Giardiasis: Association with Homosexuality MICHAEL J. SCHMERIN,
M.D.; THOMAS C. JONES,
M.D.,
F.A.C.P.; and HARVEY
KLEIN,
M.D.; New York, New York
Giardiasis is a common gastrointestinal illness among travelers. Recently an increased prevalence of giardiasis in men who had not traveled outside New York City was seen at The New York Hospital and was found to be due to transmission of this disease among homosexuals. Cases of giardiasis for a 5-year period were then reviewed, and it was discovered that 19 male patients who had not traveled or had an immunodeficiency disease were homosexuals. This accounted for 2 2 % of the adult men with giardiasis during that period. Adult women with giardiasis usually were either travelers or had an immunodeficiency disease ( 9 6 % ) . It is important to obtain a sexual history in these patients and treat sexual contacts to prevent recurrent infection. Our findings are consistent with venereal transmission of giardiasis.
T H E ORGANISM Giardia lamblia is an intestinal flagellate that can produce asymptomatic infection or cause an enteritis with symptoms ranging from acute diarrhea to chronic malabsorption. The mode of transmission is through ingestion of water contaminated with Giardia organisms. Giardiasis has been found to be a common parasitic infection of travelers. Visitors to Leningrad, Soviet Union (1), skiers in Aspen, Colorado (2), and residents of Boulder, Colorado (3) have suffered from epidemic giardiasis. Direct person-to-person transmission in families and outbreaks in nurseries in America and Sweden have been reported (4). Giardia organisms are also more likely to infect or persist in those persons with hypogammaglobulinemia or selective IgA deficiency. We recently diagnosed giardiasis in two male homosexuals who had not traveled outside New York City. Since venereal transmission of shigellosis and amebiasis has been reported and there is a well-known association between gonorrheal proctitis and rectal intercourse, we have reviewed our experience with giardiasis to determine if there is a link between homosexual practice and giardiasis. Case Reports CASE 1
A 26-year-old white male homosexual experienced a 4.5-kg weight loss, crampy abdominal pain, and foul-smelling loose stools of 1 month's duration. The patient denied traveling outside New York City and recurrent diarrhea. He noted that two • F r o m the Division of Infectious Diseases and Gastroenterology, T h e New York Hospital-Cornell Medical Center; New York, New York.
Annals of Internal Medicine 88:801-803, 1978
of his male contacts had a history of diarrhea. Physical and proctoscopic examination findings were normal. Stool tested for ova and protozoa revealed Giardia lamblia cysts and trophozoites and Entamoeba histolytica trophozoites. Complete blood count and serum Immunoelectrophoresis were normal. The patient was treated with tetracycline, 250 mg four times daily, and quinacrine, 100 mg three times daily, for 7 days, and diiodohydroxyquin, 650 mg three times daily, for 3 weeks. At follow-up 1 month later, his diarrhea had ceased and he had gained 7 kg. Stool examination was negative. He returned 1 month later with serum-positive hepatitis and foul-smelling diarrhea. Repeat stool examination revealed Giardia lamblia cysts; treatment with quinacrine, 100 mg three times daily for 7 days, resulted in negative stool for ova and protozoa. CASE 2
A 32-year-old white male homosexual had periumbilical cramps and loose, foul-smelling, nonbloody stools for 2 months. Physical and proctoscopic examination findings were normal. The patient denied traveling outside New York City, previous history of diarrhea, or milk intolerance. Stools for ova and protozoa revealed Giardia lamblia cysts. He was treated with quinacrine with relief of his symptoms. Follow-up stool examination was negative. Two months after treatment the patient returned with recurrent foul-smelling diarrhea and abdominal cramps. Stool examination was again positive for giardial cysts. He was again treated with quinacrine with resolution of his symptoms. Follow-up stool specimens have been negative. Stool specimens of the patient's sexual contacts have been unavailable for examination. These cases demonstrate that recurrence of symptoms is likely unless sexual partners are identified and treated. Most patients have abdominal complaints of mild to moderate degree that include foul-smelling, loose, frequent stools associated with nausea and crampy abdominal pain. A modest weight loss is also noted, depending on the duration of symptoms. Review of Giardiasis Cases at The New York Hospital
The medical records of all patients from whom Giardia lamblia was isolated in stool specimens submitted to The New York Hospital parasitology laboratory during a 5year period from 1 July 1971 through 30 June 1976 were reviewed. The study group included all patients over the age of 15 at the time of infection. Medical records of all patients were evaluated for sex, travel history, sexual preference, associated diseases, and history of venereal diseases. Patients were considered homosexual if this sexual preference was stated in the medical work-up or if follow-up discussions with the patient's physician revealed the patient to be homosexual. Associated diseases for which the medical record was checked included amebiasis, shigellosis, gonorrhea, syphilis, and hepatitis. © 1 9 7 8 American College of Physicians
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801
Table 1. Study Population with Giardiasis
Patient Group
Travelers Nontravelers Immunodeficiency
Meni
Women
Cases (n = 89)
Percent
Cases (« = 44)
Percent
67 19* 3
(75) (22) (3)
41 2 1
(94) (4) (2)
* All homosexuals.
