• View in gallery
    Figure 1.

    Coinfection heat map. The graph shows the frequency of coinfections by microorganism among the 59 cases simultaneously investigated for parasites, bacterial enteropathogens, and other sexually transmitted infection agents. CT = Chlamydia trachomatis; NG = Neisseria gonorrhoeae.

  • 1.

    Most H, 1968. Manhattan: a tropic isle? Am J Trop Med Hyg 17: 333354.

  • 2.

    Escolà-Vergé L, Arando M, Vall M, Rovira R, Espasa M, Sulleiro E, Armengol P, Zarzuela F, Barberá MJ, 2017. Outbreak of intestinal amoebiasis among men who have sex with men, Barcelona (Spain), October 2016–January 2017. Euro Surveill 22: 30581.

    • Search Google Scholar
    • Export Citation
  • 3.

    Okame M et al. 2012. Shigella sonnei outbreak among men who have sex with men in Tokyo. J Infect Dis 65: 277278.

  • 4.

    Rodríguez-Tajes S, Perpiñán E, Caballol B, Lens S, Mariño Z, Costa J, Vilella A, Pérez-Del-Pulgar S, Forns X, Koutsoudakis G, 2018. Hepatitis A outbreak in Barcelona among men who have sex with men (MSM), January–June 2017: a hospital perspective. Liver Int 38: 588593.

    • Search Google Scholar
    • Export Citation
  • 5.

    Baker RW, Peppercorn MA, 1982. Gastrointestinal ailments of homosexual men. Medicine (Baltimore) 61: 390405.

  • 6.

    Ortega HB, Borchardt KA, Hamilton R, Ortega P, Mahood J, 1984. Enteric pathogenic protozoa in homosexual men from San Francisco. Sex Transm Dis 11: 5963.

    • Search Google Scholar
    • Export Citation
  • 7.

    Centers for Disease Control, 1981. Amebiasis associated with colonic irrigation: Colorado. MMWR Morb Mortal Wkly Rep 30: 101.

  • 8.

    Whitlock GG, Gibbons DC, Longford N, Harvey MJ, McOwan A, Adams EJ, 2018. Rapid testing and treatment for sexually transmitted infections improve patient care and yield public health benefits. Int J STD AIDS 29: 474482.

    • Search Google Scholar
    • Export Citation
  • 9.

    Abdolrasouli A, McMillan A, Ackers JP, 2009. Sexual transmission of intestinal parasites in men who have sex with men. Sex Health 6: 185194.

    • Search Google Scholar
    • Export Citation
  • 10.

    de Vries HJ, Zingoni A, White JA, Ross JD, Kreuter A, 2014. 2013 European guideline on the management of proctitis, proctocolitis and enteritis caused by sexually transmissible pathogens. Int J STD AIDS 25: 465474.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mohammed H, Mitchell H, Sile B, Duffell S, Nardone A, Hughes G, 2016. Increase in sexually transmitted infections among men who have sex with men, England, 2014. Emerg Infect Dis 22: 8891.

    • Search Google Scholar
    • Export Citation
  • 12.

    Stark D, Fotedar R, van Hal S, Beebe N, Marriott D, Ellis JT, Harkness J, 2007. Prevalence of enteric protozoa in human immunodeficiency virus (HIV)–positive and HIV–negative men who have sex with men from Sydney, Australia. Am J Trop Med Hyg 76: 549552.

    • Search Google Scholar
    • Export Citation
  • 13.

    Calderaro A, Montecchini S, Rossi S, Gorrini C, De Conto F, Medici MC, Chezzi C, Arcangeletti MC, 2014. Intestinal parasitoses in a tertiary–care hospital located in a non-endemic setting during 2006–2010. BMC Infect Dis 14: 264.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ali SA, Hill DR, 2003. Giardia intestinalis. Curr Opin Infect Dis 16: 453460.

  • 15.

    Stark D, Beebe N, Marriott D, Ellis J, Harkness J, 2005. Prospective study of the prevalence, genotyping, and clinical relevance of Dientamoeba fragilis infections in an Australian population. J Clin Microbiol 43: 27182723.

