Clinical Infectious Diseases

SUPPLEMENT ARTICLE

Enteric Infections in Men Who Have Sex With Men

Candice J. McNeil,1 Robert D. Kirkcaldy,2 and Kimberly Workowski2,3
1
Department of Internal Medicine, Section on Infectious Diseases, Wake Forest School of Medicine, Winston Salem, North Carolina, USA; 2Division of STD Prevention, National Center for HIV,
Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia; 3Department of Medicine, Emory University, Atlanta, Georgia

Background.  Enteric pathogens are often associated with exposure to food, water, animals, and feces from infected individuals.

Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022

However, in sexual networks of men who have sex with men (MSM), transmission of enteric pathogens may occur during direct or
indirect oral–anal contact.
Methods.  We performed a scoping review of the literature for studies prior to July 2019 with key terms for gastrointestinal
syndromes (“proctitis,” “enteritis,” “proctocolitis”), enteric pathogens or sexually transmitted infections (STIs), and outbreaks using
multiple electronic databases.
Results.  We identified 5861 records through database searches, bibliography reviews, and keyword searches, of which 117 refer-
ences were included in the pathogen-specific reviews.
Conclusions.  The strength of observational data describing enteric pathogens in MSM and possible sexual transmission of en-
teric pathogens varies by pathogen; however, a robust body of literature describes the sexual transmission of Campylobacter, Giardia
lamblia, and Shigella (particularly antimicrobial-resistant strains) in sexual networks of MSM. Providers are encouraged to consider
enteritis or proctocolitis in MSM as possibly having been sexually transmitted and encourage targeted STI testing. Risk/harm re-
duction and prevention messages should also be incorporated, though there is an acknowledged paucity of evidence with regards to
effective strategies. Further research is needed to understand the transmission and prevention of enteric pathogens in MSM.
Keywords.  enteric diseases; men who have sex with men; sexual transmission.

Infection with enteric pathogens, acquired through exposure to
contaminated food and water, animals or their surroundings,
and feces of infected persons, can cause diarrheal illness and
other gastrointestinal syndromes. These syndromes include
proctocolitis (mucosal inflammation extending to 12 cm above
the anus and associated with anorectal pain and discharge, te-
nesmus, and diarrhea or abdominal cramps) and enteritis (the
presence of diarrhea and abdominal cramps and the absence of
symptoms associated with inflammation at the distal portion of
the rectum/proctitis and proctocolitis) [1]. Foodborne patho-
gens are estimated to cause 9.4 million episodes of foodborne
illness, nearly 56  000 hospitalizations, and 1351 deaths each
year in the United States [2].
Although less frequently recognized as a transmission route,
person-to-person transmission of enteric pathogens during sex
is known to occur, such as through direct (anilingus [or rim-
ming]) or indirect oral–anal sexual contact. The risk for infec-
tion with enteric pathogens during sex may be heightened by
human immunodeficiency virus (HIV), increased numbers of
sexual partners, lack of sexually transmitted infection (STI)
Correspondence: Candice J. McNeil, Department of Internal Medicine, Section on Infectious
Diseases, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC
27157 (cmcneil@wakehealth.edu).
Clinical Infectious Diseases®  2022;74(S2):S169–78
© The Author(s) 2022. Published by Oxford University Press for the Infectious Diseases Society
of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com.
https://doi.org/10.1093/cid/ciac061
prevention practices, high transmissibility of enteric pathogens,
and substance use disorder [3, 4]. Concurrency of STIs, such
as chlamydia and gonorrhea, may be associated with additional
morbidity in gay, bisexual, and other men who have sex with
men (MSM) with sexually acquired enteric pathogen infections
[5, 6]. Although published data are scarce, available data suggest
that rimming may be commonly practiced by sexually active
MSM who attend sexual health clinics and may facilitate the
transmission of STIs [7]. MSM may thus be at heightened risk
for sexual transmission of enteric pathogens.
Understanding the potential for sexual transmission of en-
teric pathogens among MSM may support enteric disease con-
trol efforts and spur improvements in sexual health clinical
services for MSM. To these ends and to identify gaps in the lit-
erature, we reviewed existing literature that examined enteric
pathogens among MSM and, when available, possible sexual
transmission of enteric pathogens among MSM.
METHODS
We conducted a scoping literature review of published studies
using PubMed, Cochrane, Embase, and CINAHL through 9
July 2019. Year limits were not set for the search. Databases were
searched using key terms for gastrointestinal syndromes (“proc-
titis,” “enteritis,” “proctocolitis”), enteric pathogens or STIs, and
outbreaks with the assistance of a reference librarian. Complete
search strategies can be found in the Supplementary Materials.
Abstracts available in English were reviewed by 1 author (C. J.

Enteric Infections in MSM • CID 2022:74 (Suppl 2) • S169

M.) and, if relevant, were selected for a more detailed review of
the article. All retrieved citations were provided in an Endnote
reference file; search outputs were combined by pathogen; du-
plicates were identified using EndNote automated “find dupli-
cates” function with preference set to match on title, author, and
year along with a manual review. Abstracts were removed from
consideration if content was in a language other than English;
content was categorized as a conference abstract, conference
proceeding, or review article; or content was not relevant to the
research question. Full text articles were reviewed to confirm
subject relevance. A secondary review of the bibliographies and
discussion with experts in the field identified additional sources
for review (C. J. M. and R. D. K.). We focused on sexual trans-
mission of enteric pathogens; we did not explore gastrointes-
tinal syndromes caused by traditional STIs, such as proctitis
from lymphogranuloma venereum, genital herpes, or Neisseria
gonorrhoeae.
RESULTS
We identified 5732 records through database searches and an
additional 129 records through review of bibliographies and
recommendations by experts in the field. A total of 5744 ref-
erences were excluded due to content in a language other than
English; content categorized as a conference abstract, con-
ference proceeding, or review article; or content that was not
relevant to the research question. The remaining 117 full text
articles were reviewed and included in the pathogen-specific
summaries.
PATHOGENS THAT CAUSE PROCTOCOLITIS
Campylobacter: Campylobacteriosis
Campylobacter sp. are responsible for an estimated 1.3 mil-
lion illnesses each year in the United States [2]. The majority
of Campylobacter cases in the United States are caused by
Campylobacter jejuni. Other species with clinical relevance in
humans include Campylobacter coli, Campylobacter concisus,
Campylobacter curvus, Campylobacter fetus, Campylobacter
gracilis, Campylobacter hominis, Campylobacter helveticus,
Campylobacter hyointestinalis, Campylobacter insulaenigrae,
Campylobacter lari, Campylobacter mucosalis, Campylobacter
rectus, Campylobacter showae, Campylobacter sputorum,
Campylobacter upsaliensis, and Campylobacter ureolyticus [8].
Infection with Campylobacter sp. causes watery or bloody di-
arrhea, fever, abdominal cramps, and weight loss of variable
severity [8]. Diagnosis can be made by culture and culture-
independent diagnostic tests, such as polymerase chain reaction
(PCR). If treatment is indicated, macrolides are often the anti-
biotic of choice [9]. However, consideration of local resistance
patterns can guide therapy, as resistance to fluoroquinolones
and macrolides is a growing concern, particularly for infections
among MSM and persons living with HIV [10–15]. Virologic
S170 • CID 2022:74 (Suppl 2) • McNeil et al
control of HIV infection may reduce the risk of recurrent infec-
tions with Campylobacter sp. [15].
Campylobacter sp. have been associated with symptomatic
and asymptomatic anorectal or intestinal disease in MSM
[16–20]. Infrequently, Campylobacter species can cause bacte-
remia and severe extraintestinal infections [8]; persons living
with HIV may experience complications and severe prolonged
infections [10, 21]. Marchand-Senécal et al [21] described a
cluster of community-acquired C. fetus in Quebec involving
13 men (12 MSM), 8 of whom were known to be living with
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
HIV. Three of the men experienced bacteremia complicated by
ruptured aortic aneurysm (n = 2) and hemorrhagic renal cyst
(n = 1); all had significantly more comorbid conditions and
disease severity than those with gastroenteritis. Notably, indi-
viduals living with HIV (1 of 3 men with bacteremia and 7 of
9 men with gastroenteritis) were not more likely to experience
complications in this study.