One hundred forty-six isolates of Giardia lamblia were obtained from both male and female patients. Ninetythree of these isolates were from men and 53 from women. Records on four male patients and nine female patients were unavailable for evaluation. Thus, the study population included 89 male and 44 female patients. As shown in Table 1, 67 men (75%) and 41 women (94%) had recently traveled to areas frequently associated with giardiasis. Two of the male travelers were homosexuals. Four patients (three men and one woman) had an associated immunodeficiency disease. The remaining 19 patients (22%) had not traveled outside New York City and were all homosexuals. Two women had not traveled outside of New York City. How they acquired the infection could not be ascertained. Using chi-square analysis the number of male nontravelers with giardiasis was statistically different from the number of female nontravelers (p < 0.01). The percentage of male homosexuals in this group (100%) was significantly different from the percentage of male homosexuals seen at The New York Hospital clinics (2.5%) (5). Table 2 indicates the areas of the world that the traveling patients visited. This information was available from 101 of the 108 travelers. Most had traveled to Latin America and the Caribbean (55%). Other prominent areas where travelers acquired Giardia included India (11%), the Far East (9%), and Russia (9%). A history of previous venereal diseases was common in the 21 male homosexuals. Six (29%) of the homosexual men had had syphilis; three (14%), gonorrhea; five (23%), amebiasis; six (29%), shigellosis; and six (29%), hepatitis. All of these infections are transmitted venereally and are prevalent in the homosexual population. Sufficient data were not available to evaluate the heterosexual men or the women for history of previous venereal disease.
No mention was made as to whether their remaining patients were immunodeficient or homosexual. The actual prevalence of homosexuals who harbor giardial organisms is probably greater than that found in this series of symptomatic men because giardiasis can often be asymptomatic. Rectal intercourse followed by oral-genital sex or oral-rectal sexual activity could provide the mode of transmission of giardiasis in the homosexual population. Recently Meyers, Kuharic, and Holmes (7) described six male homosexuals with symptomatic giardiasis, four of whom were members of the same household. At least four of the six had had oral-anal contact with other infected members of the group, and direct fecal-oral transmission was proposed as the mode of transmission. In a study of the transmission of hepatitis B among homosexuals, more than half of the homosexual population reported 10 or more partners in a 6-month period (8). Thus spread of a disease such as giardiasis could reach epidemic proportions rapidly. Spread is also accentuated by the relatively short period from infection to excretion of cysts (9 days in experimental infection [9]) and by the potentially long period of asymptomatic infection. The observation that adult men with symptomatic giardiasis who have no travel history are often homosexual is important, because it requires that the patient's partners, even if asymptomatic, be contacted to have stool examination for ova and protozoa to identify potential sources of reinfection. The patient should abstain from sexual activity until treatment has eradicated Giardia organisms from his stools. Patients with giardiasis should also be screened for other venereal diseases that have a high prevalence in the homosexual population, including syphilis, gonorrhea, amebiasis, shigellosis, and hepatitis. In 1976 Kean (10) described a homosexual man with recurrent amebiasis who was believed to have been infected and reinfected during his sexual relations. We have found that 40% of adult men with amebiasis seen at The New York Hospital during a 5-year period were homosexuals (11). Drusin and colleagues (5) reported that 57% of nontraveling men infected with shigellosis were homosexual. When isolated, Giardia lamblia should be considered a pathogen and should be treated with quinacrine, 100 mg three times daily for 5 to 7 days, or metronidazole, 250 mg three times daily for 10 days (12). Stool examination should be obtained after completion of treatment.