    • Search Google Scholar
    • Export Citation
  • 16.

    Sheehan DJ, Raucher BG, McKitrick JC, 1986. Association of Blastocystis hominis with signs and symptoms of human disease. J Clin Microbiol 24: 548550.

    • Search Google Scholar
    • Export Citation
  • 17.

    William DC, Shookhoff HB, Felman YM, DeRamos SW, 1978. High rates of enteric protozoal infections in selected homosexual men attending a venereal disease clinic. Sex Transm Dis 5: 155157.

    • Search Google Scholar
    • Export Citation
  • 18.

    Salvador F, Sulleiro E, Sánchez-Montalvá A, Alonso C, Santos J, Fuentes I, Molina I, 2016. Epidemiological and clinical profile of adult patients with Blastocystis sp. infection in Barcelona, Spain. Parasit Vectors 9: 548.

    • Search Google Scholar
    • Export Citation
  • 19.

    Pozio E, Morales MA, 2005. The impact of HIV-protease inhibitors on opportunistic parasites. Trends Parasitol 21: 5863.

  • 20.

    Quinn TC, Stamm WE, Goodell SE, Mkrtichian E, Benedetti J, Corey L, Schuffler MD, Holmes KK, 1983. The polymicrobial origin of intestinal infections in homosexual men. N Engl J Med 309: 576582.

    • Search Google Scholar
    • Export Citation
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Sexual Transmission of Intestinal Parasites and Other Enteric Pathogens among Men Who Have Sex with Men Presenting Gastrointestinal Symptoms in an STI Unit in Barcelona, Spain: A Cross-Sectional Study

Miguel Fernández-HuertaMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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Francesc ZarzuelaMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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María-Jesús BarberáInfectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain;
University of Barcelona, Barcelona, Spain

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Maider ArandoUniversitat Autònoma de Barcelona, Barcelona, Spain;
Infectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain;

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Juliana EsperalbaMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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Virginia RodríguezMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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Martí VallUniversitat Autònoma de Barcelona, Barcelona, Spain;
Infectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain;

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Vicenç FalcóUniversitat Autònoma de Barcelona, Barcelona, Spain;
Infectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain;

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Jorge-Néstor García-PérezUniversitat Autònoma de Barcelona, Barcelona, Spain;
Infectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain;

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Tomàs PumarolaMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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Mateu EspasaMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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Elena SulleiroMicrobiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain;
Universitat Autònoma de Barcelona, Barcelona, Spain;

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Sexually transmitted infections (STIs) are a major problem worldwide. In addition, the spectrum of STIs is now expanding, including parasitic, bacterial, and viral infections. The study retrospectively describes the presence of enteric pathogens among 73 patients with gastrointestinal symptoms of enteritis and proctocolitis attending to an STI unit in Barcelona, Spain, between 2015 and 2016. Only patients investigated for intestinal parasitic infections were included in the study. Different diagnostic procedures were established for the detection of parasites, bacterial enteropathogens, and other STI agents. Entamoeba histolytica was the most prevalent pathogen in our cohort (20.5%), especially among individuals with proctocolitis. Contrarily, Giardia intestinalis was detected in 11.0% of patients, only associated with enteritis cases. Polymicrobial infections were common in our study (45.2%). Of note, 55.6% of shigellosis cases were coinfected with E. histolytica. The investigation highlights the importance of including parasites as differential gastrointestinal diagnosis, disregarding travel history, particularly among risk populations.

