Cancer in a Population-based Cohort of Men and Women in Registered Homosexual Partnerships

Morten Frisch1,, Else Smith2, Andrew Grulich3 and Christoffer Johansen4

1 Department of Epidemiology Research, Danish Epidemiology Science Center, Statens Serum Institut, Copenhagen, Denmark.
2 Department of Epidemiology, Statens Serum Institut, Copenhagen, Denmark.
3 National Centre in HIV Epidemiology and Clinical Research, Sydney, New South Wales, Australia.
4 Danish Cancer Society, Institute of Cancer Epidemiology, Copenhagen, Denmark.

Received for publication September 26, 2002; accepted for publication November 19, 2002.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cancer patterns among broad populations of homosexual men and women have not been studied systematically. The authors followed 1,614 women and 3,391 men in Denmark for cancer from their first registration for marriage-like homosexual partnership between 1989 and 1997. Ratios of observed to expected cancers measured relative risk. Women in homosexual partnerships had cancer risks similar to those of Danish women in general (overall relative risk (RR) = 0.9, 95% confidence interval (CI): 0.6, 1.4), but only one woman developed cervical carcinoma in situ versus 5.8 women expected (RR = 0.2, 95% CI: 0.0, 0.97). Overall, men in homosexual partnerships were at elevated cancer risk (RR = 2.1, 95% CI: 1.8, 2.5), due mainly to human immunodeficiency virus (HIV)/acquired immunodeficiency syndrome (AIDS)-associated Kaposi’s sarcoma (RR = 136, 95% CI: 96, 186) and non-Hodgkin’s lymphoma (RR = 15.1, 95% CI: 10.4, 21.4). Anal squamous carcinoma also occurred in excess (RR = 31.2, 95% CI: 8.4, 79.8). After exclusion of Kaposi’s sarcoma, non-Hodgkin’s lymphoma, and anal squamous carcinoma, no unusual cancer risk remained (RR = 1.0, 95% CI: 0.8, 1.3). With anal squamous carcinoma and HIV/AIDS-associated cancers as notable exceptions in men, cancer incidence rates among homosexual persons in marriage-like partnerships are similar to those prevailing in society at large.

acquired immunodeficiency syndrome; anus neoplasms; cervix neoplasms; HIV; homosexuality; lymphoma, non-Hodgkin; sarcoma, Kaposi; tonsillar neoplasms

Abbreviations: Abbreviations: AIDS, acquired immunodeficiency syndrome; CI, confidence interval; HIV, human immunodeficiency virus; RR, relative risk.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In Denmark, homosexuality was cancelled from official disease classifications in 1981, and parliament passed a law in 1989, the first of its kind in the world, that enabled homosexual couples to establish marriage-like partnerships with legal implications largely similar to those applying for heterosexual marriages (1). Following the World Health Organization’s omission of homosexuality from the 10th Revision of the International Classification of Diseases published in 1992 (2), laws ensuring comprehensive legal recognition of same-sex partnerships were passed in several other European countries, including Norway in 1993, Sweden in 1994, Iceland in 1996, Hungary in 1996, the Netherlands in 1997, France in 1999, and Germany in 2001 (3). With increasing levels of both individual and societal acceptance, physicians will face new challenges in their contact with homosexual patients. Many contacts with the health-care system need no differentiation according to sexual orientation, but there may be areas where consideration of sexuality will qualify treatment and improve advice to patients (4, 5). To this end, better knowledge about health issues pertinent to this group is needed from studies of well-defined broad groups of homosexual men and women. In this article, we used data from the population-based Danish Cancer Registry to investigate the cancer profile of all men and women in Denmark who had one or more records of registered homosexual partnership between 1989 and 1997.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Since 1968, the Civil Registration System in Denmark has kept continuously updated files on basic demographic variables of its citizens (6). With a unique 10-digit personal identification number as key, recorded information includes name, date of birth, marital status, emigration, and vital status. We identified a total of 5,031 persons whose marital status was recorded at least once as registered homosexual partnership between October 1, 1989, and December 31, 1997. We excluded two persons who died from the acquired immunodeficiency syndrome (AIDS) on their partnership date and 24 persons who had emigrated from Denmark before their partnership date, because these persons contributed no observation time to the study.