Discussion
Giardia lamblia caused symptomatic disease in three distinct groups seen at The New York Hospital: travelers to endemic areas; patients with immunodeficiency diseases; and male homosexuals. These groups accounted for all cases of giardiasis in adults seen during the 5-year study period. Most patients had traveled to endemic areas such as Latin America, India, or Russia. Babb, Peck, and Vescia (6) reported that 83% of their patients in whom Giardia organisms were isolated had traveled outside the United States and that symptoms began during the trip or shortly after returning to the United States. 302
Table 2. Travel Areas of Patients with Giardiasis Area Mexico and the Caribbean South America India Far East Russia Mediterranean Africa and Middle East Rocky Mountains
Patients (n = 101) 41 14 11 9 9 7 7 3
June 1978 • Annals of Internal Medicine • Volume 88 • Number 6
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On the basis of our experience, giardiasis should be added to the growing list of venereally transmitted diseases. ACKNOWLEDGMENTS: Dr. Jones is the recipient of N I H Career Development Award AI 70754. Dr. Schmerin is supported by N I H Training Grant AM 07142. • Requests for reprints should be addressed to Thomas C. Jones, M.D.; 1300 York Avenue; New York, NY 10021. Received 19 August 1977; revision accepted 16 January 1978.
References 1. BRODSKY RE, SPENCER HC, S C H U L T Z MG: Giardiasis in American
travelers to the Soviet Union. JInfect
Dis 130:319-323, 1974
5. D R U S I N LM, G E N V E R T G, T O P F - O L S T E I N B, L E V Y - Z O M B E C K E: Shi-
gellosis. Another sexually transmitted disease? Br J Vener Dis 52:348350, 1976 6. BABB RR, PECK OC, VESCIA G F : Giardiasis—a cause of traveler's diarrhea. JAMA 217:1359-1361, 1971 7. MEYERS JD, KUHARIC HA, HOLMES KK: Giardia lamblia infection in homosexual men. Br J Vener Dis 55:54-55, 1977 8. SZUNESS W, M U C H MI, P R I N C E AM, H O O F N A G L E JH, C H E R U B I N CE,
HARLEY EJ, BLOCK GH: On the role of sexual behavior in the spread of hepatitis B infection. Ann Intern Med 83:489-495, 1975 9. R E N D T O R F F FC: The experimental transmission of human intestinal protozoan parasites. Giardia lamblia cysts given in capsules. Am J Hyg 59:209-220, 1954 10. K E A N BH: Venereal amebiasis. NY State J Med 76:930-931, 1976 11. SCHMERIN MJ, G E L S T O N A, J O N E S TC: Amebiasis—an
2. M O O R E GT, CROSS WM, M C G U I R E D, M O L L O H A N CS, G L E A S O N N N ,
H E A L Y GR, N E W T O N LH: Epidemic giardiasis at a ski resort. NEngl Med 281:402-407, 1969 3. SCHULTZ MG: Giardiasis. JAMA 233:1383-1384, 1975
4. ORMISTON G, TAYLOR J, WILSON GS: Enteritis in a nursery home associated with Giardia lamblia. Br Med J 2:151-154, 1942
J
increasing
problem among homosexuals in New York City. JAMA 238:1386-1387, 1977 12. Drugs for parasitic infection. Med Lett Drugs Ther 16 (2):5-12, 18 January 1974
Schmerin et al. • Giardiasis
Downloaded From: http://annals.org/pdfaccess.ashx?url=/data/journals/aim/19534/ by a University of California San Diego User on 01/24/2017
803
M.D.; THOMAS C. JONES,
M.D.,
F.A.C.P.; and HARVEY
KLEIN,
M.D.; New York, New York
Giardiasis is a common gastrointestinal illness among travelers. Recently an increased prevalence of giardiasis in men who had not traveled outside New York City was seen at The New York Hospital and was found to be due to transmission of this disease among homosexuals. Cases of giardiasis for a 5-year period were then reviewed, and it was discovered that 19 male patients who had not traveled or had an immunodeficiency disease were homosexuals. This accounted for 2 2 % of the adult men with giardiasis during that period. Adult women with giardiasis usually were either travelers or had an immunodeficiency disease ( 9 6 % ) . It is important to obtain a sexual history in these patients and treat sexual contacts to prevent recurrent infection. Our findings are consistent with venereal transmission of giardiasis.