Outbreaks of Campylobacter infections are commonly asso-
ciated with consumption of unpasteurized dairy products; con-
taminated poultry, produce, and water; and person-to-person
transmission (possibly during sex) and outbreaks. However,
there have been outbreaks where these classic exposures have
not been identified among MSM. Gaudreau et al [11, 13] re-
ported outbreaks of C. jejuni infections in Quebec, Canada,
among MSM who did not share common food sources.
Outbreaks of C. coli were also reported in MSM during an
overlapping timeframe where recent sexual exposure was re-
ported in addition to reports of condomless sex and visits to
bathhouses or sex clubs in some of the men [12, 14]. Similarly,
Marchand-Senécal et al [21] noted that 12 of 13 men identi-
fied in a C. fetus cluster investigation reported sexual contact
with men, 11 reported high-risk sexual behaviors including
frequenting gay male sexual venues and meeting partners on
the internet during the incubation period for C. fetus infec-
tion, and 7 of the 13 were documented with 30 STIs other than
HIV within 3 years of their Campylobacter infection. Quinn et
al [22] found that a greater percentage of MSM infected with
Campylobacter species (76.9%) or Campylobacter-like organ-
isms (74.2%) engaged in anilingus in the prior month compared
with those without enteric infections (54.9%; P < .05). In sev-
eral of these reports, sexually transmitted infections including
HIV, N. gonorrhoeae, Chlamydia trachomatis, C. trachomatis
lymphogranuloma venereum serovars, Treponema pallidum,
and other enteric pathogens were identified among MSM diag-
nosed with Campylobacter [11–14, 21].
Entamoeba histolytica: Amebiasis
Entamoeba histolytica (EH), a pathogenic amoeba, is a leading
cause of diarrheal disease globally, contributing to millions of
cases annually [23]. Infections typically occur in individuals
living in endemic regions, travelers from endemic regions,
and those living in settings where hygiene and sanitation are
insufficient [23]. The majority of patients are asymptomatic;
when symptoms occur, they often include mild diarrhea and
abdominal cramping. However, EH can cause bloody diarrhea
(dysentery), extraintestinal manifestations, and fulminant di-
sease [23]. Though some studies suggest that EH serves as a
commensal pathogen in MSM [24, 25], others have described
significant morbidity associated with EH infections in high-
risk groups [23, 26–29]. Persons living with HIV may be at in-
creased risk for EH infection [30] and associated complications,
including invasive disease [26–29].
Acknowledging that symptoms alone may not reliably pre-
dict the presence of sexually transmitted enteric infections, the
role of diagnostics for men who present with gastrointestinal
symptoms to confirm the diagnosis and support targeted treat-
ment cannot be overstated. Molecular testing remains the most
reliable diagnostic and has become the gold standard in EH di-
agnosis, though the cost is prohibitive in low-resource settings.
A combination of testing modalities is often used to make the
diagnosis of EH. Direct visualization via microscopy, though
widely used, has poor sensitivity and specificity and cannot re-
liably distinguishing EH from other intestinal protozoa [23]. As
an adjunct to stool studies, serologies exhibit high sensitivity
and specificity and are used in the diagnosis of extraintestinal
disease where stool studies may be negative. Notably, these
tests cannot distinguish between current and past infections
[23]. Treatment of symptomatic and asymptomatic infec-
tions is recommended; treatment of asymptomatic infections
can minimize transmission and development of sympto-
matic disease [23]. Those with clinical disease require both an
amebicidal tissue-active agent and a luminal cysticidal agent.
Recommended treatments include metronidazole or tinidazole,
iodoquinol, or paromomycin [23].
Sexual transmission of EH has been reported to occur in
heterosexual and same-sex couples. Salit et al [31] described
a possible cluster of EH cases with the aid of genotyping and
phylogenetic analysis in a sexual network that included female
same-sex and opposite-sex partners where oral–anal sex was
the common exposure. In several industrialized countries, high
morbidity from EH has been reported in MSM communities. In
their study of EH in Taiwanese MSM living with HIV, Hung et al
[32] noted that same-sex partnerships among men were associ-
ated with EH infection (positive serology or antigen and PCR).
Additionally, they used genomic analysis to find that clusters
of EH occurred in geographically unrelated patients, suggesting
that person-to-person transmission may be occurring. Quinn
et al reviewed the etiology of anorectal infections in MSM and
reported a case of EH anorectal infection with stool wet mount
positive for EH trophozoites and stool studies positive for EH
and giardia cysts in MSM with no travel risk factors and who
reported anilingus and receptive anal sex. Stool examination of
his sex partners revealed EH cysts, suggesting sexual transmis-
sion [16]. EH is reported to be a cause of symptomatic anorectal
or intestinal disease in MSM [16, 17]. Outbreaks of EH among
MSM have been described in Canada [33], the United States
[34, 35], and Spain [36]. There have also been case reports of
MSM with EH presumed to be sexually transmitted [27, 28, 37–
42]. The affected MSM had a sexual exposure and/or seemed
to lack traditional EH risk factors. Direct oral–anal sexual con-
tact, such as anilingus, and indirect contact, such as fellatio
after anal–genital intercourse, are significantly associated with
EH among MSM [17, 43–48]. Direct rectal inoculation through
receptive anal sex has also been reported [49]. A wide range
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
of EH test positivity has been observed among MSM (from as
low as 0.2% to as high as 47%), with variation by region, indi-
vidual risk behavior, and HIV status [17, 30, 43, 45–47, 49–68].
Concurrent enteric pathogens [25, 56, 69] and sexually trans-
mitted infections [25, 27, 35, 36, 44, 48] with EH infection have
been reported.
Shigella
Shigella accounts for an estimated 500 000 cases of shigellosis
annually in the United States [2], with serogroups including
Shigella sonnei, Shigella flexneri, Shigella boydii, and Shigella
dysenteriae. The typical onset of symptoms is 1–4 days following
exposure but may be longer. Shigella causes the abrupt onset
of bloody diarrhea, fever, abdominal pain, tenesmus, and ma-
laise [70]. Shigella is highly transmissible, requiring fewer than
10 organisms to cause infection [71]. Persons living with HIV
may be more likely to experience severe manifestations of infec-
tion [15]. Diagnosis is based on culture or, increasingly, PCR.
However, culture is the mainstay diagnostic test for species-
level identification and antimicrobial susceptibility testing to
guide therapy [70]. Because shigellosis is often self-limiting,
treatment is not always required. Immunocompromised per-
sons, such as those living with HIV, should be treated as it may
shorten the duration of illness and decrease infectivity. When
empiric therapy is indicated, a fluoroquinolone is the treatment
of choice [15]. However, antimicrobial selection is complicated
by the emergence of bacterial strains resistant to ampicillin and
trimethoprim and, most recently, to azithromycin, ceftriaxone,
and ciprofloxacin. These resistance patterns have been re-
ported among MSM and persons living with HIV infection
[72–79]. Moreover, returning travelers might harbor resistance
to many of the common antibiotics used to treat Shigella [15,
80]. Consideration of resistance patterns (local and destination
country), host factors, and the severity of illness are necessary
to guide treatment type and duration [9, 15, 72, 80].
