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

Ana Carolina M. GonçalvesUniversity 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. GabbayUniversity 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 MascarenhasUniversity 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. YassakaUniversity 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. MoranUniversity 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. FragaUniversity 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 CastroUniversity 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 FrancoUniversity 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. MachadoUniversity 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. RossitUniversity 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.

INTRODUCTION

In Latin America one-third of all human immunodeficiency virus (HIV)-positive individuals reside in Brazil, a country that mirrors the international trend in the increase in prevalence of this infection. Sixty percent of all cases are concentrated in Southeastern Brazil, an area which also leads in the absolute number of deaths by the disease1 and in percentage (90%) of people living 5 years after diagnosis.2 Among the clinical manifestations consequent to immunosuppression by HIV, diarrhea is of concern because of the considerable reduction in immunologic response in the intestinal mucosa, making local unspecific defense difficult and, thus, accentuating its severity. 3,4 Moreover, traditionally non-pathogenic microorganisms and opportunistic infections have played an important role in the etiology of this disease.5

The aim of this work was to conduct a case-controlled study to evaluate the potential role of bacterial, yeast, parasitic, and viral enteropathogens in an adult HIV-infected group from Southeastern Brazil and also to study the correlation of these microorganisms with clinical and sociodemographic characteristics.

MATERIAL AND METHODS

Patient enrollment and sample collection.

The study was conducted from April 2006 to June 2007 by the staff of the Center for Microorganism Investigations (CIM), Southeastern Brazil. Sample collection and clinical evaluation was performed by the physicians of the regional center of acquired immunodeficiency syndrome (AIDS) treatment of Hospital de Base (HB), catering for a large population. Viral analysis was conducted at Evandro Chagas Institute (Virology Section), North Brazil. Patients were enrolled during hospitalization, after outpatient clinic evaluation at HB because of HIV. One fecal sample was collected from “cases” (clinical signs of diarrhea—three or more daily episodes of unformed stools) and from “controls” (without any gastrointestinal symptoms for more than 30 days before hospitalization). They were recruited from all individuals with the presence of anti-HIV antibodies by enzyme-linked immunosorbent assay (ELISA) and Western blot, in any HIV risk category.6 These were excluded if they were pregnant, less than 18 years of age, signs of non-infectious diarrhea (drug-associated diarrhea), or mental disorders. Clinical data including drug therapy, previous hospitalizations, viral load (VERSANT HIV-1 RNA 3.0 Assay bDNA, Siemens, Bayswater Victoria, Australia), and immune status (TriTEST CD4 FITC/CD8 PE/CD3 PerCP, Becton Dickinson, CA) were obtained from medical records according to a protocol approved by the Research Ethics Board of the Medicine School in São José do Rio Preto. Epidemiologic data were collected by a standard interviewer-administered questionnaire (Table 1).

Laboratory analysis.

Stool samples were transported in Cary–Blair transport media for bacterial and yeast analysis. Two clean containers were used for fecal collection and stored at −70°C for parasites and viruses studies. All specimens were immediately sent and examined at CIM according to standard bacteriologic and mycologic procedures. 7,8 Enteric protozoan were studied by immunoenzimatic assays.7 To detect viruses, molecular methods were applied as recommended, with modifications.913

Statistical analysis.

To obtain independence among proportions, we applied the χ2 test or the Fisher’s exact test and for odds ratio (OR) we considered a 95% confidence interval (CI) (Epi Info, version 6.0, CDC, Atlanta, GA). The relationship between the studied variables was assessed using the Wilcoxon rank sum test. The adopted significance level for statistical inference was 5%.

RESULTS

Forty diarrheicand 60 non-diarrheic HIV-seropositive/AIDS patients were included. As summarized in Table 1, approximately half of them were men and the difference between mean ages and genders did not show significant differences, indicating a well-matched population. The sociodemographic and clinical characteristics were not associated to diarrhea, except for severe immunosuppression and the isolation of at least one enteropathogen (P = 0.0055 and 0.008, respectively). The cases, all presenting non-severe diarrhea, were more commonly infected and/or colonized by two or more enteropathogens (8/40) compared with controls (1/60; P = 0.0026; Fisher’s exact test). The simultaneous presence of Giardia lamblia, Entamoeba histolytica, Salmonella Gallinarum, and Shigella flexneri was detected in one diarrheic patient. The clinical signs studied, such as abdominal pain, vomiting, and fever, and the presence of mucous and/or blood in stools, were more frequently observed in the case group (P < 0.05).