T H E ORGANISM Giardia lamblia is an intestinal flagellate that can produce asymptomatic infection or cause an enteritis with symptoms ranging from acute diarrhea to chronic malabsorption. The mode of transmission is through ingestion of water contaminated with Giardia organisms. Giardiasis has been found to be a common parasitic infection of travelers. Visitors to Leningrad, Soviet Union (1), skiers in Aspen, Colorado (2), and residents of Boulder, Colorado (3) have suffered from epidemic giardiasis. Direct person-to-person transmission in families and outbreaks in nurseries in America and Sweden have been reported (4). Giardia organisms are also more likely to infect or persist in those persons with hypogammaglobulinemia or selective IgA deficiency. We recently diagnosed giardiasis in two male homosexuals who had not traveled outside New York City. Since venereal transmission of shigellosis and amebiasis has been reported and there is a well-known association between gonorrheal proctitis and rectal intercourse, we have reviewed our experience with giardiasis to determine if there is a link between homosexual practice and giardiasis. Case Reports CASE 1
A 26-year-old white male homosexual experienced a 4.5-kg weight loss, crampy abdominal pain, and foul-smelling loose stools of 1 month's duration. The patient denied traveling outside New York City and recurrent diarrhea. He noted that two • F r o m the Division of Infectious Diseases and Gastroenterology, T h e New York Hospital-Cornell Medical Center; New York, New York.
Annals of Internal Medicine 88:801-803, 1978
of his male contacts had a history of diarrhea. Physical and proctoscopic examination findings were normal. Stool tested for ova and protozoa revealed Giardia lamblia cysts and trophozoites and Entamoeba histolytica trophozoites. Complete blood count and serum Immunoelectrophoresis were normal. The patient was treated with tetracycline, 250 mg four times daily, and quinacrine, 100 mg three times daily, for 7 days, and diiodohydroxyquin, 650 mg three times daily, for 3 weeks. At follow-up 1 month later, his diarrhea had ceased and he had gained 7 kg. Stool examination was negative. He returned 1 month later with serum-positive hepatitis and foul-smelling diarrhea. Repeat stool examination revealed Giardia lamblia cysts; treatment with quinacrine, 100 mg three times daily for 7 days, resulted in negative stool for ova and protozoa. CASE 2
A 32-year-old white male homosexual had periumbilical cramps and loose, foul-smelling, nonbloody stools for 2 months. Physical and proctoscopic examination findings were normal. The patient denied traveling outside New York City, previous history of diarrhea, or milk intolerance. Stools for ova and protozoa revealed Giardia lamblia cysts. He was treated with quinacrine with relief of his symptoms. Follow-up stool examination was negative. Two months after treatment the patient returned with recurrent foul-smelling diarrhea and abdominal cramps. Stool examination was again positive for giardial cysts. He was again treated with quinacrine with resolution of his symptoms. Follow-up stool specimens have been negative. Stool specimens of the patient's sexual contacts have been unavailable for examination. These cases demonstrate that recurrence of symptoms is likely unless sexual partners are identified and treated. Most patients have abdominal complaints of mild to moderate degree that include foul-smelling, loose, frequent stools associated with nausea and crampy abdominal pain. A modest weight loss is also noted, depending on the duration of symptoms. Review of Giardiasis Cases at The New York Hospital
The medical records of all patients from whom Giardia lamblia was isolated in stool specimens submitted to The New York Hospital parasitology laboratory during a 5year period from 1 July 1971 through 30 June 1976 were reviewed. The study group included all patients over the age of 15 at the time of infection. Medical records of all patients were evaluated for sex, travel history, sexual preference, associated diseases, and history of venereal diseases. Patients were considered homosexual if this sexual preference was stated in the medical work-up or if follow-up discussions with the patient's physician revealed the patient to be homosexual. Associated diseases for which the medical record was checked included amebiasis, shigellosis, gonorrhea, syphilis, and hepatitis. © 1 9 7 8 American College of Physicians
Downloaded From: http://annals.org/pdfaccess.ashx?url=/data/journals/aim/19534/ by a University of California San Diego User on 01/24/2017
801
Table 1. Study Population with Giardiasis
Patient Group
Travelers Nontravelers Immunodeficiency
Meni
Women
Cases (n = 89)
Percent
Cases (« = 44)
Percent
67 19* 3
(75) (22) (3)
41 2 1
(94) (4) (2)
* All homosexuals.
