VOL. 55, No. 6

JUNE 1979

SEXUALLY TRANSMITTED ENTERIC DIS EAS ES YEHUDI M. FELMAN, M.D. Associate Clinical Professor of Dermatology State University of New York Downstate Medical Center Brooklyn, New York Director, Bureau of Venereal Disease Control New York City Department of Health

NICHOLAS B. RICCIARDI, Ph.D. Research Microbiologist Bureau of Venereal Disease Control New York City Department of Health New York, New York

T HE sexual transmission of enteric pathogens has recently been recognized as a significant health hazard. Sexual transmission of protozoal pathogens such as Giardia lamblia, Entameba histolytica, and Dientamoeba fragilis in the urban homosexual population was first reported in 1972.1 Since then, several more papers have appeared in the literature describing cases of amebiasis, giardiasis, hepatitis B, salmonellosis, and shigellosis that were sexually transmitted, primarily among homosexual men. These enteric infections, which have traditionally been associated with contaminated food or water and encountered among Americans with a history of foreign travel, are now found in significant numbers among individuals without a history of such travel. The investigation of their



water supply has failed to show fecal contamination.2 Instead, certain types of sexual activity such as anilingus and fellatio of a fecally contaminated penis provide an excellent mechanism to spread these diseases by fecal-oral contamination.3 Kazel, Sohn, and Cassaco reported in 1972 six cases of shigellosis and 17 cases of amebiasis among 260 homosexual patients.4 Dritz and Back in 1974 reported 50 cases of Shigella enteritis among the homosexual community of San Francisco.5 Drusin in 1976 stated that 17 (or 45%) of 38 patients treated in New York Hospital for shigellosis were homosexual. This percentage was much greater than the homosexual percentage of the hospital population.6 Dritz and Broft in 1977 documented the sexual transmission of two cases of typhoid fever in the San Francisco area. Thus, Salmonella typhi, one of the most pathogenic enteric bacteria, can also be transmitted sexually.7 Sporadic appearances of amebiasis and shigellosis have occurred among men in San Francisco where no history of a common food source could be obtained, but in a large number of cases there was a history of frequent oral-genital and oral-anal contact.8 More recently, William, Shookhoff, Felman, and De Ramos reported that of 89 sexually active homosexual men screened for protozoal cysts on stool examination, 27, or 30%, were positive. Further investigation of the group revealed 18 with amebiasis and 11 with giardiasis. Six men had both amebiasis and giardiasis. The presence of the infection correlated best with a history of anilingus and fecal-oral transmission rather than place of birth, travel, or history of symptoms.9 Statistical evidence of this health hazard has also been accumulating. Forty percent of all reported cases of amebiasis in the United States during 1977 were from New York City. Eighty percent of these cases were located in the borough of Manhattan, and the lower West Side, with its large male homosexual community, had the highest morbidity rate.10 Viral hepatitis, type B, has been found to be transmitted sexually.11-15 Dritzman et al. in 1977 demonstrated that exposure to hepatitis B virus was 8.8 times greater for homosexual men than for heterosexual men.11 In 1975 Fosner, Buchholz, and Gerth demonstrated a higher antihepatitis surface antigen (anti HBs) among prostitutes when compared to females and nuns of matched age. 1" Antibody studies in Greece also support the venereal transmission of hepatitis B.17 Hepatitis type A is thought to be transmitted via the fecal-oral route, but the rate of transmission is low and presence of hepatitis A antibody correlates better with low Bull. N.Y. Acad. Med.



social-economic status than with sexual preference or activity.'8 There are no serologic tests for non-A, non-B hepatitis. Consequently, sexual transmission of non-A, non-B hepatitis can only be inferred, as common with hepatitis B.19 SHIGELLOSIS



Shigellosis is generally a disease of children and less frequently of adults. Adults presenting with shigellosis usually give a history of foreign travel or exposure to infected children.20 In the absence of the above situations, sexual transmission must be suspected. Likewise, the sexual transmission of Salmonella sp. must be suspected when there is a lack of food-related sources. The patient should be carefully questioned about sexual preference, sexual habits, and a history of other sexually transmitted diseases. The major sexual mode of transmission of Shigella sp. is anilingus. Less commonly, fellatio may result in fecal-oral transmission. The incubation period is one to seven days, usually less than four days. The symptoms range from asymptomatic to severe abdominal cramps. Other signs and symptoms include nausea, vomiting, diarrhea, fever, abdominal tenderness, dehydration, and stools containing blood, mucus, or pus. The diagnosis is made by swabbing a fresh stool specimen onto MacConkey's Shigella Salmonella agar. Treatment involves fluid and electrolyte replacement and antibiotic treatment using either tetracycline or ampicillin 500 mg. orally q.i.d. for seven days. It must be noted that shigellosis can have an asymptomatic carrier state of up to one year during which the disease may be transmitted. Salmonella has the same sexual transmission as shigella. However, the asymptomatic carrier state can be shorter. The incubation period is 6 to 72 hours, usually 12 to 36 hours. The signs, symptoms, diagnosis, and treatment are the same as shigellosis. With both salmonellosis and shigellosis, drug sensitivities are appropriate for drugregimen information and epidemiologic purposes. AMEBIASIS AND GIARDIASIS