Recent increases in incident cases of Shigella among adult
men have been described in the United States and might be
associated with transmission among MSM [81]. Outbreak and
surveillance studies of Shigella among MSM have been identi-
fied in Amsterdam [82], Australia [83–85], Canada [33, 86–90],
Germany [91], Taiwan [77, 92], the United Kingdom [93–99],
and the United States [5, 34, 75, 76, 100–104]. Intercontinental
Enteric Infections in MSM • CID 2022:74 (Suppl 2) • S171
spread among MSM has also been described [105]. Case re-
ports have described Shigella infections in MSM associated
with oral–anal [106] and oral–genital transmission [83] and
in the absence of traditional risk factors for disease transmis-
sion, suggesting sexual transmission. Several observational
studies have documented biologic, behavioral, and social
factors associated with shigellosis infections. Homelessness
[104], substance use disorder [6, 95, 97], and having met
partners through facilitators of casual sexual connections in-
cluding sex venues [84, 97, 107] have also been associated with
shigellosis in MSM. Coinfection with STIs including chla-
mydia, gonorrhea, hepatitis C, HIV, EH, and giardia among
MSM with Shigella within the United States and Europe has
also been described [5, 6, 20, 37, 69, 108]. Investigators in San
Francisco, California, found that direct anal contact (such as
anilingus) with a sexual partner (adjusted odds ratio [aOR],
9.56; 95% confidence interval [CI], 1.69–54.0) and living with
HIV (aOR, 8.59; 95% CI, 2.56–28.9) were independently asso-
ciated with shigellosis in MSM [5]. The frequency of contact
and other specific types of anal contact, such as fingering, in-
strumentation, and insertion of the penis, may also play a role
in the occurrence of shigellosis [5]. Keay et al [109] have also
described Shigella enteritis in a large population of persons re-
ceiving HIV care in the United Kingdom where the majority
of cases were identified in MSM (92%). Among the MSM with
Shigella enteritis for whom a sexual history was available, 58%
had at least 1 casual partner in the last month, the majority
recalled oral–anal contact (62%), and 33% reported insertive
and/or receptive oral sex [109]. In a population-based case-
control study of MSM living with and without HIV in Taiwan,
Wu et al found that high HIV viral load (aOR, 4.9; 95% CI,
1.4–16.9), gonorrhea (aOR, 29.4; 95% CI, 2.3–340.2), and
syphilis (aOR, 4.3; 95% CI, 1.6–11.6) were independent risk
factors for shigellosis. Behavioral factors such as oral–anal sex
(aOR, 15.5; 95% CI, 3.6–66.7), chem sex (aOR, 5.6; 95% CI,
1.4–22.7), and the use of poppers (aOR, 10.9; 95% CI, 1.9–
64.2) in the last 12 months were found to be independent risks
for shigellosis [108].
PATHOGENS THAT CAUSE ENTERITIS
Giardia lamblia: Giardiasis
Giardia lamblia is the most common intestinal parasite in the
United States; approximately 1.2 million illnesses attributable
to giardiasis occur in the United States annually [2]. Although
most infections are asymptomatic, infections with G. lamblia
can cause diarrhea, malabsorption, abdominal cramps, nausea,
and dehydration within approximately 1–2 weeks after infec-
tion. Complications of chronic infection include reactive ar-
thritis and irritable bowel syndrome [110]. Diagnosis is made
by direct visualization, EIA, or PCR [9]. Treatment options in-
clude tinidazole, nitazoxanide, or metronidazole [9].
S172 • CID 2022:74 (Suppl 2) • McNeil et al
Older studies suggested possible sexual transmission of gi-
ardiasis among MSM [50–52, 111, 112]. Although there are
limited data on specific sexual acts associated with giardiasis
in MSM, Esfandiari et al [113] reported anal–penile sex to be
significantly associated with the presence of giardia (OR, 2.9;
P = .017); Markell et al [55] found giardia related to oral–anal
sex (P < .001); Phillips et al [43] identified oral–anal sex as a
significant predictor of G. lamblia infection among MSM; and
William et al [50] and Levinson et al [57] found enteric pro-
tozoal infections associated with specific sexual behaviors.
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
Polymicrobial infections have been reported in MSM with pro-
tozoal infections [19, 37, 50, 56, 58]. The presence of protozoal
cysts has been noted in persons with a prior history of gonor-
rhea (P < .02) infection [44].
Cystoisospora
Cystoisospora belli (formerly Isospora belli) is a microscopic par-
asite that can cause infection through indirect contact with fecal
contaminated food and/or water. Symptoms include low-grade
fever, watery diarrhea, abdominal pain, cramping, anorexia,
nausea, and vomiting [15]. Immunocompromised hosts may be
at risk for debilitating disease including persistent or chronic di-
arrhea leading to dehydration, electrolyte disturbances, weight
loss, and malabsorption. Extra intestinal manifestations have
also been reported [15]. This infection is diagnosed using a
modified acid-fast stain performed on a concentrated specimen,
ultraviolet fluorescence microscopy, or nucleic acid amplifica-
tion testing (NAAT). The treatment of choice is trimethoprim-
sulfamethoxazole; pyrimethamine is an alternative option [9].
Oral–anal contact with an infected person has been proposed
as a mode of transmission. Case reports of C. belli among MSM,
with sexual contact as the presumptive mode of transmission,
have been reported [114, 115].
Cryptosporidium: Cryptosporidiosis
Cryptosporidium is a protozoal parasite that can cause wa-
tery diarrhea, abdominal cramps, nausea and vomiting, and
extraintestinal manifestations; severe manifestations and pro-
longed disease may occur in immunocompromised individ-
uals [15]. Cryptosporidiosis in humans is commonly caused
by Cryptosporidium hominis, Cryptosporidium parvum, and
Cryptosporidium meleagridis. Transmission may occur through
direct contact with feces from infected humans or animals or
contact with contaminated water [15]. This infection is diag-
nosed using a modified acid-fast stain performed on a concen-
trated specimen, ultraviolet fluorescence microscopy, or NAAT.
The treatment of choice is nitazoxanide. In persons living with
HIV, concomitant use of antiretroviral therapy and subsequent
immune reconstitution may facilitate microbiologic and clinical
response to treatment [9].
Cryptosporidiosis has been associated with infections in
MSM [18, 116–119] and is an AIDS-defining illness [15]. Data
on possible transmission during sexual contact are sparse.
Danila et al [119] described 8 cases identified among MSM
living with HIV in Minneapolis–St. Paul during 2013–2014.
Although transmission by sexual contact was not identified,
no common food, water, or animal exposures were reported.
In a population of persons living with HIV, Pedersen et al [116]
noted that rates of cryptosporidiosis were significantly lower
for intravenous drug users than for MSM and for women com-
pared with men. Sorvillo et al [120] noted that the prevalence
of cryptosporidiosis was higher in persons whose HIV expo-
sure was through sexual contact (3.9%) than among persons
in other HIV exposure categories (2.6%; P < .01). Although
far from definitive, associations between Cryptosporidium and
anal sex and multiple partners have been described. In a small
case-control study of MSM, Hellard et al [118] demonstrated an
association of diarrhea from Cryptosporidium with having had
more than 1 anal sex partner (OR, 6.67; 95% CI, 1.15–38.60;
P = .034). Similarly, Caputo et al [117] found that increased
Cryptosporidium serological response in MSM was positively
associated with the number of sexual partners (P = .04) and re-
ported anal sex (P = .03).
Microsporidia: Microsporidiosis
Microsporidia are a collection of obligate intracellular parasites,
and multiple species are associated with microsporidia infec-
tions in humans [121]. Human microsporidiosis is largely an
opportunistic infection seen in severely immunocompromised
patients with AIDS. Clinical manifestations are varied, in-
cluding diarrheal disease and disseminated infections [15, 121].
Diagnosis is made by morphologic identification using trans-
mission electron microscopy, specialized stains, or PCR [15].
Treatment of microsporidiosis in persons living with HIV in-
volves antiretroviral therapy to restore immune function and
supportive care. Additional consideration of other therapeutic
agents targeted to microsporidia species are discussed in ex-
isting guidelines [15].
Cotte et al [122] found that having male sex partners was in-
dependently associated with microsporidia infections in men
living with HIV. Using a case-control approach, Hutin et al [123]
reported that the risk factors for intestinal microsporidiosis in
persons living with HIV included CD4 lymphocyte count ≤100
cells/mm3 (OR, 6.5; 95% CI, 1–42), swimming in a pool within
the last 12 months (OR, 9.2; 95% CI, 2.1–38.9), and having
sexual contact with other men (OR, 7.6; 95% CI, 1–59.5). In this
study, the presumed modes of transmission were waterborne,
fecal–oral transmission, and sexual contact [123].
Enterobius vermicularis: Enterobiasis
Most human infections with the nematode Enterobius
vermicularis are asymptomatic. When present, symptoms may
include nocturnal anal pruritus, abdominal pain, irritability,
and anorexia. Infection occurs directly or indirectly through
fecal–oral contact [124]. Diagnosis is made by microscopic vis-
ualization of eggs collected from the perianus of an infected
individual or direct visualization of the adult worms at the
perianus. Treatment includes mebendazole, pyrantel pamoate,
or albendazole [125]. Sexual transmission of Enterobius has
been described in MSM in association with sex with an infected
partner [126–128].
