated risk factors and immune status. Jpn J Infect Dis 60 :76–81.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Fontanet AL, Sahlu T, Rinke de Wit T, Messele T, Masho W, Woldemichael T, Yeneneh H, Coutinho RA, 2000. Epidemiology of infections with intestinal parasites and human immunodeficiency virus (HIV) among sugar-estate residents in Ethiopia. Ann Trop Med Parasitol 94 :269–278.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Caccio SM, Ryan U, 2008. Molecular epidemiology of giardiasis. Mol Biochem Parasitol 160 :75–80.

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