One hundred forty-six isolates of Giardia lamblia were obtained from both male and female patients. Ninetythree of these isolates were from men and 53 from women. Records on four male patients and nine female patients were unavailable for evaluation. Thus, the study population included 89 male and 44 female patients. As shown in Table 1, 67 men (75%) and 41 women (94%) had recently traveled to areas frequently associated with giardiasis. Two of the male travelers were homosexuals. Four patients (three men and one woman) had an associated immunodeficiency disease. The remaining 19 patients (22%) had not traveled outside New York City and were all homosexuals. Two women had not traveled outside of New York City. How they acquired the infection could not be ascertained. Using chi-square analysis the number of male nontravelers with giardiasis was statistically different from the number of female nontravelers (p < 0.01). The percentage of male homosexuals in this group (100%) was significantly different from the percentage of male homosexuals seen at The New York Hospital clinics (2.5%) (5). Table 2 indicates the areas of the world that the traveling patients visited. This information was available from 101 of the 108 travelers. Most had traveled to Latin America and the Caribbean (55%). Other prominent areas where travelers acquired Giardia included India (11%), the Far East (9%), and Russia (9%). A history of previous venereal diseases was common in the 21 male homosexuals. Six (29%) of the homosexual men had had syphilis; three (14%), gonorrhea; five (23%), amebiasis; six (29%), shigellosis; and six (29%), hepatitis. All of these infections are transmitted venereally and are prevalent in the homosexual population. Sufficient data were not available to evaluate the heterosexual men or the women for history of previous venereal disease.
No mention was made as to whether their remaining patients were immunodeficient or homosexual. The actual prevalence of homosexuals who harbor giardial organisms is probably greater than that found in this series of symptomatic men because giardiasis can often be asymptomatic. Rectal intercourse followed by oral-genital sex or oral-rectal sexual activity could provide the mode of transmission of giardiasis in the homosexual population. Recently Meyers, Kuharic, and Holmes (7) described six male homosexuals with symptomatic giardiasis, four of whom were members of the same household. At least four of the six had had oral-anal contact with other infected members of the group, and direct fecal-oral transmission was proposed as the mode of transmission. In a study of the transmission of hepatitis B among homosexuals, more than half of the homosexual population reported 10 or more partners in a 6-month period (8). Thus spread of a disease such as giardiasis could reach epidemic proportions rapidly. Spread is also accentuated by the relatively short period from infection to excretion of cysts (9 days in experimental infection [9]) and by the potentially long period of asymptomatic infection. The observation that adult men with symptomatic giardiasis who have no travel history are often homosexual is important, because it requires that the patient's partners, even if asymptomatic, be contacted to have stool examination for ova and protozoa to identify potential sources of reinfection. The patient should abstain from sexual activity until treatment has eradicated Giardia organisms from his stools. Patients with giardiasis should also be screened for other venereal diseases that have a high prevalence in the homosexual population, including syphilis, gonorrhea, amebiasis, shigellosis, and hepatitis. In 1976 Kean (10) described a homosexual man with recurrent amebiasis who was believed to have been infected and reinfected during his sexual relations. We have found that 40% of adult men with amebiasis seen at The New York Hospital during a 5-year period were homosexuals (11). Drusin and colleagues (5) reported that 57% of nontraveling men infected with shigellosis were homosexual. When isolated, Giardia lamblia should be considered a pathogen and should be treated with quinacrine, 100 mg three times daily for 5 to 7 days, or metronidazole, 250 mg three times daily for 10 days (12). Stool examination should be obtained after completion of treatment.
