Outbreak of Shigella flexneri and Shigella sonnei enterocolitis in men who have sex with men, Quebec, 1999 to 2001

Shigella spp., which are most commonly acquired in tropical zones but can also be acquired in temperate zones, are a frequent cause of enterocolitis. Since only a low dose is needed to cause infection, Shigella spp. can be transmitted from person to person, both directly and indirectly⁽¹⁾.

The goals of this study were to: investigate the possibility of Shigella (S.) flexneri and Shigella sonnei outbreaks in the Quebec population of men who have sex with men (MSM); to examine the sensitivity of these strains to three antibiotics; and to evaluate the risk factors associated with the Shigella spp. infections identified through the epidemiological surveys of the Direction de la santé publique (DSP) de Montréal-Centre.

Serotyping of S. flexneri strains, as well as molecular characterization by pulse field gel electrophoresis (PFGE) using Blnl and Xbal enzymes from S. flexneri (serotype 3) and S. sonnei strains acquired in Quebec, as well as from control strains, were carried out at the Laboratoire de santé publique du Québec, based on the methods previously described and, in the case of PFGE, the interpretation criteria described by Tenover⁽²⁾. The sensitivity of Shigella spp. strains to ampicillin, trimethoprim-sulfamethoxazole (TMP-SMX) and ciprofloxacin, as determined using NCCLS methods⁽³⁾, was reviewed. Epidemiological surveys of Shigella spp. infections reported to DSP Montréal-Centre in 2001 were analysed.

Between 1999 and 2001, 76 cases of Shigella spp. infection were identified by the medical microbiology and infectiology laboratory of Hôpital Saint-Luc (Centre hospitalier de l'Université de Montréal). All 38 patients infected with a strain acquired in Quebec, as well as 19 of the 38 patients infected with a strain acquired abroad, were men (p = 0.0000019).

From December 1999 to December 2000, S. flexneri serotype 3 (PFGE pattern A) was documented in seven men between the ages of 26 and 40 who had acquired the infection in Quebec (patients 1 to 7, Table 1). Sexual orientation and HIV status were known for two of these patients: both were MSM and both were HIV positive. Three strains of S. flexneri serotype 3 (patterns B, C and D respectively), isolated in two men and one woman (patients 8 to 10, Table 1), were used as control strains.

Between February 2000 and December 2001, a S. sonnei strain with PFGE pattern A was documented in 27 men between the ages of 22 and 54 who had acquired the infection in Quebec (patients 1 to 27, Table 2). The sexual orientation of five of these patients was known: all five were MSM. HIV status was known for three of these patients: two were HIV negative and the third was HIV positive. Five strains of S. sonnei, (PFGE patterns A5, A5b, C, C1 and G respectively), isolated in three men and two women (patients 28 to 32, Table 2) were used as control strains.

Table 1. Epidemiological and molecular data of 10 patients with a serotype 3 Shigella flexneri infection recorded in Quebec

Table 2. Epidemiological and molecular data of 32 patients with Shigella sonnei infection recorded in Quebec

Antibiotic sensitivity was known for 31 of the 34 epidemic Shigella spp. strains: 100% of the strains were resistant to ampicillin and sensitive to ciprofloxacin, and 90.3% were resistant to TMP-SMX.

Six S. flexneri strains displayed PFGE pattern A and the 7th strain displayed pattern A-4, when the Blnl enzyme was used (Figure 2). Seventeen S. sonnei strains displayed PFGE pattern A, and one, eight, and one S. sonnei strains displayed, respectively, patterns A-1, A-2, and A-4 when the XbaI enzyme was used (Figure 3). Molecular characterization of S. flexneri using the Xbal enzyme and characterization of S. sonnei using the Blnl enzyme produced results that were concordant with those obtained with the other enzyme respectively (data not shown).

In 2001, 147 cases of Shigella spp. infection were reported to DSP Montréal-Centre. Ninety-three of these patients (63.3%) had acquired the infection in Quebec: 76.3% were infected with S. sonnei, 21.5% with S. flexneri, and 2.2% were infected with another species or an unknown species. Sixty-six of the 93 patients (71%) who became infected in Quebec were men. Thirty out of 37 men (81%) whose sexual orientation was known were MSM and 29 of them (96.7%) had an S. sonnei infection. In 2000, only two cases of S. sonnei infection in MSM had been reported to DSP Montréal-Centre.

Three of the patients infected with an epidemic strain of S. sonnei (patients 2, 8 and 27, Table 2) developed - within 2 to 20 months of this enteric infection - Campylobacter jejuni subsp. jejuni (C. jejuni) enterocolitis, which proved sensitive to tetracycline but resistant to erythromycin and ciprofloxacin and was epidemic among MSM in Quebec between December 1999 and November 2001⁽⁴⁾. The sexual orientation of one of the patients who presented both of these enteric infections was not known.

Figure 1 presents the number of cases of S. flexneri, S. sonnei and C. jejuni recorded each month in MSM in Quebec, between December 1999 and December 2001. The outbreaks of S. flexneri and C. jejuni overlapped from December 1999 to December 2000, the epidemics of C. jejuni and S. sonnei were concomitant from February 2000 to November 2001, and outbreaks of all three enteropathogenic bacteria overlapped from February to December 2000. These enteric infections, epidemic in MSM, arose concomitantly with increases in high-risk sexual behaviour and sexually transmitted diseases (STDs) among these Quebec patients⁽⁵⁾.