The sexual mode of transmission of these pathogens is the same as the bacterial pathogens. The etiologic agents of amebiasis are Entamoeba histolytica and Dientamoeba fragilis, while the etiologic agent of giardiasis is Giardia lamblia. The incubation period for amebiasis varies from a few days to several months, but is usually two to four weeks. The signs and Vol. 55, No. 6 June 1979



symptoms of amebiasis range from an asymptomatic state to diarrhea, blood and mucus in feces, dyspepsia, abdominal cramps, fever, chills, flatulence, irritable bowels, and abdominal tenderness. The diagnosis requires direct smear identification of cysts or trophozoites from purged stools. The smears are stained with hematoxylin. A culture identifying trophozoites or rectal biopsy can also be used. At present, there is a medical controversy over the accepted medical management of these diseases because of probable differences in sensitivity of strains from various geographical locations. The incubation period for giardiasis is from five days to four weeks. The signs and symptoms for this infection may include chronic diarrhea, anorexia, abdominal cramps, bloating, fatigue, frequent, loose, pale, greasy stools, flatulence, epigastric pain, abdominal tenderness, and weight loss. However, some patients may be asymptomatic. The diagnosis is by direct smear identification of cysts or trophozoites in stools or trophozoites in duodenal drainage. The treatment includes quinacrine hydrochloride 100 mg. t.i.d. x five to'seven days or metronidazole 250 mg. t.i.d. x 10 days. HEPATITIS

The incubation period for hepatitis and other information is summarized in the table. The sexual mode of transmission of hepatitis B includes any sexual practice that involves exposure to infectious saliva, semen, urine, vaginal secretions, and menstrual blood. The hepatitis B surface antigen has been identified in all the above fluids.2125 Any oral or anal contact with these infected fluids can result in the viral particle being absorbed across mucosal surfaces.19


Patients presenting to a physician with an enteric infection without a history of the classic means of transmission have most likely been infected sexually. Thus, patients should be advised that their sexual contacts are probably infected as well. All sexually active individuals who perform anilingus, especially the male homosexual, bisexual, and their sexual contacts are at risk for these infections.26 Careful attention should be given to purged stool examinations and to repeated stool cultures. Infected individuals must be advised not to expose others to their infection not only while they are symptomatic but during the carrier state. Unfortunately, the true scope of this problem in the sexually Bull. N.Y. Acad. Med.




Usually acute onset

Hepatitis B Usually insidious onset

Brief incubation period (15-45 days) Infrequent venereal transmission

Longer incubation period (30-180 days) Frequent venereal transmission

Non-A, non-B hepatitis Clinically indistinguishable from other viral hepatitides

Venereal transmission suggested; parenteral transmission confirmed Prophylaxis recommended Prophylaxis with ISG of Effective prophylaxis unwith ISG (immune serum variable or limited effect- known globulin) iveness; prophylaxis with hepatitis B immune globulin limited to restricted instances of exposure Markers: Markers: Markers: Not available Only hepatitis A antibody HBsAg (surface antigen) HBcAG (core antigen) (not routinely available) HBeAG (core antigen)

active homosexual community has not been fully appreciated by most

physicians. The majority of men seem to be asymptomatic or minimally symptomatic.10 It must be noted that patients found negative for protozoal pathogens and positive for nonpathogens should be retested. Nonpathogenic protozoa usually serve as a marker for pathogens. Thus, additional stool examinations should be performed. Anoscopy and sigmoidoscopy are useful to locate the small hemorrhagic ulcers usually associated with amebiasis. Barium enemas can be employed to eliminate the possibility of other etiologies. It is not uncommon for patients to go through various expensive and time-consuming examinations when all that was necessary for the diagnosis was a purged stool examination. Therefore, information about patients' sexual practices can be very helpful. Because open admission of sexual preferences is required of homosexuals seeking an examination for sexually transmitted diseases, it is important not to alienate the homosexual patient in dealing with him.27 The infected patient must be treated with a nonjudgemental attitude. Thus, any negative attitude perceived by the patient may irritate him and thus impede the flow of this information. All individuals who engage in anilingus and fellatio risk these infections, including heterosexuals. Food handlers with an asymptomatic or a Vol. 55, No. 6 June 1979