Discussion
Giardia lamblia caused symptomatic disease in three distinct groups seen at The New York Hospital: travelers to endemic areas; patients with immunodeficiency diseases; and male homosexuals. These groups accounted for all cases of giardiasis in adults seen during the 5-year study period. Most patients had traveled to endemic areas such as Latin America, India, or Russia. Babb, Peck, and Vescia (6) reported that 83% of their patients in whom Giardia organisms were isolated had traveled outside the United States and that symptoms began during the trip or shortly after returning to the United States. 302
Table 2. Travel Areas of Patients with Giardiasis Area Mexico and the Caribbean South America India Far East Russia Mediterranean Africa and Middle East Rocky Mountains
Patients (n = 101) 41 14 11 9 9 7 7 3
June 1978 • Annals of Internal Medicine • Volume 88 • Number 6
Downloaded From: http://annals.org/pdfaccess.ashx?url=/data/journals/aim/19534/ by a University of California San Diego User on 01/24/2017
On the basis of our experience, giardiasis should be added to the growing list of venereally transmitted diseases. ACKNOWLEDGMENTS: Dr. Jones is the recipient of N I H Career Development Award AI 70754. Dr. Schmerin is supported by N I H Training Grant AM 07142. • Requests for reprints should be addressed to Thomas C. Jones, M.D.; 1300 York Avenue; New York, NY 10021. Received 19 August 1977; revision accepted 16 January 1978.
References 1. BRODSKY RE, SPENCER HC, S C H U L T Z MG: Giardiasis in American
travelers to the Soviet Union. JInfect
Dis 130:319-323, 1974
5. D R U S I N LM, G E N V E R T G, T O P F - O L S T E I N B, L E V Y - Z O M B E C K E: Shi-
gellosis. Another sexually transmitted disease? Br J Vener Dis 52:348350, 1976 6. BABB RR, PECK OC, VESCIA G F : Giardiasis—a cause of traveler's diarrhea. JAMA 217:1359-1361, 1971 7. MEYERS JD, KUHARIC HA, HOLMES KK: Giardia lamblia infection in homosexual men. Br J Vener Dis 55:54-55, 1977 8. SZUNESS W, M U C H MI, P R I N C E AM, H O O F N A G L E JH, C H E R U B I N CE,
HARLEY EJ, BLOCK GH: On the role of sexual behavior in the spread of hepatitis B infection. Ann Intern Med 83:489-495, 1975 9. R E N D T O R F F FC: The experimental transmission of human intestinal protozoan parasites. Giardia lamblia cysts given in capsules. Am J Hyg 59:209-220, 1954 10. K E A N BH: Venereal amebiasis. NY State J Med 76:930-931, 1976 11. SCHMERIN MJ, G E L S T O N A, J O N E S TC: Amebiasis—an
2. M O O R E GT, CROSS WM, M C G U I R E D, M O L L O H A N CS, G L E A S O N N N ,
H E A L Y GR, N E W T O N LH: Epidemic giardiasis at a ski resort. NEngl Med 281:402-407, 1969 3. SCHULTZ MG: Giardiasis. JAMA 233:1383-1384, 1975
4. ORMISTON G, TAYLOR J, WILSON GS: Enteritis in a nursery home associated with Giardia lamblia. Br Med J 2:151-154, 1942
J
increasing
problem among homosexuals in New York City. JAMA 238:1386-1387, 1977 12. Drugs for parasitic infection. Med Lett Drugs Ther 16 (2):5-12, 18 January 1974
Schmerin et al. • Giardiasis
Downloaded From: http://annals.org/pdfaccess.ashx?url=/data/journals/aim/19534/ by a University of California San Diego User on 01/24/2017
803