We used identity-secure data linkage on the files of the national AIDS registry (in operation since 1983, including Danish AIDS cases diagnosed since 1980 (7)) and the Danish Cancer Registry (in operation since 1943 (8)) to assess AIDS status and cancer outcomes in the cohort. Information about human immunodeficiency virus (HIV) status could not be established for all cohort members, because registration of HIV in Denmark (unlike registration for cancer and AIDS) is not person identifiable (9). For all 5,005 persons (1,614 women and 3,391 men), follow-up for cancer started on the date of first partnership (date of AIDS diagnosis in a supplementary analysis restricted to persons with AIDS) and ended on the date of death (9.8 percent), emigration (3.9 percent), disappearance (0.4 percent), or December 31, 1997 (85.9 percent), whichever occurred first. In all analyses, whether stratified by sex, age at first partnership (below or above the median), or AIDS status, observed cancers were compared with the numbers expected based on cancer incidence rates for the entire Danish population. Specifically, population cancer incidence rates stratified by sex, age in 5-year groups, and 5-year calendar periods were multiplied by the corresponding stratum-specific person-years of observation, and these contributions were summed over strata to determine the expected numbers for any given type of cancer. In all analyses, the ratios of observed to expected cancers (standardized incidence ratios) served as measures of the relative risk. Assuming a Poisson distribution of the observed cancers, we calculated 95 percent confidence intervals for the relative risks using Byar’s approximation (10).

Whether HIV-related immunosuppression contributes to the previously reported increased risk of invasive anal squamous carcinoma in homosexual men (11) remains unclear. To qualify the interpretation of findings for this particular cancer, we sought additional information about HIV infection that had not yet progressed to AIDS in the patients’ hospital files.

The study was approved by the Data Inspection Board in Denmark (approval numbers 1998-1200-179 and 2001-41-1239).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The cohort of 1,614 women and 3,391 men in registered homosexual partnerships was followed over a total of 22,255 person-years for development of cancer (average, 4.1 years for women and 4.6 years for men). The median age at first partnership date was 38 years, being 37 (range, 18–80) years for women and 38 (range, 18–87) years for men. Among women and men, 22 percent and 13 percent, respectively, had a record of one or more heterosexual marriages before the first registered homosexual partnership. Selected background characteristics of the study cohort are presented in table 1.


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TABLE 1. Characteristics of 1,614 women and 3,391 men in registered homosexual partnerships, Denmark, 1989–1997
 
Women
Cancer incidence among 1,614 homosexually partnered women differed little from that of Danish women in general, both overall (relative risk (RR) = 0.9, 95 percent confidence interval (CI): 0.6, 1.4; n = 24 cancers) and for each individual major organ system (table 2). The incidence of invasive cervical carcinoma was close to the expected (RR = 1.8, 95 percent CI: 0.4, 5.2; n = 3), but only one woman was recorded with cervical carcinoma in situ versus 5.8 women expected, thus representing a statistically significant deficit (RR = 0.2, 95 percent CI: 0.0, 0.97). Three cancers of the uterine corpus (RR = 3.4, 95 percent CI: 0.7, 10.0) and four lung cancers (RR = 2.1, 95 percent CI: 0.6, 5.4) were in excess of the expected, yet insignificantly so. No unusual occurrence was seen for ovarian cancer or breast cancer (table 2). Results were unchanged after restriction of the analysis to those 1,570 women with no record of cancer prior to first registration as a homosexual partner (RR = 0.9, 95 percent CI: 0.6, 1.4; n = 23 cancers).


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TABLE 2. Invasive cancers and cervical carcinoma in situ among 1,614 women in registered homosexual partnerships, Denmark, 1989–1997
 
