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Continuing transmission of sexually transmitted diseases among patients infected with HIV-1 attending genitourinary medicine clinics in England and Wales

^a Public Health Laboratory Service, Communicable Disease Surveillance Centre, London NW9 5EQ, ^b Academic Department of Genitourinary Medicine, Mortimer Market Centre, London WC 6AY, ^c Public Health Laboratory Service, Virus Reference Division, London NW9 5HT

Correspondence to: Dr Catchpole.

Abstract

Objective: To determine whether those who are aware of being infected with HIV continue to adopt behaviours that place others at risk of HIV infection.
Design: Ongoing survey of current diagnosis of sexually transmitted disease and awareness of HIV infection among patients attending genitourinary medicine clinics.
Setting: Six genitourinary medicine clinics in England and Wales (two in London and four outside) participating in unlinked anonymous HIV serosurveillance during 1990-3.
Subjects: All attenders having blood drawn for syphilis serology for the first time during the calendar quarter of attendance.
Main outcome measures: The proportion of syphilis serology specimens with antibody to HIV-1 detected by unlinked anonymous testing of the residue. The proportion of attenders infected with HIV-1 who remained clinically undetected, and the proportion who had another recently acquired sexually transmitted disease.
Results: Of 85441 specimens tested, 2328 (2.7%) were positive for antibodies to HIV-1. About 30% of these specimens were from attenders whose HIV-1 infection remained clinically undetected. HIV-1 infection was found to coexist with another recently acquired sexually transmitted disease in 651 attenders, of whom 522 were homosexual or bisexual men. Of these, 245 (47%) already knew themselves to be infected with HIV-1. This proportion increased between 1990 and 1993.
Conclusions: A considerable proportion of patients infected with HIV-1 are not identified by voluntary confidential HIV testing in genitourinary medicine clinics. Substantial numbers of homosexual or bisexual men attending genitourinary medicine clinics continue to practise unsafe sex despite being aware of their infection with HIV-1.

Introduction

As the HIV epidemic evolves, important questions concerning current levels of infection, optimal strategies for detecting people infected with HIV in contact with health services, and the effectiveness of prevention programmes remain unanswered.¹ The occurrence of new episodes of other sexually transmitted diseases among people infected with HIV must be a strong indicator for continuing risk of HIV transmission in the sexually active population. If transmission of these other sexually transmitted diseases is also continuing among those who are aware of their HIV infection then this raises questions about the effectiveness of counselling after testing and the potential benefit of policies designed to encourage HIV testing.

The unlinked anonymous survey of HIV seroprevalence among attenders of genitourinary medicine clinics in England and Wales provided an opportunity to look at these questions because it collects data on current diagnoses of sexually transmitted diseases and patients' awareness of their HIV status, as well as the result of unlinked anonymous HIV tests.

Patients and methods

Six genitourinary medicine clinics and associated laboratories were selected by using the criteria of large case load and willingness to participate for a minimum of five years. Approval for the survey was obtained from the Public Health Laboratory Service and local ethics committees. The principles of the method of unlinked anonymous testing,² which minimises the participation bias inherent in voluntary confidential HIV case finding,^{3 4 5} were followed. The detailed methods applied in the clinics and that for laboratory tests are described elsewhere.⁶

All attenders, including those known to be positive for antibodies to HIV-1, having blood drawn for syphilis serology for the first time during the calendar quarter of attendance were eligible for inclusion in the survey. If patients declared that they had been diagnosed or were known to have been diagnosed as positive for HIV-1 before the current episode of attendance this was recorded on the survey form.

A limited dataset was collected for each eligible attender and was matched at the coordinating centre with the result of the test for HIV-1 on the unlinked anonymous residue of the syphilis serology sample for that attender. The analyses presented in this paper are based on a dataset that contained the following items: diagnosis of sexually transmitted disease for each attender (coded as on the statistical return (KC60) made by genitourinary medicine clinics to the Department of Health), calendar quarter of clinic attendance, age group, exposure category, previous awareness of being infected with HIV, and unlinked anonymous test result. Data indicating the clinic attended were not included within the database to prevent the remote risk of deductive disclosure.² Exposure categories used for the analysis were homosexual or bisexual men, heterosexual men, heterosexual women, and "other." Attenders known to inject drugs were included in the "other" exposure category and excluded from the homosexual or bisexual and heterosexual categories.