Since sexual transmission of enteric pathogens was first reported in 1967,1 different publications have described parasitic, bacterial, and viral outbreaks worldwide associated with sexual acquisition, predominantly among men who have sex with men (MSM).25 Thus, several intestinal protozoan infections, previously reported as tropical related, are now recognized also as sexually transmitted infections (STIs). Oral–anal sex, fingering, or fomites are the most common sexual routes of transmission.6,7 In addition, the current diversity of sexual practices, including sex in group often with anonymous partners, the use of drugs during sexual activities, and the rapid geographical mobility of individuals along countries, makes partner notification and spread control especially complicated.6 Although molecular assays have been implemented for the detection of major STIs,8 the diagnosis of parasitic infections remains being based mostly on direct microscopy. Nevertheless, several antigen detection tests for Entamoeba histolytica (EH), Giardia intestinalis (GI), and Cryptosporidium sp. have been recently developed and may play a key role in rapid diagnosis and guided treatment. The main objective of the study was to describe the presence of intestinal parasites and other enteric pathogens among patients with gastrointestinal symptoms attending to a referral STI unit in Barcelona, Spain.

The research was conducted retrospectively among individuals with gastrointestinal symptoms of enteritis or proctocolitis attending to the STI Unit Vall d’Hebron-Drassanes in Barcelona, Spain, between January 2015 and December 2016. Enteritis was considered when large-volume watery diarrhea, abdominal cramps, nausea, malaise, or weight loss was present.9,10 On the other hand, proctocolitis was defined as the presence of milder symptoms of enteritis with additional abdominal tenderness, anorectal bleeding and mucopurulent discharge, or tenesmus.9,10 Only patients investigated for intestinal parasitic infections were systematically included in the study.

Different diagnostic procedures were established according to the medical criteria. Wet mounts for direct microscopic observation of fresh stools and Crypto/Giardia Duo-Strip antigen detection assays (Coris Bioconcepts, Gembloux, Belgium) were used to identify parasites from fecal samples in cases of acute diarrhea. Also, the ELISA Entamoeba CELISA Path (Cellabs, Sydney, Australia) was used for the detection of EH in diarrheal feces or for confirmation of EH-compatible forms at microscopic observation. On the other hand, concentrated stained smears of stool specimens for microscopic examination were performed in all gastrointestinal syndromes for the detection of both pathogenic and commensal protozoa.

In addition, bacterial fecal cultures for Shigella spp., Campylobacter spp., Salmonella spp., and the pathogenic Escherichia coli strains were performed in most cases. Also, real-time polymerase chain reaction techniques were performed for Neisseria gonorrhoeae (NG) and Chlamydia trachomatis (CT) rectal detection, including lymphogranuloma venereum (LGV) genotypes, in most cases.

Sociodemographic and clinical characteristics of the patients were collected through a comprehensive review of the medical record. The Chi-squared tests, or the Fisher exact test when appropriate, were used to compare categorical variables. Mann–Whitney U-tests were performed between continuous variables. Odds ratios (ORs) and their corresponding 95% CIs were calculated when appropriate. Differences with P < 0.05 were considered statistically significant. Ethical approval for the study was obtained from the Vall d’Hebron University Hospital Ethics Committee (approval number 405/2018).

A total of 73 patients were attended for gastrointestinal symptoms during the study period. The clinical and epidemiological characteristics of the study population are summarized in Table 1. All study individuals were MSM (based on the gender of sex partners), of whom 68.5% (95% CI, 56.6–78.9%) were HIV positive.

Table 1

Clinical and epidemiological characteristics of the 73 patients studied, stratified by the presence or absence of parasites

CharacteristicsPatients with intestinal protozoa (n = 43)Patients without intestinal protozoa (n = 30)P-value
No. (%)No. (%)
Median age (interquartile range)37.8 (28.8–44.0)33.5 (27.4–39.7)0.239
HIV infection28 (65.1)22 (73.3)0.458
Syphilis history28 (65.1)16 (53.3)0.313
Travel history* (< 6 months)5 (11.6)4 (13.3)0.827
Previous antimicrobial treatment (< 1 month)2 (4.7)3 (10.0)0.384
Clinical manifestation
 Enteritis34 (79.1)24 (80.0)0.923
 Proctocolitis9 (20.9)6 (20.0)

* Travel to tropical or subtropical regions.