Men
The overall risk of cancer among 3,391 men in registered homosexual partnerships was increased twofold (RR = 2.1, 95 percent CI: 1.8, 2.5; n = 139) (table 3). This excess was due almost entirely to high numbers of Kaposi’s sarcoma (RR = 136, 95 percent CI: 96, 186; n = 38) and non-Hodgkin’s lymphoma (RR = 15.1, 95 percent CI: 10.4, 21.4; n = 32) cases. A statistically significant excess was also seen for anal squamous carcinoma (RR = 31.2, 95 percent CI: 8.4, 79.8; n = 4). Hospital files and AIDS registry information for the anal cancer patients showed that three men had been HIV positive for at least 2, 4, and 9 years, respectively, prior to the anal cancer diagnosis, and two of these patients developed clinical AIDS 2 years before and 1 year after the anal cancer, respectively. The fourth anal cancer patient had undetermined HIV status. There was an excess of cancers of the buccal cavity and pharynx (RR = 2.5, 95 percent CI: 1.1, 5.8; n = 7), of which two cases were oral Kaposi’s sarcoma in patients with AIDS. Two pharyngeal cancers were tonsillar squamous carcinoma (RR = 5.6, 95 percent CI: 0.6, 20.2). After exclusion of Kaposi’s sarcoma, non-Hodgkin’s lymphoma, and anal squamous carcinoma, there remained no overall excess risk of cancer (RR = 1.0, 95 percent CI: 0.8, 1.3; n = 65) (table 3). A similar negative overall association was seen when restricting the analysis to those 3,054 men who were not recorded as having developed AIDS through year 2001 (all cancers: RR = 1.0, 95 percent CI: 0.8, 1.3; n = 65) (table 3). There was no significant excess of tobacco- or alcohol-associated cancers of the respiratory organs, liver, pancreas, or urinary organs, but power was limited at each site. The results presented in table 3 were unchanged when analyses were restricted to men who had no record of cancer prior to their first registration as a homosexual partner (RR = 2.1, 95 percent CI: 1.8, 2.5; n = 131, for all cancers among 3,262 men regardless of AIDS status, and RR = 1.0, 95 percent CI: 0.8, 1.3; n = 59, for all cancers among 2,969 men without AIDS).


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TABLE 3. Invasive cancers among men in registered homosexual partnerships, Denmark, 1989–1997
 
Stratification of the cohort of all 3,391 men by age at first partnership (above or below the median) showed that the overall relative risk of cancer was considerably higher among men who were younger than 38 years at first partnership (RR = 7.2, 95 percent CI: 5.3, 9.6; n = 47) than among those who were 38 years or older (RR = 1.6, 95 percent CI: 1.3, 1.9; n = 92). No such difference was seen between women aged less than 38 years at first partnership (RR = 0.8, 95 percent CI: 0.2, 2.1; n = 4) and those aged 38 years or older (RR = 0.9, 95 percent CI: 0.6, 1.5; n = 20). Of the 47 cancers among men in the younger group, 21 were Kaposi’s sarcoma (RR = 141, 95 percent CI: 87, 216), 14 were non-Hodgkin’s lymphoma (RR = 35.7, 95 percent CI: 19.5, 59.9), and three were anal squamous carcinoma (RR = 150, 95 percent CI: 31, 437). After exclusion of Kaposi’s sarcoma, non-Hodgkin’s lymphoma, and anal squamous carcinoma, cancer risk was not significantly elevated in either group (RR = 1.5, 95 percent CI: 0.7, 2.9; n = 9, in the younger group vs. RR = 1.0, 95 percent CI: 0.8, 1.3; n = 56, in the older group).

A separate follow-up analysis from the time of AIDS diagnosis among 317 men whose AIDS diagnosis was in or before 1997 confirmed remarkably high relative risks for Kaposi’s sarcoma (RR = 3,838, 95 percent CI: 2,830, 5,089; n = 48) and non-Hodgkin’s lymphoma (RR = 442, 95 percent CI: 283, 657; n = 24). These observed numbers of cancers cannot be derived from table 3 because of different starting points for follow-up in the underlying analyses.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In industrialized parts of the world, the HIV/AIDS epidemic resulted in unprecedented focus on health issues among the subset of homosexual men who are HIV positive. Dramatically increased risks of Kaposi’s sarcoma, non-Hodgkin’s lymphoma, anal cancer, and certain other malignancies in HIV-positive homosexual men have been documented in large-scale epidemiologic studies (1215). In contrast, only limited data have been published on cancer in broader groups of homosexual men. In one study, Koblin et al. (16) studied 15,565 homosexual men in New York, New York, and San Francisco, California, two of the epicenters of the AIDS epidemic in the United States, but HIV antibody status was known only for 15 percent of the study subjects and, of these, most (78 percent) were HIV seropositive. Thus, analyses of the small HIV-negative subset were statistically unstable. A study from Pittsburgh, Pennsylvania, followed 769 HIV-seronegative homosexual men for 5,708 person-years and observed no unusual cancer pattern in these young men. Specifically, eight cancers other than nonmelanoma skin cancers occurred versus 8.1 expected (17). To the best of our knowledge, this is the first study of cancer patterns in a truly population-based cohort of homosexual men and women registered in marriage-like partnerships. All persons in Denmark who became a registered homosexual partner between 1989 and 1997 were eligible for study. We had a total of 22,255 person-years of follow-up for cancer, and cancer incidence rates in the cohort were compared with those of the general population in Denmark. With the notable exception of those 9–10 percent of homosexually partnered men who had or developed AIDS, our study shows that Danish men and women in registered homosexual partnerships generally have cancer risks similar to those of the population as a whole.