Strongyloidiasis
Strongyloides stercoralis, another nematode, is the primary
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
Strongyloides sp. associated with disease in humans. Infection
occurs through contact with soil contaminated with larvae and
through autoinfection. Most infections are asymptomatic; how-
ever, gastrointestinal symptoms can include intermittent diar-
rhea and constipation, abdominal pain, and dyspepsia [129].
Diagnosis is made through direct microscopic visualization
or through immunodiagnostic tests [9]. First-line therapy for
strongyloidiasis is ivermectin [129].
Though rare, person-to-person transmission does occur.
Phillips et al [43] reported Strongyloides spp. and Trichuris
trichiura were significantly associated with oral–anal sex
(P < .05). Sorvillo et al [130] reported S. stercoralis infection in
a man who had sex with men and found that 2 of his male con-
tacts had stool specimens positive for S. stercoralis.
Escherichia coli
More than 300 000 cases of Escherichia coli infections, which cause
gastrointestinal and extraintestinal illnesses, occur in the United
States annually [2]. Diarrheagenic pathotypes of E. coli include
Shiga toxin-producing E. coli/verocytotoxin-producing E. coli/
enterohemorrhagic E. coli, enterotoxigenic E. coli, enteropathogenic
E. coli, enteroaggregative E. coli, enteroinvasive E. coli, and diffusely
adherent E. coli, which may be transmitted through contact with
water, food, animals, or people [131]. Infections are diagnosed by
stool culture, molecular assay, or NAAT [9]. There is no clear ben-
efit associated with antimicrobial treatment [9].
Coinfection of enteroaggregative E. coli with chlamydia has
been reported in a study of MSM, the majority of whom were
asymptomatic. The role of asymptomatic infection in the sexual
transmission of enteric pathogens warrants further review
[20]. Surveillance data from Europe demonstrated a cluster of
verocytotoxin-producing E. coli O117:H7 VT1 among MSM
with no reported food, water, or animal exposures. Unprotected
oral–anal sex, fisting, and coprophilia were reported, suggesting
sexual transmission. Other reported risk behaviors included the
use of geospatial network applications to locate partners, at-
tending sex parties, and substance use approximate to exposure
[132].
Salmonella
An estimated 1.2 million cases of Salmonella occur annually
in the United States [2]. Disease manifestations of Salmonella
Enteric Infections in MSM • CID 2022:74 (Suppl 2) • S173
include gastrointestinal and extraintestinal illness; severity and
presentation of symptoms may vary [9]. Persons living with
HIV are at increased risk for complications from Salmonella
gastroenteritis including bacteremia [15]. Salmonella infections
often occur in humans following ingestion of or contact with
fecally contaminated food or water or contact with raw meat
or poultry [9]. Due to concerns about antimicrobial resistance,
stool culture for antimicrobial susceptibility testing may be pre-
ferred over NAAT [9, 15]. Treatment is not recommended for
individuals with a normal immune system as symptoms are
often self-limiting. Persons living with HIV should be treated
due to morbidity and mortality risk associated with Salmonella
infection. The treatment of choice in persons living with HIV is
a fluoroquinolone. However, local resistance patterns should be
factored into treatment decisions. Virologic control of HIV may
reduce the risk of recurrent infections with Salmonella [15].
Case reports have described acute typhoid fever (caused by
Salmonella typhi) occurring in men who were sexual contacts
of men known to be carriers of S. typhi and in whom no other
risk factors for transmission were found [133]. A cluster of S.
typhi was also described in men with no history of foreign travel
but with the common exposure of sex (oral–anal, oral–genital,
insertive anal, receptive anal, and/or digital–anal) with an in-
fected person [134].
DISCUSSION
Enteric pathogens are primarily transmitted through ingestion
of or contact with food or water contaminated by infected feces.
Because exposure to infected feces can also occur during sex,
multiple enteric pathogens also have the potential for transmis-
sion during sex. Direct (such as rimming) or indirect (such as
fingering or fisting) oral–anal contact during sex may facilitate
person-to-person transmission of enteric pathogens during
sex. The strength of the observational data describing pos-
sible sexual transmission of enteric pathogens varies by path-
ogen. While only limited data are available that suggest sexual
transmission of S. stercoralis, E. vermicularis, and C. belli, a ro-
bust epidemiological literature points toward sexual transmis-
sion of Campylobacter, G. lamblia, and Shigella. Case reports,
case-control studies, and biological plausibility support the role
that direct (anilingus) or indirect (fisting or fellatio after anal–
genital intercourse) sexual oral–anal contact contribute to the
spread of these pathogens.
Increased awareness of possible sexual transmission of en-
teric pathogens may help bridge traditional divides between
clinical care of STIs and diarrheal illnesses and between public
health STI and enteric disease control efforts. Bringing aware-
ness of this possible transmission vehicle to those who provide
clinical care may improve sexual health services and clinical
care for MSM. Clinicians who diagnose and treat persons with
enteric pathogens are encouraged to ascertain a thorough sexual
S174 • CID 2022:74 (Suppl 2) • McNeil et al
history from their patients. A brief sexual history to ascertain
the gender and number of recent sex partners and the type of
recent sexual activities (with a focus on oral–anal contact) may
help clinicians to tailor educational prevention messages and
may inform treatment (in light of Campylobacter and Shigella
antimicrobial resistance among MSM) and decisions whether
to offer HIV and STI screening. All sexually active adults diag-
nosed with an enteric pathogen should be counseled about
prevention of transmission of enteric pathogens during sex
and through other vehicles and include messaging such as the
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
benefits of hand hygiene, avoiding swimming while ill, avoiding
food and water sources that could potentially be contaminated
with fecal material, and avoiding fecal exposure during sex by
cleansing the genitals prior to sex, correct and consistent use
of barrier protection during sex, and avoiding sex with part-
ners actively experiencing diarrhea or recently recovered from
enteric infection. Clinicians are encouraged to consider sexual
transmission of enteric pathogens when evaluating MSM for
enteritis or proctocolitis. It is important to provide relevant edu-
cational prevention messages to patients with diarrheal illnesses
and referral for further clinical evaluation if appropriate diag-
nostics are not readily available. Future research can explore
the intersection of enteric pathogens and STIs/HIV, such as
whether MSM with enteric pathogens are at an increased risk of
HIV acquisition and the benefits of utilizing preexposure pro-
phylaxis as a part of a comprehensive STI/HIV prevention plan.
Knowledge of the potential for sexual transmission of enteric
pathogens may also inform public health approaches to public
health prevention and control. Establishment of standard def-
initions for and approaches to the investigation of sexual trans-
mission of enteric pathogens may advance these efforts [135].
There are limited published data on the efficacy of approaches
to prevent sexual transmission of enteric organisms. In the ab-
sence of objective data, education of affected populations at risk
for the sexual transmission of enteric diseases and risk reduction
strategies that might reduce transmission should be discussed.
This is particularly important as the lack of perceived risk can be
associated with failure to incorporate preventative sexual prac-
tices and environmental measures in MSM at risk for certain en-
teric pathogens [136]. Keystone et al [52] found that cleansing
(bathing or cleansing enemas) before anal sex was correlated
with reduced transmission of enteric pathogens. All sexually
active adults, including MSM, may consider avoiding direct
contact with feces during sex, delaying sex until diarrhea has re-
solved, using barrier protection (condoms during insertive anal
sex, gloves during digital–anal sex and fisting, and dental dams,
natural rubber latex sheets, or a cut-open nonlubricated condom
placed over the anus during anilingus), changing condoms after
anal sex, and performing hand hygiene during and bathing after
sex to reduce the risk of disease transmission. Additionally, ac-
knowledging that transmission events may occur in the context
of substance use disorder [97, 137], risk and harm reduction
strategies may be needed to augment preventative sex practices
and environmental measures. The lack of data on effective pre-
vention approaches, however, highlights an important gap in
knowledge and an opportunity for further research.
It is noteworthy that some Campylobacter and Shigella strains
in MSM have been associated with antimicrobial resistance.
Similarly, the prevalence of antimicrobial-resistant N. gonorrhoeae
isolates in MSM are higher than in men who have sex with women
[138]. Differences in antimicrobial resistance patterns make de-
signing an empiric treatment more challenging. Yet another un-
known is the role of emerging pathogens such as Mycoplasma
genitalium on promoting antimicrobial resistance of rectal mi-
crobiota. Future research to understand factors that contribute
to resistance in MSM and evaluate the likelihood of these micro-
organisms sharing genetic resistance determinants is warranted.