The presence of parasites and other enteric pathogens found in our cohort is described in Table 2. Entamoeba histolytica resulted the most prevalent pathogen (20.5% [95% CI, 12.0–31.6%]), especially among individuals with proctocolitis. On the contrary, GI was detected in 11.0% of patients (95% CI, 4.9–20.5%) and it was only associated with enteritis cases. The prevalence of shigellosis among the study population was 13.0% (95% CI, 6.1–23.3%), more prevalent among proctocolitis cases. Furthermore, the prevalence of the STIs NG and CT was also higher among proctocolitis cases (33.3% [95% CI, 11.8–61.6%]) than the one among enteritis syndromes (17.0% [95% CI, 7.6–30.8%]). It is noteworthy that all CT infections detected among patients with proctocolitis were caused by LGV genotypes.

Table 2

Prevalence of protozoa, enteropathogenic bacteria, and other STI agents in our cohort, stratified by clinical syndrome

MicroorganismPatients with enteritis (n = 58)Patients with proctocolitis (n = 15)P-value
No. (%)No. (%)
Protozoan parasites
Entamoeba histolytica11/58 (19.0)4/15 (26.7)0.510
Giardia intestinalis8/58 (13.8)0/15 (0.0)0.193
Cryptosporidium sp.0/58 (0.0)1/15 (6.7)0.206
Dientamoeba fragilis*3/58 (5.2)1/15 (6.7)0.773
Blastocystis hominis*11/58 (19.0)2/15 (13.3)0.258
 Nonpathogenic protozoa†15/58 (25.9)4/15 (26.7)0.949
Bacterial enteropathogens
Shigella sp.‡7/56 (12.5)2/13 (15.4)0.780
Campylobacter sp.0/56 (0.0)1/13 (7.7)0.188
Escherichia coli spp.§12/56 (21.4)1/13 (7.7)0.253
Other STI agents
Neisseria gonorrhoeae6/47 (12.8)3/15 (20.0)0.488
Chlamydia trachomatis5/47 (10.6)3‖/15 (20.0)0.346

STI = sexually transmitted infection.

* Unclear pathogenic potential.

† The nonpathogenic protozoa include the following: other Entamoeba sp., Endolimax nana, Iodamoeba bütschlii, Trichomonas hominis, and Chilomastix mesnilii.

Shigella flexneri was the most common specie in our cohort accounting for seven cases, whereas only two were caused by Shigella sonnei.

§ Nine E. coli syndromes were caused by enteropathogenic (EPEC) strains, three by enterotoxigenic (ETEC), and one by enteroinvasive (EIEC).

‖ Lymphogranuloma venereum genotype.

Polymicrobial infections were detected in 33 cases (45.2% [95% CI, 33.5–57.3%]), with no differences between syndromes (8/15 among proctocolitis versus 25/58 among enteritis cases; P = 0.478). Figure 1 shows the frequency of coinfections by microorganism among the 59 cases investigated simultaneously for parasites, bacterial enteropathogens, and other STI agents. Prominently, in five shigellosis cases (55.6% [95% CI, 21.2–86.3%]), EH was also detected.

Figure 1.
Figure 1.

Coinfection heat map. The graph shows the frequency of coinfections by microorganism among the 59 cases simultaneously investigated for parasites, bacterial enteropathogens, and other sexually transmitted infection agents. CT = Chlamydia trachomatis; NG = Neisseria gonorrhoeae.

Citation: The American Journal of Tropical Medicine and Hygiene 101, 6; 10.4269/ajtmh.19-0312

Univariate analyses were used to examine the relationships between the baseline characteristics of the study population and the presence of amebiasis. No significant associations between EH infection, age (P = 0.616), and HIV status (9/15 patients infected with EH were HIV positive versus 41/58 among noninfected individuals; P = 0.429) were found. On the other hand, despite not reaching significance, syphilis history (12/15 versus 32/58; OR 3.3 [95% CI, 0.8–12.8], P = 0.091) and tropical/subtropical travel history in the last 6 months (4/15 versus 5/58; OR 3.9 [95% CI, 0.9–16.8], P = 0.071) resulted associated with EH infection.