Despite its population-based nature, its virtually complete follow-up, and the high-quality national cancer registry data used to identify cancers in the cohort (8), some limitations of our study need careful consideration. It is unclear how representative the legally partnered men and women in our cohort are of all homosexual men and women. No official statistics provide estimates of the number and demographic characteristics of homosexual men and women in Denmark. The proportion of men who reported ever having experienced homosexual intercourse in a self-administered postal survey of sexual behavior in 1990 was 2.7 percent (18), yielding an estimated total of approximately 55,000 homosexual men of age 18 or more years in Denmark. If true, the 3,391 homosexually partnered men in our study would represent around only 6 percent of all homosexual men in Denmark. However, homosexual behavior is likely to be underreported in sexual behavior surveys (19), so the true proportion of all homosexual men and women in Denmark who registered in homosexual partnerships may well be even lower, probably in the order of one to a few percent.

What characteristics might plausibly differ between legally partnered and other homosexual men and women? Theoretically, HIV/AIDS and associated immunosuppression-associated cancers might be more common among unpartnered homosexual men in unstable relationships than among men in registered homosexual partnerships. However, we did observe a clear excess of such immunosuppression-associated cancers in the cohort, so the impact of HIV/AIDS was certainly present. Indeed, selection of individuals with AIDS into the cohort may have occurred, as illustrated by the two men who were excluded from the study because they died from AIDS on their respective partnership dates. It has been estimated that 8–10 percent of Danish homosexual men during the years covered by our study were HIV infected (9). In the current study, HIV status was unknown, but 337 of 3,391 men (10 percent) had AIDS, so rather than being a self-selected group of homosexual men at low risk of HIV/AIDS, our cohort of legally partnered men may well have been more directly affected by the HIV/AIDS epidemic than other homosexual men in Denmark. Importantly, since only a few specific cancers are convincingly related to AIDS-related immunosuppression (13), and since HIV infection with mild immune deficiency appears not to alter cancer risk materially (20), our findings for homosexually partnered men without AIDS are likely to reflect general cancer patterns among homosexually partnered, immunocompetent men.

We used standardized incidence ratios to estimate relative risks as is customary in population-based cohort studies with rare exposures. Standardized incidence ratios generally produce slightly conservative relative risk estimates, because observed cancers among the exposed (in this case people registered in homosexual partnerships) also contribute to the numerator of the population rates used to calculate expected cancers. The degree to which standardized incidence ratios produce conservative relative risk estimates depends on the proportion of exposed persons in the total population and the size of the true relative risk, with larger bias toward the null for cancers with large differences in incidence between exposed and unexposed persons. Legally partnered homosexual men and women represent around only one in 1,000 adult Danes, so inclusion of cancers in this small group had no measurable impact on the population rates used to calculate expected cancers. Specifically, with an exposure frequency of one per thousand in the population, standardized incidence ratios will be no more than 0.3 percent too conservative in all situations with true relative risks of between 0.33 and 3. Consequently, our statistically insignificant relative risks close to unity (as estimated by standardized incidence ratios) most likely reflect that, for most cancers, there is no quantitatively important difference in cancer incidence between persons in registered homosexual partnerships and other people in Denmark. However, our findings of significantly and highly increased relative risks for Kaposi’s sarcoma, non-Hodgkin’s lymphoma, and anal squamous carcinoma among men and of significantly reduced relative risk for cervical carcinoma in situ among women most likely represent conservative estimates of underlying true associations.

Although the information we used to identify homosexual persons is likely to be highly specific (few persons in registered same-sex partnerships not homosexual), it was highly insensitive if intended to capture all the homosexual persons in Denmark (most homosexual persons not registered in same-sex partnerships). Consequently, generalization of our findings for legally partnered homosexual persons to the broader population of homosexual men and women in Denmark may not be justified. Specifically, our cohort study may not reliably describe cancer patterns among homosexual men and women who live alone or with a legally unrecognized partner or those who keep their homosexuality in the closet.