Figure 1. Number of patients infected with Shigella spp. or erythro and cipro-resistant Campylobacter jejuni acquired in Quebec, 1999-2001

Figure 2. Pulse field gel electrophoresis (PFGE) of Blnl enzyme from 10 strains of Shigella flexneri

Lanes 1, 6 and 10: controlmolecular weights. Lanes 2-5, 7-8: PFGE pattern A: patients 1-6, Table 1. Lane 9: PFGE pattern A-4: patient 7, Table 1. Lanes 11-13: PFGE patterns B, C and D: patients 8, 10 and 9 respectively, Table 1.

Figure 3. Pulse field gel electrophoresis (PFGE) of Xbal enzyme from 13 strains of Shigella sonnei

Lanes 1, 14: controlmolecular weights. Lanes 2, 12: PFGE pattern A5. Lanes 3, 5-8, 11: PFGE pattern A: patients 2-4, 6-7, 12-18, 22-26, Table 2. Lanes 4, 9: PFGE patterns C and C1. Lane 10: PFGE pattern A2: patients 1, 5, 8-10, 20-21, 27. Lane 13: PFGE pattern G.

Molecular and epidemiological studies confirm that there were outbreaks of S. flexneri (December 1999 to December 2000) and S. sonnei (February 2000 to December 2001) among MSM in Quebec. The epidemiological data point to sexual transmission: all patients infected by a locally-acquired epidemic strain of Shigella spp. were men; the seven men whose sexual orientation was known were MSM, and three presented a C. jejuni infection that had been sexually acquired and was epidemic in the male homosexual population in Quebec. The study carried out by DSP Montréal-Centre confirmed the occurrence of an active outbreak of S. sonnei in MSM at the time of study, whereas the S. flexneri outbreak documented up until December 2000 had come to an end by the time the DSP study began. The demographic data and risk factors of patients infected in these Shigella epidemics, as well as the duration of the two outbreaks (13 and 23 months) argue against a common source, such as food.

Between 1996 and 2000, a number of Canadian, American, and Australian studies reported an increase in high-risk sexual behaviour, as well as an increase in STDs among MSM^(5,6). An outbreak of sexually-transmitted Shigella spp. infections among gay men was described for the first time in 1974⁽⁶⁾. An outbreak of S. sonnei was recently reported in MSM in British Columbia⁽⁶⁾ and San Francisco⁽⁷⁾. In North America, Shigella outbreaks in this population had previously been attributable to the flexneri species⁽⁶⁾. Gay men have also been reported as being at increased risk of contracting Campylobacter spp. and Helicobacter spp.⁽⁸⁾ infections.

The outbreaks described in this study are the first documented outbreaks of Shigella spp. in MSM in Quebec. To our knowledge, a simultaneous outbreak of sexually transmitted S. flexneri, S. sonnei and C. jejuni infections had not previously been documented in the male homosexual community. It would be interesting to compare the PFGE patterns of the S. sonnei strains isolated during this outbreak with those of the epidemic S. sonnei strains isolated in the gay communities of British Columbia and San Francisco. Gay and bisexual men must be educated in the prevention of sexually transmitted enteric diseases, along with the prevention of other STDs^(5-7). They must use barriers to prevent the transmission of enteric pathogens and avoid sexual relations when experiencing gastro- intestinal symptoms. In a context of resurgent enteric infections in MSM, it is important to confirm the sexual orientation of men who present with this clinical profile.

References

1. DuPont HL. Shigella species (bacillary dysentery) In: Mandell GL, Bennett JE, Dolin R (eds.), Principles and practice of infectious diseases 2005, 6th ed. Churchill Livingston, Philadelphia, Pa. p. 2655-61.

2. Swaminathan B, Barrett TJ, Hunter SB et al. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerging Infect Dis 2001; 7(3): 382-9.

3. National Committee for Clinical Laboratory Standards. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard, 5th ed. NCCLS publication No. M7-A5. National Committee for Clinical Laboratory Standards, Wayne, Pa., 2001.

4. 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 Diseases 2003;37:131-6.

5. HIV Infections Among MSM in Canada. HIV/AIDS Epi-Update, Health Canada, April 2003, p. 41-46.

6. Strauss B, Kurzac C, Embree G et al. Clusters of Shigella sonnei in men who have sex with men, British Columbia, 2001. CCDR 2001;27:109-14.

7. Klausner JD, Aragon T, Enanoria WTA et al. Shigella sonnei outbreak among men who have sex with men, San Francisco, California, 2000-2001. MMWR 2001;50:922-6.

8. Laughon BE, Vernon AA, Druckman DA et al. Recovery of Campylobacter species from homosexual men. J Infect Dis 1988;158:464-7.

Source: C Gaudreau, MD, Medical microbiology and infectiology, Hôpital Saint-Luc, Centre hospitalier de l'Université de Montréal; A Bruneau, MD, Direction de la santé publique Montréal-Centre; J Ismaïl, BSc, Laboratoire de santé publique du Québec/INSPQ, Sainte-Anne-de-Bellevue, Quebec, Canada.