This study was a scoping review, and abstracts that were not
indexed at the time of the review may not have been captured.
We used MeSH terms and keyword searches on multiple plat-
forms; however, it is still possible to have missed relevant ar-
ticles due to misclassifications. We also limited our review to
English-language articles and might have missed relevant arti-
cles if published in a different language. Across cited articles,
the manner by which men were classified as MSM was incon-
sistent; this variation points to the need for better ascertainment
of sexual orientation and gender of sex partner among reported
cases of enteric disease, and greater standardization of how
MSM are classified by public health officials.
Multiple enteric pathogens can be transmitted through sexual
contact. Because oral–anal contact during sex may be common
among sexually active MSM, this population may be dispro-
portionately affected; however, it is also possible that sexual
transmission of enteric pathogens occurs among heterosexual
men and women. Shifts in heterosexual sexual practices, such
as increasing oral–anal or genital–anal sex [139–141], could
conceivably contribute to future shifts in the epidemiology of
sexually transmitted enteric infections. For now, increasing
recognition of sexual transmissibility of enteric pathogens will
improve clinical care and public health prevention efforts for
MSM.
Notes
Acknowledgments. We thank Janine Tillett, Wake Forest University
School of Medicine, Carpenter Medical Library, and Martha Knuth, Stephen
B. Thacker Centers for Disease Control and Prevention (CDC) Library, for
assistance in search strategy development; and Mateusz P. Karwowski, MD,
MPH; Kim Gray, PAC; Amanda Garcia-Williams, PhD; and Katie Fullerton
MPH, for assistance with concept design.
Disclaimer. The findings and conclusions presented here are those of the
author(s) and do not necessarily represent the official position of the CDC.
Financial support. C. J. M. was supported by an intergovernmental per-
sonnel act through the Program Development and Quality Improvement
Branch, CDC Division of STD Prevention, during portions of this review.
Supplement sponsorship. This supplement is sponsored by The Centers
for Disease Control and Prevention.
Potential conflicts of interest. C. J. M. reports grants or contracts paid
to Wake Forest University Health Sciences from the National Institutes of
Health (NIH), Biomedical Advanced Research and Development Authority
(BARDA)/GlaxoSmithKline (GSK), BD, Binx, Cepheid, CDC, Gilead,
Hologic, and National Association of County and City Health Officials
(NACCHO), as well as honoraria from Georgia Family Physicians, Core
Concepts in Health, and the Infectious Diseases Society of America; re-
ports unpaid participation on a data safety monitoring board or advisory
board through the NIH; and reports receipt of supplies from Lupin Ltd paid
to Wake Forest University Health Sciences. All remaining authors: No re-
ported conflicts of interest. All authors have submitted the ICMJE Form for
Disclosure of Potential Conflicts of Interest. Conflicts that the editors con-
sider relevant to the content of the manuscript have been disclosed.
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
References
1. Workowski KA, Bachmann LH, Chan PA, et al. MMWR Morb Mortal Wkly
Rep 2021; 70:1–187. doi: 10.15585/mmwr.rr7004a1. PMID: 34292926; PMCID:
PMC8344968.
2. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the
United States—major pathogens. Emerg Infect Dis 2011; 17:7–15.
3. Weber J. Sexually acquired parasitic infections in homosexual men. Parasitol
Today 1985; 1:93–5.
4. Daskalakis DC, Blaser MJ. Another perfect storm: Shigella, men who have sex
with men, and HIV. Clin Infect Dis 2007; 44:335–7.
5. Aragon TJ, Vugia DJ, Shallow S, et al. Case-control study of shigellosis in San
Francisco: the role of sexual transmission and HIV infection. Clin Infect Dis
2007; 44:327–34.
6. Cresswell FV, Ross S, Booth T, et al. Shigella flexneri: a cause of significant mor-
bidity and associated with sexually transmitted infections in men who have sex
with men. Sex Transm Dis 2015; 42:344.
7. Cornelisse VJ, Fairley CK, Read TRH, et al. Associations between anorectal chla-
mydia and oroanal sex or saliva use as a lubricant for anal sex: a cross-sectional
survey. Sex Transm Dis 2018; 45:506–10.
8. Kaakoush NO, Castano-Rodriguez N, Mitchell HM, Man SM. Global epidemi-
ology of Campylobacter infection. Clin Microbiol Rev 2015; 28:687–720.
9. Shane AL, Mody RK, Crump JA, et al. 2017 Infectious Diseases Society of
America clinical practice guidelines for the diagnosis and management of infec-
tious diarrhea. Clin Infect Dis 2017; 65:1963–73.
10. Perlman DM, Ampel NM, Schifman RB, et al. Persistent Campylobacter jejuni
infections in patients infected with the human immunodeficiency virus (HIV).
Ann Intern Med 1988; 108:540–6.
11. Gaudreau C, Michaud S. Cluster of erythromycin- and ciprofloxacin-resistant
Campylobacter jejuni subsp. jejuni from 1999 to 2001 in men who have sex with
men, Quebec, Canada. Clin Infect Dis 2003; 37:131–6.
12. Gaudreau C, Helferty M, Sylvestre JL, et al. Campylobacter coli outbreak in men
who have sex with men, Quebec, Canada, 2010-2011. Emerg Infect Dis 2013;
19:764–7.
13. Gaudreau C, Rodrigues-Coutlée S, Pilon PA, Coutlée F, Bekal S. Long-lasting out-
break of erythromycin- and ciprofloxacin-resistant Campylobacter jejuni subspe-
cies jejuni from 2003 to 2013 in men who have sex with men, Quebec, Canada.
Clin Infect Dis 2015; 61:1549–52.
14. Gaudreau C, Pilon PA, Sylvestre JL, Boucher F, Bekal S. Multidrug-resistant
Campylobacter coli in men who have sex with men, Quebec, Canada, 2015. Emerg
Infect Dis 2016; 22:1661–3.
15. Panel on Opportunistic Infections in Adults and Adolescents with HIV.
Guidelines for the prevention and treatment of opportunistic infec-
tions in adults and adolescents with HIV: recommendations from the
Centers for Disease Control and Prevention, the National Institutes of
Health, and the HIV Medicine Association of the Infectious Diseases
Society of America. Available at: https://clinicalinfo.hiv.gov/en/guidelines/
adult-and-adolescent-opportunistic-infection/.
16. Quinn TC, Corey L, Chaffee RG, Schuffler MD, Brancato FP, Holmes KK.
The etiology of anorectal infections in homosexual men. Am J Med 1981;
71:395–406.
17. Quinn TC, Stamm WE, Goodell SE, et al. The polymicrobial origin of intestinal
infections in homosexual men. N Engl J Med 1983; 309:576–82.
18. Laughon BE, Druckman DA, Vernon A, et al. Prevalence of enteric pathogens
in homosexual men with and without acquired immunodeficiency syndrome.
Gastroenterology 1988; 94:984–93.
19. Rompalo AM, Roberts P, Johnson K, Stamm WE. Empirical therapy for the man-
agement of acute proctitis in homosexual men. JAMA 1988; 260:348–53.
20. Hughes G, Silalang P, Were J, et al. Prevalence and characteristics of gastrointes-
tinal infections in men who have sex with men diagnosed with rectal chlamydia
infection in the UK: an “unlinked anonymous” cross-sectional study. Sex Transm
Infect 2018; 94:518–21.
Enteric Infections in MSM • CID 2022:74 (Suppl 2) • S175
 21. Marchand-Senécal X, Bekal S, Pilon PA, Sylvestre JL, Gaudreau C. Campylobacter
fetus cluster among men who have sex with men, Montreal, Quebec, Canada,
2014-2016. Clin Infect Dis 2017; 65:1751–3.
22. Quinn TC, Goodell SE, Fennell C, et al. Infections with Campylobacter jejuni
and Campylobacter-like organisms in homosexual men. Ann Intern Med 1984;
101:187–92.
23. Shirley D-AT, Farr L, Watanabe K, Moonah SA. Review of the global burden, new
diagnostics, and current therapeutics for amebiasis. Open Forum Infect Dis 2018;
5:ofy1–61-ofy.