In cases of acute diarrhea at medical examination, wet mounts of fresh stool for direct microscopical examination and rapid stool antigen detection assays for GI and Cryptosporidium sp. were performed. Among GI-infected individuals, six (75.0% [95% CI, 34.9–96.8%]) presented diarrhea at the time of consultation. All six cases (100.0% [95% CI, 54.1–100.0]) resulted positive for giardiasis by, both, stool antigen detection and wet mounts. On the other hand, 13 positive EH cases by ELISA had acute diarrhea at medical examination (92.9% [95% CI, 66.1–99.8%]), but fresh stool examination detected amebas in only six cases (46.2% [95% CI, 19.2–74.9%]).

In our cohort, all symptomatic individuals recruited were MSM, of whom 68.5% were HIV positive. Men who have sex with men remain, indeed, at a higher risk for STIs in comparison to other populations.11 In addition, previous investigations have suggested that sexual risk behaviors may have increased among HIV-positive patients, likely because of the introduction of highly active antiretroviral therapy (HAART) and the absence of HIV transmission once undetectable, expanding the prevalence of STIs, including intestinal parasites, in this subpopulation.9,12 This fact may account for the notable prevalence of HIV-infected MSM in our cohort. Of note, information regarding CD4 count, viral load, or HAART is missing among HIV-infected participants.

Despite protozoan infections are frequently asymptomatic and self-limited, they can also cause intestinal symptoms. We found EH to be the most prevalent pathogen, especially among individuals with proctocolitis. Although the prevalence of EH among general population in non-endemic areas is low,13 amebiasis has become a major concern in MSM. Because protozoans are transmitted by the fecal–oral route, direct or indirect oral–anal sex is considered the main reason for the increased rates of EH carriage in this population.9 History of syphilis, a marker of risky sexual behavior, and recent travel to tropical/subtropical regions were associated with amebiasis in our cohort, although not reaching significance. These risk factors have been similarly correlated with the presence of protozoan infections in previous reports.9 Giardia intestinalis, also notably prevalent in our study population (11.0%), was only present in cases of enteritis. In fact, the affinity of this protozoan to cause inflammation of the small intestine rather than proctitis symptoms is well established.9,10,14 Because EH and GI need a very low infective dose (10–100 cysts), they are both more likely to be sexually transmitted. Dientamoeba fragilis and Blastocystis hominis are only occasionally implicated in diarrhea in humans.15,16 These parasites and other commensal protozoan were frequent in our cohort (26.0%), mostly as concomitant findings. Despite the unclear clinical impact of these microorganisms, their presence indicates fecal contamination and, as a consequence, strongly supports a vigorous search for pathogens in additional samples.17,18 The low prevalence of cryptosporidiosis in our study (1.4%), strongly associated with MSM suffering from AIDS, is consistent with a generally well-controlled HIV population in developed countries because of the use of HAART.19

In sexually related gastrointestinal syndromes, polymicrobial infections are common, particularly in proctocolitis cases.20 Thus, almost half of the individuals studied (45.2%) harbored polymicrobial infections. It is remarkable that in 55.6% of shigellosis cases, EH was also detected. Because both organisms share human niche (colon) and probable syndrome (proctocolitis), these pathogens should be screened in case of gastrointestinal syndromes. Neisseria gonorrhoeae and CT infections likely contributed little to symptoms and they may mostly represent an asymptomatic carriage found during STI screening in our study population. Nevertheless, it is important to consider both rectal infections in individuals reporting receptive condomless anal intercourse as part of the routine STI screening, particularly in the presence of gastrointestinal symptoms.10

Some limitations to our report must be addressed. First of all, because of the retrospective design of the study, sociodemographic and clinical registrations might be missing. In addition, because the record of these data relies on the clinician, information may be susceptible to misreporting. It is also important to point that sexual transmission of the intestinal pathogens is presumed because patients were attended to the STI unit referring sexual risk behaviors; nevertheless, other routes of spread cannot be discarded. Finally, only individuals investigated for intestinal parasites were incorporated to the research. Thus, certain risk groups such as MSM or HIV-positive individuals may be overrepresented, whereas some other patients with gastrointestinal symptoms may have been excluded, biasing the incidence of protozoan infections in our study population.