Enteropathogenic Escherichia coli (EPEC) was the commonest bacteria (22.5%) and 12.5% of them produced extended-spectrum beta-lactamase (ESBL), as well one enteroinvasive E. coli (EIEC) strain. One-third of all E. coli were multiresistant. Candida albicans was isolated in more than half of the patients, whereas the remaining were “non-albicans” species. No patient carried rotavirus, only one the astrovirus and the calicivirus, detected in 10% of the cases, was associated to diarrhea (P = 0.0233; Fisher’s exact test). The following parasites were detected: Cryptosporidium parvum (9%), G. lamblia (5%), and E. histolytica (2%). Protozoan carriers were at stronger risk of diarrhea, however G. lamblia was the only parasite significantly associated (P = 0.0087; Fisher’s exact test). No significant associations were observed between the presences of blood or mucous in stools, fever, abdominal pain, and vomiting with infection by G. lamblia or calicivirus (Table 2).

DISCUSSION

Sociodemographic features in our study population were equivalent to those described in the Brazilian AIDS epidemic.2 Environmental exposure does not seem to play a role as a risk factor for diarrhea in the studied population. However, severe immunosuppression was associated with this manifestation, as was previously verified in other HIV-positive populations, including infants. 4,7,1417

Within the 100 stool samples, 137 microorganisms were detected with G. lamblia and calicivirus significantly associated with diarrhea. Enterobacteria were isolated in 25% and 11.7% of diarrheic and non-diarrheic individuals, respectively, repeating the percentage found in diarrheic HIV-seropositive children from the same region.7 In different HIV-positive adult populations results varied from failure to detect any enter-obacteria, 18 low positivity 19 to high positivity rates. 14,20 Two of the isolated EPEC serotypes 0111:H- and 026:H11 were previously reported as prevalent among diarrheic children 21 and cattle feces 22 in São Paulo state. Ciprofloxacin ESBL producing 23 or quinolone-resistant 24 EPEC O102 serogroup strains were isolated before from hospitalized adults. Interestingly, the O102:H30 EPEC isolated in our study proved to be an ESBL quinolone-resistant strain. Even though serogrouping itself (O antigen only) must not be taken as an EPEC diagnostic method, 21 the results obtained highlight the need for further study on virulence factors, such as those encoded by the Stx and eae genes, to define their relevance. Another limitation we acknowledge is the absence of molecular methodology for EAggEC detection, previously recognized as an important enteropathogen in HIV-seropositive patients. 14 Higher frequencies of Shigella spp. isolation were reported in HIV-seropositive Africans, 14 Indians,25 and Peruvians 20 compared with our results, whereas the frequencies of Salmonella spp. were found to be similar. In Brazil, these two species were not important in an infantile HIV-seropositive diarrheic population.7

Undoubtedly, the major endogenous reservoir of Candida spp. is the gastrointestinal tract, 26 source of microbial translocation and fungemia, 27,28 however there is a controversy about its role as a diarrhea-causing enteropathogen. 29,30 As for C. albicans, the isolation in stools of HIV patients from different countries 7,14,18,3133 yielded prevalence rates of 2.86% to 39.1%. Our results are the highest reported levels (53%).