24. Allason-Jones E, Mindel A, Sargeaunt P, Williams P. Entamoeba histolytica as a
commensal intestinal parasite in homosexual men. N Engl J Med 1986; 315:353–6.
25. Allason-Jones E, Mindel A, Sargeaunt P, Katz D. Outcome of untreated infection
with Entamoeba histolytica in homosexual men with and without HIV antibody.
BMJ 1988; 297:654–7.
26. Hung CC, Deng HY, Hsiao WH, et al. Invasive amebiasis as an emerging para-
sitic disease in patients with human immunodeficiency virus type 1 infection in
Taiwan. Arch Intern Med 2005; 165:409–15.
27. Stark D, van Hal SJ, Matthews G, Harkness J, Marriott D. Invasive amebiasis in
men who have sex with men, Australia. Emerg Infect Dis 2008; 14:1141–3.
28. Ishioka H, Umezawa M, Hatakeyama S. Fulminant amebic colitis in an HIV-
infected homosexual man. Intern Med 2011; 50:2851–4.
29. Torigoe T, Nakayama Y, Yamaguchi K. Development of perianal ulcer as a result
of acute fulminant amoebic colitis. World J Gastroenterol 2012; 18:4794–7.
30. Chen Y, Zhang Y, Yang B, et al. Seroprevalence of Entamoeba histolytica infection
in HIV-infected patients in China. Am J Trop Med Hyg 2007; 77:825–8.
31. Salit IE, Khairnar K, Gough K, Pillai DR. A possible cluster of sexually trans-
mitted Entamoeba histolytica: genetic analysis of a highly virulent strain. Clin
Infect Dis 2009; 49(3): 346–53.
32. Hung CC, Ji DD, Sun HY, et al. Increased risk for Entamoeba histolytica infec-
tion and invasive amebiasis in HIV seropositive men who have sex with men in
Taiwan. PLoS Negl Trop Dis 2008; 2:e175.
33. Narayan S, Galanis E. Are enteric infections sexually transmitted in British
Columbia? Can Commun Dis Rep 2016; 42:24–9.
34. Dritz SK, Ainsworth TE, Back A, et al. Patterns of sexually transmitted enteric
diseases in a city. Lancet 1977; 2:3–4.
35. Schmerin MJ, Gelston A, Jones TC. Amebiasis: an increasing problem among
homosexuals in New York City. JAMA 1977; 238:1386–7.
36. Escola-Verge L, Arando M, Vall M, et al. Outbreak of intestinal amoebiasis among
men who have sex with men, Barcelona (Spain), October 2016 and January 2017.
Euro Surveill 2017; 22:30581. doi: 10.2807/1560-7917.ES.2017.22.30.30581.
PMID: 28797327; PMCID: PMC5553055.
37. Mildvan D, Gelb AM, William D. Venereal transmission of enteric pathogens in
male homosexuals: two case reports. JAMA 1977; 238:1387–9.
38. Hurwitz AL, Owen RL. Venereal transmission of intestinal parasites. West J Med
1978; 128:89–91.
39. Burnham WR, Reeve RS, Finch RG. Entamoeba histolytica infection in male
homosexuals. Gut 1980; 21:1097–9.
40. Ylvisaker JT, McDonald GB. Sexually acquired amebic colitis and liver abscess.
West J Med 1980; 132:153–7.
41. Saltzberg DM, Hall-Craggs M. Fulminant amebic colitis in a homosexual man.
Am J Gastroenterol 1986; 81:209–12.
42. Mitarai S, Nagai H, Satoh K, Hebisawa A, Shishido H. Amebiasis in Japanese ho-
mosexual men with human immunodeficiency virus infection. Intern Med 2001;
40:671–5.
43. Phillips SC, Mildvan D, William DC, Gelb AM, White MC. Sexual transmission
of enteric protozoa and helminths in a venereal-disease-clinic population. N Engl
J Med 1981; 305:603–6.
44. Chin AT, Gerken A. Carriage of intestinal protozoal cysts in homosexuals. Br J
Vener Dis 1984; 60:193–5.
45. Takeuchi T, Okuzawa E, Nozaki T, et al. High seropositivity of Japanese homo-
sexual men for amebic infection. J Infect Dis 1989; 159:808.
46. Weinke T, Friedrich-Janicke B, Hopp P, Janitschke K. Prevalence and clinical im-
portance of Entamoeba histolytica in two high-risk groups: travelers returning
from the tropics and male homosexuals. J Infect Dis 1990; 161:1029–31.
47. James R, Barratt J, Marriott D, Harkness J, Stark D. Seroprevalence of Entamoeba
histolytica infection among men who have sex with men in Sydney, Australia. Am
J Trop Med Hyg 2010; 83:914–6.
48. Lo YC, Ji DD, Hung CC. Prevalent and incident HIV diagnoses among Entamoeba
histolytica-infected adult males: a changing epidemiology associated with sexual
transmission—Taiwan, 2006-2013. PLoS Negl Trop Dis 2014; 8:e3222.
49. Zhou F, Li M, Li X, et al. Seroprevalence of Entamoeba histolytica infection among
Chinese men who have sex with men. PLoS Negl Trop Dis 2013; 7:e2232.
50. William DC, Shookhoff HB, Felman YM, DeRamos SW. High rates of enteric pro-
tozoal infections in selected homosexual men attending a venereal disease clinic.
Sex Transm Dis 1978; 5:155–7.
S176 • CID 2022:74 (Suppl 2) • McNeil et al
51. Kean BH, William DC, Luminais SK. Epidemic of amoebiasis and giardiasis in a
biased population. Br J Vener Dis 1979; 55:375–8.
52. Keystone JS, Keystone DL, Proctor EM. Intestinal parasitic infections in homo-
sexual men: prevalence, symptoms and factors in transmission. Can Med Assoc J
1980; 123:512–4.
53. Robertson DHH, McMillan A, Young H. Homosexual transmission of amoeb-
iasis. J R Soc Med 1982; 75(7): 564–5.
54. Sargeaunt PG, Oates JK, MacLennan I, Oriel JD, Goldmeier D. Entamoeba
histolytica in male homosexuals. Br J Vener Dis 1983; 59:193–5.
55. Markell EK, Havens RF, Kuritsubo RA, Wingerd J. Intestinal protozoa in homo-
sexual men of the San Francisco Bay area: prevalence and correlates of infection.
Am J Trop Med Hyg 1984; 33:239–45.
56. Ortega HB, Borchardt KA, Hamilton R, Ortega P, Mahood J. Enteric patho-
genic protozoa in homosexual men from San Francisco. Sex Transm Dis 1984;
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
11:59–63.
57. Levinson W, Dunn PM, Cooney TG, Sampson JH. Parasitic infections in asymp-
tomatic homosexual men: cost-effective screening. J Gen Intern Med 1986;
1:150–4.
58. Peters CS, Sable R, Janda WM, Chittom AL, Kocka FE. Prevalence of enteric para-
sites in homosexual patients attending an outpatient clinic. J Clin Microbiol 1986;
24:684–5.
59. Sorvillo FJ, Strassburg MA, Seidel J, et al. Amebic infections in asymptomatic ho-
mosexual men, lack of evidence of invasive disease. Am J Public Health 1986;
76:1137–9.
60. Aceti A, Pennica A, Ippolito G, et al. Antiamebic antibodies in homosexual men.
N Engl J Med 1987; 316:692.
61. Takeuchi T, Miyahira Y, Kobayashi S, Nozaki T, Motta SR, Matsuda J. High sero-
positivity for Entamoeba histolytica infection in Japanese homosexual men: fur-
ther evidence for the occurrence of pathogenic strains. Trans R Soc Trop Med Hyg
1990; 84:250–1.
62. Ko NY, Lee HC, Chang JL, et al. Prevalence of human immunodeficiency virus
and sexually transmitted infections and risky sexual behaviors among men vis-
iting gay bathhouses in Taiwan. Sex Transm Dis 2006; 33:467–73.
63. Tsai JJ, Sun HY, Ke LY, et al. Higher seroprevalence of Entamoeba histolytica in-
fection is associated with human immunodeficiency virus type 1 infection in
Taiwan. Am J Trop Med Hyg 2006; 74:1016–9.