Statistical power is another issue deserving comment. Our cohort was young, and the average follow-up period for cancer (4.4 years) was rather short. Consequently, our study lacks power to study cancer risks in homosexually partnered men and women of more advanced ages, and we had limited power to detect moderately increased risks for rare cancers. However, the risk for invasive anal squamous carcinoma, which is believed to be caused by certain types of sexually transmitted human papillomaviruses, notably type 16 (21), was significantly 31-fold elevated at a crude incidence of 25.6 per 100,000 person-years. A markedly elevated risk of anal cancer has been reported previously in homosexual men with HIV/AIDS (11, 20, 22, 23), but the possible role of immunosuppression remains unclear. Among HIV-positive men, the rate of human papillomavirus acquisition and progression to anal squamous intraepithelial lesions has been found to increase with decreasing levels of cellular immune competence as measured by CD4-positive T-lymphocyte cell concentrations (24, 25). However, convincing prospective evidence to show that immunosuppression increases the risk of anal carcinoma in situ and invasive anal cancer is lacking. The presence of extreme relative risks for these malignant lesions among homosexual men with AIDS (22) cannot be taken as evidence that immunosuppression plays a crucial role for in situ and invasive anal cancers. The apparent association with immunosuppression could be confounded by other etiologic factors that may differ between HIV-infected and HIV-uninfected men, for example, anal coinfections with multiple human papillomavirus types (26). Since only one of the four cases of anal cancer in the present study occurred in a potentially HIV-negative patient, the present study does not suggest the existence of an extreme risk of anal cancer in HIV-negative homosexual men. Although there may be reason to consider the introduction of screening for anal cancer precursor lesions in HIV-positive homosexual men (27), the approximately 17-fold increased risk of anal cancer in homosexually partnered men without AIDS (based on two patients, of whom only one was potentially HIV negative) provides little support for the view that such screening should be introduced in broader populations of predominantly HIV-negative homosexual men (28).

Our finding of two cases of tonsillar squamous carcinoma represents an almost sixfold increased risk. Although this might be a chance finding, as indicated by a wide confidence interval that includes unity, it is worthy of notice that tonsillar cancer has recently been linked etiologically to anogenital cancer-associated human papillomaviruses (29, 30).

Health-related matters among homosexual women have been studied only sparsely (5). Our study helps to address empirically unsupported expectations of an excess of breast cancer and cervical cancer in these women (31, 32). We observed seven breast cancers (vs. 7.5 expected) in our cohort of 1,614 women, a finding that fails to suggest etiologic influence of factors specific to, or particularly prevalent among, homosexual women. The observed number of invasive cervical cancers was also close to the expected, but there was a statistically significant deficit of cervical carcinoma in situ. Although caution in interpretation is warranted because of small numbers, the significantly low incidence of cervical carcinoma in situ combined with an incidence of invasive cervical cancers close to that of the general Danish female population might reflect inadequate attendance to cervical cancer screening programs among homosexual women. Failure among homosexual women to attend generally recommended Papanicolaou smear screening programs has been reported in studies from the United States (33, 34). Homosexual women may consider themselves to be at low risk of cervical carcinoma. However, more than one in five women in our study had been heterosexually married prior to their first registered homosexual partnership, and others may have been heterosexually exposed to human papillomaviruses without marrying. In addition, human papillomavirus infections are not uncommon among homosexual women reporting no sexual encounters with men (34).

We observed a slight, yet insignificant, excess of uterine corpus cancers, which is in accordance with prior findings of higher endometrial cancer risk in single than married women (35). High socioeconomic status and unopposed estrogenic stimulation of the endometrium are associated with elevated risk of cancer of the uterine corpus (36). Our data do not include socioeconomic indicators, and the childbearing patterns, frequency of obesity, and use of exogenous estrogens in these women also remain unknown. However, because these risk factors for uterine corpus cancer are similarly associated with the risk of breast cancer, which was not increased, our data fail to support the existence of an unusual risk of these cancers in homosexual women.

Apart from HIV/AIDS-associated cancers and anal squamous carcinoma in men, Danish men and women in registered homosexual partnerships appear not to be at any unusual cancer risk compared with the general population. If, as in other countries, the significant deficit of cervical carcinoma in situ is due to inadequate screening among homosexual women, improved screening attendance may render invasive cervical cancer a rarity among these women in the future.


    ACKNOWLEDGMENTS
 
This study was supported by the Psychosocial Research Foundation of the Danish Cancer Society (grant 97-225-57).

The authors thank programmers Andrea Meersohn of the Danish Cancer Society and Katja Moreno of the National AIDS Registry for computer assistance.


    NOTES
 
Correspondence to Dr. Morten Frisch, Department of Epidemiology Research, Danish Epidemiology Science Center, Statens Serum Institut, 5 Artillerivej, DK-2300 Copenhagen, Denmark (e-mail: mfr{at}ssi.dk). Back


    REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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