Our present data on rotavirus and astrovirus reinforce the previously reported possibility of low circulation of both viruses in the studied region.7 This is the first report of calicivirus as a causative agent of diarrhea in HIV-seropositive adults. In Brazil, norovirus was detected in 60% of a non-HIV population during an outbreak of diarrhea in the southwestern region (Rio de Janeiro State) 34 and in 8.6% of the infant population from the West Central region of the country. 35 In fact, Sapovirus and Norovirus have already been detected in hospitalized and non-hospitalized children, both in outbreaks of diarrhea and isolated cases, with an occurrence compared with rotavirus. 36,37 In HIV-seropositive adults, calicivirus was detected in a frequency of 7% in North Americans, 38 whereas in Venezuelans it ranged from null 39 to a 9.4% isolation frequency. 40

Crysptosporidium parvum revealed a high prevalence in asymptomatic HIV-seropositive/AIDS patients in the same Brazilian region 5 years ago, although not associated with diarrhea. 6,41 Similar to the other Brazilian studies, here E. hystolitica was not associated to diarrhea. 7,42,43 Giardia lamblia positive association to diarrhea in our study, 41 corroborates data from São Paulo city (450 km apart from the study area). 13 In Brazilian distinct regions, a large difference in its frequency has been observed with several reports of significant associations with diarrhea in HIV-positive patients. 5,7,4143 A wide variation, ranging from 3% to 14%, was also detected in other countries, making comparisons difficult. 20,44,45 Our results are comparable to the lowest national rates (4%), repeating those obtained 4 years before in the same population. 41 The mechanism by which G. lamblia causes diarrhea and low intestinal absorption remains controversial, but one possible explanation is the involvement of multiple factors such as the age of cysts, the host immune status, and the parasite genetic variability. 46 Another possibility could be concurrent gut infections with calicivirus because in our study three patients shared this combination.

There is a great diversity of pathogens and opportunistic agents in HIV individuals, with a high prevalence of mixed colonization/infection, which is a concern because they act as reservoirs. These data are relevant in the improvement of therapies and controlling diarrhea in the HIV-seropositive population and highlight the need for study on pathogen-host interactions.

Table 1

Sociodemographic and clinical characteristics of 100 HIV-seropositive/AIDS patients in respect to the presence (cases; N = 40) or absence (controls; N = 60) of clinical signs of diarrhea*

Table 1
Table 2

Absolute and relative incidences of the different enteropathogens detected in stools of the 100 HIV-seropositive/AIDS patients in respect to the presence (cases; N = 40) or absence (controls; N = 60) of clinical signs of diarrhea*

Table 2

*

Address correspondence to 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. E-mail: andrea@famerp.br

Authors’ addresses: Ana Carolina Musa Gonçalves, University Center of Rio Preto (UNIRP), Rua Yvete Gabriel Atique, no 45, Boa Vista, 15025-400-São José do Rio Preto, SP-Brazil, Tel/Fax: +55 17 32113000, E-mail: acmusa23@yahoo.com.br. Yvone Benchmol Gabbay and Joana D’Arc Mascarenhas, Virology Section, Evandro Chagas Institute, BR-316 Km 07 s/n, Ananindeua, PA-Brazil, Tel/Fax: +55 91 32142015/32142016, E-mail: yvonegabbay@iec.pa.gov.br and joanamascarenhas@iec.pa.gov.br. Luciana Conceição Moran, Valéria Daltibari Fraga, Marcela Braga Yassaka, and Ricardo Luiz Dantas Machado, 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 32015736, E-mails: lucianamoran@famerp.br, valeriafraga@famerp.br, ma_yassaka@yahoo.com.br, and ricardomachado@famerp.br. Célia Franco and Edna Castro, Infectious ans Parasitic Diseases Service of Hospital de Base, Avenida Brigadeiro Faria Lima, 5544, Vila São Pedro, 15090-000, São José do Rio Preto, SP-Brazil, Tel/Fax: +55 17 32015006, E-mails: cfranco@famerp.br and ednacastrohb@hotmail.com. Andréa Regina B. Rossit, Center for Micro organism 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.

Acknowledgments: We thank Irineu Luiz Maia for his help on discussing important issues on the clinical aspects of the HIV population and Elizabete Santos and Alexandre Linhares from the Evandro Chagas Institute for institutional support of viral analysis.

Financial support: This work was supported by grants from: the Medicine School in São José do Rio Preto (BAP-FAMERP), FAPESP, and the Post Graduate Support Program (PROAP-CAPES). Marcela B. Yassaka was supported by a scholarship from the National Council for Research and Development – PIBIC/CNPq-FAMERP.

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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.
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