64. Stark D, Fotedar R, van Hal S, et al. Prevalence of enteric protozoa in human im-
munodeficiency virus (HIV)-positive and HIV-negative men who have sex with
men from Sydney, Australia. Am J Trop Med Hyg 2007; 76:549–52.
65. Hung CC, Ko NY, Ko WC, et al. Amoebiasis among patrons visiting gay saunas in
Taiwan. HIV Med 2008; 9:787–9.
66. Lee HC, Ko NY, Lee NY, Chang CM, Ko WC. Seroprevalence of viral hepatitis and
sexually transmitted disease among adults with recently diagnosed HIV infection
in Southern Taiwan, 2000-2005: upsurge in hepatitis C virus infections among
injection drug users. J Formos Med Assoc 2008; 107:404–11.
67. Hung CC, Wu PY, Chang SY, et al. Amebiasis among persons who sought vol-
untary counseling and testing for human immunodeficiency virus infection: a
case-control study. Am J Trop Med Hyg 2011; 84:65–9.
68. Ko NY, Lee HC, Hung CC, et al. Trends of HIV and sexually transmitted infec-
tions, estimated HIV incidence, and risky sexual behaviors among gay bathhouse
attendees in Taiwan: 2004-2008. AIDS Behav 2011; 15:292–7.
69. Fernández-Huerta M, Zarzuela F, Barberá MJ, et al. Sexual transmission of in-
testinal 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. Am J Trop Med Hyg 2019; 101:1388–91.
70. Kotloff KL, Riddle MS, Platts-Mills JA, Pavlinac P, Zaidi AKM. Shigellosis. Lancet
2018; 391:801–12.
71. DuPont HL, Levine MM, Hornick RB, Formal SB. Inoculum size in shigellosis
and implications for expected mode of transmission. J Infect Dis 1989;
159:1126–8.
72. Hoffmann C, Sahly H, Jessen A, et al. High rates of quinolone-resistant strains of
Shigella sonnei in HIV-infected MSM. Infection 2013; 41:999–1003.
73. Hassing RJ, Melles DC, Goessens WH, Rijnders BJ. Case of Shigella flexneri in-
fection with treatment failure due to azithromycin resistance in an HIV-positive
patient. Infection 2014; 42:789–90.
74. Heiman KE, Karlsson M, Grass J, et al. Notes from the field: Shigella with de-
creased susceptibility to azithromycin among men who have sex with men—
United States, 2002-2013. MMWR Morb Mortal Wkly Rep 2014; 63:132–3.
75. Bowen A, Eikmeier D, Talley P, et al. Notes from the field: outbreaks of Shigella
sonnei infection with decreased susceptibility to azithromycin among men who
have sex with men—Chicago and metropolitan Minneapolis-St. Paul, 2014.
MMWR Morb Mortal Wkly Rep 2015; 64:597–8.
76. Bowen A, Grass J, Bicknese A, Campbell D, Hurd J, Kirkcaldy RD. Elevated risk
for antimicrobial drug-resistant Shigella infection among men who have sex with
men, United States, 2011-2015. Emerg Infect Dis 2016; 22:1613–6.
 77. Chiou CS, Izumiya H, Kawamura M, et al. The worldwide spread of ciprofloxacin-
resistant Shigella sonnei among HIV-infected men who have sex with men,
Taiwan. Clin Microbiol Infect 2016; 22:383.e11––.e16.
78. Baker KS, Dallman TJ, Field N, et al. Common determinants of antimicrobial
resistance in sequential episodes of sexually transmitted shigellosis in men who
have sex with men: a cross-sectional study. The Lancet 2017; 389(Supplement
1):S24.
79. Murray K, Reddy V, Kornblum JS, et al. Increasing antibiotic resistance in Shigella
spp. from infected New York City residents, New York, USA. Emerg Infect Dis
2017; 23:332–5.
80. Lane CR, Sutton B, Valcanis M, et al. Travel destinations and sexual behavior as
indicators of antibiotic resistant Shigella strains—Victoria, Australia. Clin Infect
Dis 2015; 62:722–9.
81. Hurd J, Collier S, Judd M, Bowen A. Increasing relative burden of laboratory-
confirmed Shigella flexneri infections among U.S. men, 2003-2013: an emerging
sexually transmitted disease. Sex Transm Dis 2016; 43:S151.
82. Van Rijckevorsel GG, Sonder GJ, Bovee LP, Thiesbrummel HF, Geskus RB, Van
Den Hoek A. Trends in hepatitis A, B, and shigellosis compared with gonor-
rhea and syphilis in men who have sex with men in Amsterdam, 1992-2006. Sex
Transm Dis 2008; 35:930–4.
83. Chen M, Delpech V, O’Sullivan B, Donovan B. Shigella sonnei: another cause of
sexually acquired reactive arthritis. Int J STD AIDS 2002; 13:135–6.
84. O’Sullivan B, Delpech V, Pontivivo G, et al. Shigellosis linked to sex venues,
Australia. Emerg Infect Dis 2002; 8:862–4.
85. Valcanis M, Brown JD, Hazelton B, et al. Outbreak of locally acquired
azithromycin-resistant Shigella flexneri infection in men who have sex with men.
Pathology 2015; 47:87–8.
86. Strauss B, Kurzac C, Embree G, Sevigny R, Paccagnella A, Fyfe M. Clusters of
Shigella sonnei in men who have sex with men, British Columbia, 2001. Can
Commun Dis Rep 2001; 27:109–10; discussion 10-4.
87. Public Health Agency of Canada. Outbreak of Shigella flexneri and Shigella
sonnei enterocolitis in men who have sex with men, Quebec, 1999 to 2001. Can
Commun Dis Rep 2005; 31:85–90.
88. Ratnayake R, Allard R, Pilon PA. Shifting dominance of Shigella species in men
who have sex with men. Epidemiol Infect 2012; 140:2082–6.
89. Wilmer A, Romney MG, Gustafson R, et al. Shigella flexneri serotype 1 infections
in men who have sex with men in Vancouver, Canada. HIV Med 2015; 16:168–75.
90. Mohan K, Hibbert M, Rooney G, et al. What is the overlap between HIV and
shigellosis epidemics in England: further evidence of MSM transmission? Sex
Transm Infect 2018; 94:67–71.
91. Marcus U, Zucs P, Bremer V, et al. Shigellosis—a re-emerging sexually transmitted
infection: outbreak in men having sex with men in Berlin. Int J STD AIDS 2004;
15:533–7.
92. Liao YS, Liu YY, Lo YC, Chiou CS. Azithromycin-nonsusceptible Shigella flexneri
3a in men who have sex with men, Taiwan, 2015-2016. Emerg Infect Dis 2016;
23:345–6.
93. Morgan O, Crook P, Cheasty T, et al. Shigella sonnei outbreak among homosexual
men, London. Emerg Infect Dis 2006; 12:1458–60.
94. Gaudreau C, Barkati S, Leduc JM, Pilon PA, Favreau J, Bekal S. Shigella spp. with
reduced azithromycin susceptibility, Quebec, Canada, 2012-2013. Emerg Infect
Dis 2014; 20:854–6.
95. Mook P, McCormick J, Bains M, et al. ESBL-producing and macrolide-resistant
Shigella sonnei infections among men who have sex with men, England, 2015.
Emerg Infect Dis 2016; 22:1948–52.
96. Borg ML, Modi A, Tostmann A, et al. Ongoing outbreak of Shigella flexneri se-
rotype 3a in men who have sex with men in England and Wales, data from 2009-
2011. Euro Surveill 2012; 17:20137. PMID: 22490381.
97. Gilbart VL, Simms I, Jenkins C, et al. Sex, drugs and smart phone applications:
findings from semistructured interviews with men who have sex with men diag-
nosed with Shigella flexneri 3a in England and Wales. Sex Transm Infect 2015;
91:598–602.
98. Simms I, Field N, Jenkins C, et al. Intensified shigellosis epidemic associated
with sexual transmission in men who have sex with men—Shigella flexneri and
S. sonnei in England, 2004 to end of February 2015. Euro Surveill 2015; 20:21097.
doi: 10.2807/1560-7917.es2015.20.15.21097. PMID: 25953129.
99. Serafino Wani RL, Filson SA, Chattaway MA, Godbole G. Invasive shigellosis in
MSM. Int J STD AIDS 2016; 27:917–9.