In conclusion, the study manages to explore the presence of intestinal parasites and other enteric pathogens among MSM with presumptive sexually acquired gastrointestinal infections attending to an STI unit in Barcelona, Spain. Among individuals reporting sexual risk activities, the differential diagnosis of gastrointestinal disease should include parasites disregarding travel history, especially in MSM. In addition, the use of rapid techniques, such as stool antigen detection assays or wet mounts, may be helpful in STI units for a rapid diagnosis and management of parasitic gastrointestinal infections. Although sexual transmission of intestinal parasites is well known in specialized STI units, general practitioners may not be fully aware of this route of spread with the consequent underdiagnosis of these infections. Additional screening of further STIs should be offered to individuals reporting sexual risk conducts. Furthermore, a proper sexual education, especially hygienic measures, in these risk populations may control reinfection and sexual spread of intestinal protozoan infections.

Acknowledgments:

We thank the staff of the laboratory and STI Unit, Vall d’Hebron-Drassanes, particularly the nursing team, for their essential work. We also thank the Microbiology Department of the Vall d’Hebron University Hospital.

REFERENCES

  • 1.

    Most H, 1968. Manhattan: a tropic isle? Am J Trop Med Hyg 17: 333354.

  • 2.

    Escolà-Vergé L, Arando M, Vall M, Rovira R, Espasa M, Sulleiro E, Armengol P, Zarzuela F, Barberá MJ, 2017. Outbreak of intestinal amoebiasis among men who have sex with men, Barcelona (Spain), October 2016–January 2017. Euro Surveill 22: 30581.

    • Search Google Scholar
    • Export Citation
  • 3.

    Okame M et al. 2012. Shigella sonnei outbreak among men who have sex with men in Tokyo. J Infect Dis 65: 277278.

  • 4.

    Rodríguez-Tajes S, Perpiñán E, Caballol B, Lens S, Mariño Z, Costa J, Vilella A, Pérez-Del-Pulgar S, Forns X, Koutsoudakis G, 2018. Hepatitis A outbreak in Barcelona among men who have sex with men (MSM), January–June 2017: a hospital perspective. Liver Int 38: 588593.

    • Search Google Scholar
    • Export Citation
  • 5.

    Baker RW, Peppercorn MA, 1982. Gastrointestinal ailments of homosexual men. Medicine (Baltimore) 61: 390405.

  • 6.

    Ortega HB, Borchardt KA, Hamilton R, Ortega P, Mahood J, 1984. Enteric pathogenic protozoa in homosexual men from San Francisco. Sex Transm Dis 11: 5963.

    • Search Google Scholar
    • Export Citation
  • 7.

    Centers for Disease Control, 1981. Amebiasis associated with colonic irrigation: Colorado. MMWR Morb Mortal Wkly Rep 30: 101.

  • 8.

    Whitlock GG, Gibbons DC, Longford N, Harvey MJ, McOwan A, Adams EJ, 2018. Rapid testing and treatment for sexually transmitted infections improve patient care and yield public health benefits. Int J STD AIDS 29: 474482.

    • Search Google Scholar
    • Export Citation
  • 9.

    Abdolrasouli A, McMillan A, Ackers JP, 2009. Sexual transmission of intestinal parasites in men who have sex with men. Sex Health 6: 185194.

    • Search Google Scholar
    • Export Citation
  • 10.

    de Vries HJ, Zingoni A, White JA, Ross JD, Kreuter A, 2014. 2013 European guideline on the management of proctitis, proctocolitis and enteritis caused by sexually transmissible pathogens. Int J STD AIDS 25: 465474.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mohammed H, Mitchell H, Sile B, Duffell S, Nardone A, Hughes G, 2016. Increase in sexually transmitted infections among men who have sex with men, England, 2014. Emerg Infect Dis 22: 8891.