minimally symptomatic infection may not be aware of their infection. Therefore, strict enforcement of sanitary hygienic codes that govern people employed in this capacity is important. REFERENCES 1. Abrahm, P. M.: Snakes in the grass or 12. Wright, R. A.: Hepatitis B and the the worms turn on. J.A. M.A. 221:917, HbAg carrier. An outbreak related to 1972. sexual contact. J.A.M.A. 232:717-21, 2. Kean, B. H.: Venereal amebiasis. N. Y. 1975. State J. Med. 76:930-31, 1976. 13. Fulford, K. W. M., Dane, D. S., 3. William, D. C., Felman, Y. M., Marr, Catheral, R. B., et al.: Australian antiJ. S., and Shookhoff H. B.: Sexually gen and antibody among patients attendtransmitted enteric pathogens in male ing a clinic for sexually transmitted dishomosexual population. N. Y. State J. eases. Lancet 1:1470-73, 1973. Med. 77:2050-52, 1977. 14. Lim, K. S., Wong, V. T., Fulford, K. W. M., et al.: Role of sexual and non4. Kazol, H. W., Sohn, N., and Cassaco, sexual practices in the transmission of J. 1.: The gay bowel syndrome: Clinihepatitis B. Br. J. Vener. Dis. 53:190cal pathological correlation in 260 cases. Clinic and Lab. Science 6:18492, 1977. 15. Szmuness, W, Much, M. I., Prince, A. 92, 1976. M., et al: On the role of sexual behavior 5. Dritz, S. K. and Back, A. F.: Shigella in the spread of hepatitis B infection. enteritis venereally transmitted disease. Ann. Intern. Med. 83:489-95, 1975. N. Engl. J. Med. 291:1194, 1974. 6. Drusin, L. M., Genvent, G., Topf- 16. Frosner, G. G., Bucholz, H. M., and Gerth, H. J.: Prevalence of hepatitis B Ostein, B., et al: E shigellosis, another antibody in prostitutes. Am. J. sexually transmitted disease. Br. J. Epidemiol. 102:241-59, 1975. Vener. Dis. 52:348-50, 1976. 7. Dritz, S. K. and Broff, E. H.: Sexually 17. Papeavangelon, G., Trichopoulos, T., Kremastinou, T., et al.: Prevalence of transmitted typhoid fever. N. Engl. J. hepatitis B antigen and antibody in prosMed. 296:1359-60, 1977. titutes. Br. Med. J. 2:256-58, 1974. 8. Dritz, S. K., Ainsworth, T. E., Garrand, W. F., et. al: Patterns of sexually 18. Szmuness, W., Dienstag, J. L. Purcell, R. H., et al.: Distribution of antibody to transmitted diseases in a city. Lancet hepatitis A antigen in urban adult popu2:3, 1977. lation. N. Engl. J. Med. 295:755-59, 9. William, D. C., Shookhoff, H. B., Fel1976. man, Y. M., and DeRamos, S. W.: High rates of enteric protozoal infections in 19. Morb. Mort. Weekly Rep., C.D.C. 26:425-42, 1977. selected homosexual men attending a veneral disease clinic. Sex. Trans. Dis. 20. Bader M.: Sexual transmission of shigellosis.Med. Asp. Human Sexual. 12:755:155-57, 1978. 76, 1978. 10. Service and Vital Statistics by Health Center District in New York City, 1977. 21. Villarejos, V. M., Visona, K. A., Gutierrez, A., et al.: Role of saliva, New York City Dept. of Health, pp. urine and feces in the transmission of 16-21. 11. Deitzman, D. E., Harnish, C. G. E., type B hepatitis. N. Engl. J. Med. Alexander, R. E., and Homes, K. K.: 291:1375-78, 1974. Hepatitis B surface antigen (HBsAg) 22. Mazzur, S.: Menstrual blood as a vehicle prevalence in homosexual and heteroof Australia-antigen transmission. sexual men. J.A.M.A. 238:2625-26, Lancet 1:320, 1974. 1977. 23. Heathcote, J., Cameron, C. H., and

Bull. N.Y. Acad. Med.



Dane, D. S.: Hepatitis B antigen in Med. 285:1363-64, 1971. saliva and semen. Lancet 1:72-73, 1974. 26. Mildvan, D., Gelb, A. M., and Wil24. Darani, M. and Gerber, M: Hepatitis B liam, D. C.: Venereal transmission of antigen in vaginal secretion (letter). enteric pathogens in male homosexuals. Lancet 2:1008, 1974. Two case reports. J.A.M.A. 238: 25. Hersh, T., Melnick, J. L., Goyal, R. 1387-89, 1977. K., et al.: Non-parenteral transmission 27. Felman, Y. M. and Morrison, J.: Examof viral hepatitis B (Australia antigen asining the homosexual male for sexually sociated serum hepatitis). N. Engl. J. transmitted diseases. J.A. M.A. 238: 2046-47, 197'.

Vol. 55, No. 6 June 1979

Sexually transmitted enteric diseases.

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