100. Dritz SK, Back AF. Letter: Shigella enteritis venereally transmitted. N Engl J Med
1974; 291:1194.
101. Bader M, Pedersen AH, Williams R, Spearman J, Anderson H. Venereal transmis-
sion of shigellosis in Seattle-King County. Sex Transm Dis 1977; 4:89–91.
102. Centers for Disease Control and Prevention. Shigella sonnei outbreak among men
who have sex with men—San Francisco, California, 2000-2001. JAMA 2002;
287:37–8.
103. Centers for Disease Control and Prevention. Shigella flexneri serotype 3 infec-
tions among men who have sex with men—Chicago, Illinois, 2003-2004. MMWR
Morb Mortal Wkly Rep 2005; 54:820–2.
104. Hines JZ, Pinsent T, Rees K, et al. Notes from the field: shigellosis outbreak
among men who have sex with men and homeless persons—Oregon, 2015-2016.
MMWR Morb Mortal Wkly Rep 2016; 65:812–3.
105. Baker KS, Dallman TJ, Ashton PM, et al. Intercontinental dissemination of
azithromycin-resistant shigellosis through sexual transmission: a cross-sectional
study. Lancet Infect Dis 2015; 15:913–21.
106. Brodrick R, Sagar J. Toxic megacolon from sexually transmitted Shigella sonnei
infection. Int J Colorectal Dis 2012; 27:415.
107. Gaudreau C, Ratnayake R, Pilon PA, Gagnon S, Roger M, Lévesque S.
Ciprofloxacin-resistant Shigella sonnei among men who have sex with men,
Canada, 2010. Emerg Infect Dis 2011; 17:1747–50.
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022
108. Wu HH, Shen YT, Chiou CS, Fang CT, Lo YC. Shigellosis outbreak among MSM
living with HIV: a case-control study in Taiwan, 2015-2016. Sex Transm Infect
2019; 95:67–70.
109. Keay R, Singh G, Abdul-Latif M, Rayment M, Nelson M. Shigella flexneri enteritis
in risk-taking HIV-infected MSM. J Infect 2014; 68:103–4.
110. Einarsson E, Ma’ayeh S, Svard SG. An up-date on Giardia and giardiasis. Curr
Opin Microbiol 2016; 34:47–52.
111. Meyers JD, Kuharic HA, Holmes KK. Giardia lamblia infection in homosexual
men. Br J Vener Dis 1977; 53:54–5.
112. Esfandiari A, Swartz J, Teklehaimanot S. Clustering of giardiosis among AIDS
patients in Los Angeles County. Cell Mol Biol (Noisy-le-grand) 1997; 43:1077–83.
113. Esfandiari A, Jordan WC, Brown CP. Prevalence of enteric parasitic infection
among HIV-infected attendees of an inner city AIDS clinic. Cell Mol Biol (Noisy-
le-grand) 1995; 41:S19–23.
114. Ma P, Kaufman D, Montana J. Isospora belli diarrheal infection in homosexual
men. AIDS Res 1983; 1:327–38.
115. Forthal DN, Guest SS. Isospora belli enteritis in three homosexual men. Am J Trop
Med Hyg 1984; 33:1060–4.
116. Pedersen C, Danner S, Lazzarin A, et al. Epidemiology of cryptosporidiosis
among European AIDS patients. Genitourin Med 1996; 72:128–31.
117. Caputo C, Forbes A, Frost F, et al. Determinants of antibodies to cryptosporidium
infection among gay and bisexual men with HIV infection. Epidemiol Infect
1999; 122:291–7.
118. Hellard M, Hocking J, Willis J, Dore G, Fairley C. Risk factors leading to cryp-
tosporidium infection in men who have sex with men. Sex Transm Infect 2003;
79:412–4.
119. Danila RN, Eikmeier DL, Robinson TJ, La Pointe A, DeVries AS. Two concurrent
enteric disease outbreaks among men who have sex with men, Minneapolis-St.
Paul area. Clin Infect Dis 2014; 59:987–9.
120. Sorvillo FJ, Lieb LE, Kerndt PR, Ash LR. Epidemiology of cryptosporidiosis
among persons with acquired immunodeficiency syndrome in Los Angeles
County. Am J Trop Med Hyg 1994; 51:326–31.
121. Field AS, Milner DA Jr. Intestinal microsporidiosis. Clin Lab Med 2015;
35:445–59.
122. Cotte L, Rabodonirina M, Chapuis F, et al. Waterborne outbreak of intestinal
microsporidiosis in persons with and without human immunodeficiency virus
infection. J Infect Dis 1999; 180:2003–8.
123. Hutin YJ, Sombardier MN, Liguory O, et al. Risk factors for intestinal
microsporidiosis in patients with human immunodeficiency virus infection: a
case-control study. J Infect Dis 1998; 178:904–7.
124. Cook GC. Enterobius vermicularis infection. Gut 1994; 35:1159–62.
125. The Medical Letter. Drugs for Parasitic Infections Treat Guidel Med Lett 2013;
11(Suppl):e1–31.
126. Waugh MA. Threadworm infestation in homosexuals. Trans St Johns Hosp
Dermatol Soc 1972; 58:224–5.
127. McMillan A. Threadworms in homosexual males. Br Med J 1978; 1:367.
128. Waugh MA. Letter: sexual transmission of intestinal parasites. Br J Vener Dis
1974; 50:157.
129. Krolewiecki A, Nutman TB. Strongyloidiasis: a neglected tropical disease. Infect
Dis Clin North Am 2019; 33:135–51.
130. Sorvillo F, Mori K, Sewake W, Fishman L. Sexual transmission of Strongyloides
stercoralis among homosexual men. Br J Vener Dis 1983; 59:342.
131. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol
2004; 2:123–40.
132. Simms I, Gilbart VL, Byrne L, et al. Identification of verocytotoxin-producing
Escherichia coli O117:H7 in men who have sex with men, England, November
2013 to August 2014. Euro Surveill 2014; 19:20946. doi:10.2807/1560-7917.
es2014.19.43.20946. PMID: 25375900.
133. Dritz SK, Braff EH. Sexually transmitted typhoid fever. N Engl J Med 1977;
296:1359–60.
Enteric Infections in MSM • CID 2022:74 (Suppl 2) • S177
 134. Reller ME, Olsen SJ, Kressel AB, et al. Sexual transmission of typhoid fever: a
multistate outbreak among men who have sex with men. Clin Infect Dis 2003;
37:141–4.
135. Bernstein K, Bowen VB, Kim CR, et al. Re-emerging and newly recognized sexu-
ally transmitted infections: can prior experiences shed light on future identifica-
tion and control? PLoS Med 2017; 14:e1002474.
136. Kim LS, Stansell J, Cello JP, Koch J. Discrepancy between sex- and water-
associated risk behaviors for cryptosporidiosis among HIV-infected patients in
San Francisco. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 19:44–9.
137. Bains M, Crook P, Field N, Hughes G. Safer chemsex: consideration of Shigella. Br
J Gen Pract 2016; 66:124.
138. Kirkcaldy RD, Zaidi A, Hook EW 3rd, et al. Neisseria gonorrhoeae antimicrobial
resistance among men who have sex with men and men who have sex exclusively
S178 • CID 2022:74 (Suppl 2) • McNeil et al
with women: the Gonococcal Isolate Surveillance Project, 2005-2010. Ann Intern
Med 2013; 158:321–8.
139. Mosher WD, Chandra A, Jones J. Sexual behavior and selected health measures:
men and women 15–44 years of age, United States, 2002. Advance data from
vital and health statistics. Hyattsville, MD: National Center for Health Statistics,
2005.
140. Copen CE, Chandra A, Febo-Vazquez I. Sexual behavior, sexual attraction, and
sexual orientation among adults aged 18–44 in the United States: data from the
2011–2013 National Survey of Family Growth. Natl Health Stat Rep 2016; (88):1–
14. PMID: 26766410.
141. Habel MA, Leichliter JS, Dittus PJ, Spicknall IH, Aral SO. Heterosexual anal and
oral sex in adolescents and adults in the United States, 2011-2015. Sex Transm Dis
2018; 45:775–82.
Downloaded from https://academic.oup.com/cid/article/74/Supplement_2/S169/6567964 by Stanford University user on 25 April 2022