    • Search Google Scholar
    • Export Citation
  • 12.

    Stark D, Fotedar R, van Hal S, Beebe N, Marriott D, Ellis JT, Harkness J, 2007. Prevalence of enteric protozoa in human immunodeficiency virus (HIV)–positive and HIV–negative men who have sex with men from Sydney, Australia. Am J Trop Med Hyg 76: 549552.

    • Search Google Scholar
    • Export Citation
  • 13.

    Calderaro A, Montecchini S, Rossi S, Gorrini C, De Conto F, Medici MC, Chezzi C, Arcangeletti MC, 2014. Intestinal parasitoses in a tertiary–care hospital located in a non-endemic setting during 2006–2010. BMC Infect Dis 14: 264.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ali SA, Hill DR, 2003. Giardia intestinalis. Curr Opin Infect Dis 16: 453460.

  • 15.

    Stark D, Beebe N, Marriott D, Ellis J, Harkness J, 2005. Prospective study of the prevalence, genotyping, and clinical relevance of Dientamoeba fragilis infections in an Australian population. J Clin Microbiol 43: 27182723.

    • Search Google Scholar
    • Export Citation
  • 16.

    Sheehan DJ, Raucher BG, McKitrick JC, 1986. Association of Blastocystis hominis with signs and symptoms of human disease. J Clin Microbiol 24: 548550.

    • Search Google Scholar
    • Export Citation
  • 17.

    William DC, Shookhoff HB, Felman YM, DeRamos SW, 1978. High rates of enteric protozoal infections in selected homosexual men attending a venereal disease clinic. Sex Transm Dis 5: 155157.

    • Search Google Scholar
    • Export Citation
  • 18.

    Salvador F, Sulleiro E, Sánchez-Montalvá A, Alonso C, Santos J, Fuentes I, Molina I, 2016. Epidemiological and clinical profile of adult patients with Blastocystis sp. infection in Barcelona, Spain. Parasit Vectors 9: 548.

    • Search Google Scholar
    • Export Citation
  • 19.

    Pozio E, Morales MA, 2005. The impact of HIV-protease inhibitors on opportunistic parasites. Trends Parasitol 21: 5863.

  • 20.

    Quinn TC, Stamm WE, Goodell SE, Mkrtichian E, Benedetti J, Corey L, Schuffler MD, Holmes KK, 1983. The polymicrobial origin of intestinal infections in homosexual men. N Engl J Med 309: 576582.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Elena Sulleiro, Microbiology Department, Vall d’Hebron University Hospital, Passeig Vall d’Hebron, Barcelona 119-129 08035, Spain. E-mail: esulleir@vhebron.net

Authors’ addresses: Miguel Fernández-Huerta, Francesc Zarzuela, Juliana Esperalba, Virginia Rodríguez, Tomàs Pumarola, Mateu Espasa, and Elena Sulleiro, Microbiology Department, Vall d’Hebron University Hospital, PROSICS Barcelona, Barcelona, Spain, and Universitat Autònoma de Barcelona, Barcelona, Spain, E-mails: miguelferhuer@gmail.com, fzarzuela@vhebron.net, jesperalba@vhebron.net, vrgarrido@vhebron.net, tpumarola@vhebron.net, mespasa@tauli.cat, and esulleir@vhebron.net. María-Jesús Barberá, Infectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain, and University of Barcelona, Barcelona, Spain, E-mail: mjbarberag@gmail.com. Maider Arando, Martí Vall, Vicenç Falcó, and Jorge-Néstor García-Pérez, Infectious Diseases Department, Sexually Transmitted Infections Unit Vall d’Hebron-Drassanes, Vall d’Hebron University Hospital, Barcelona, Spain, and Universitat Autònoma de Barcelona, Barcelona, Spain, E-mails: marando@vhebron.net, mvall.bcn.ics@gencat.cat, vfalco@vhebron.net, and jornega@gmail.com.

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