The diagnoses of sexually transmitted disease assigned to attenders were classified according to the likelihood that they indicated a history of recent unprotected sexual intercourse. Diagnoses listed in the box were classified as clinical indicators of recent high risk behaviour.

Cross contamination between some specimens was found to have occurred in one centre during the fourth quarter of 1991 and the first quarter of 1992. All data for the two quarters concerned were removed from the dataset used for the analyses presented in this paper.

Results

The results presented are for 85441 records for which a survey form and a corresponding laboratory result had been received by August 1994 for patients seen between the beginning of 1990 and the end of 1993 but exclude all patients seen in the last quarter of 1991 and the first quarter of 1992. Overall, 0.6% of eligible patients objected to testing, and specimens from these attenders remained untested. There were no significant differences in objection rates between exposure categories.

Four hundred and sixty four (27%) specimens positive for antibody to HIV-1 from homosexual or bisexual men, 96 (59%) from heterosexual men, and 59 (41%) from heterosexual women were from attenders whose HIV-1 infection remained clinically undetected at the end of that clinic episode (table 1). Two hundred and eighty three (16%) such specimens from homosexual or bisexual men, 24 (15%) from heterosexual men, and 29 (20%) from heterosexual women were from attenders whose infection was diagnosed during that clinic episode. The remaining positive specimens were from attenders already known to be infected with HIV-1 before that clinic episode.

Table 1--Awareness of infection with HIV-1 by exposure category by year. (Figures in
 brackets are percentages of all positive)
--------------------------------------------------------------------------------------------
                                         Specimens positive for antibody to HIV-1
--------------------------------------------------------------------------------------------
                                            Aware of                          Undetected
                                           infection with   New diagnosis   infection with
Category of                 Total (% of     HIV-1 before     during clinic  HIV-1 at end of
exposure    Total tested   total tested)   clinic episode   clinic episode  clinic episode
--------------------------------------------------------------------------------------------
Homosexual or bisexual men*:
 1990           1978         359 (18.1)       199 (55)         52 (14)         108 (30)
 1991           2810         451 (16.0)       244 (54)         78 (17)         129 (29)
 1992           2829         475 (16.8)       279 (59)         79 (17)         117 (25)
 1993           2977         440 (14.8)       256 (58)         74 (17)         110 (25)
  Total        10594        1725 (16.3)       978 (57)        283 (16)         464 (27)
Heterosexual men*:
 1990           7487          32 (0.4)         6 (19)           6 (19)          20 (63)
 1991           8115          38 (0.5)        13 (34)           5 (1)           20 (53)
 1992           8256          23 (0.3)         6 (13)           6 (13)          11 (48)
 1993          10109          71 (0.7)        19 (27)           7 (10)          45 (69)
  Total        33967         164 (0.5)        44 (27)          24 (15)          96 (59)
Heterosexual women*:
 1990           7217          21 (0.3)         6 (29)           3 (14)          12 (57)
 1991           8479          32 (0.4)        12 (38)           4 (13)          16 (50)
 1992           9155          42 (0.5)        17 (40)          10 (24)          15 (36)
 1993          11410          48 (0.4)        20 (42)          12 (25)          16 (33)
  Total        36261         143 (0.4)        55 (38)          29 (20)          59 (41)
Other/unknown exposure categories:
 1990           1215          69 (5.7)        42 (61)           7 (10)          20 (29)
 1991           1067          79 (7.4)        49 (62)          11 (14)          19 (24)
 1992            857          70 (8.2)        44 (63)          14 (20)          12 (17)
 1993           1480          78 (5.3)        58 (74)          12 (15)           8 (10)
  Total         4619         296 (6.4)       193 (65)          44 (15)          59 (20)
--------------------------------------------------------------------------------------------
Grand total    85441         2328 (2.7)      1270 (55)        380 (16)         678 (29)
--------------------------------------------------------------------------------------------
*Excludes attenders known to have injected drugs.

 Conditions likely to have been acquired
 through recent unprotected sexual
 intercourse
 KC60
 code     Condition
 A1-3     Infectious syphilis
 A9       Epidemiological treatment of suspected
          syphilis
 B1.4a-b  Other complicated gonorrhoea (excluding
          pelvic inflammatory disease and epididymitis)
 B1.1-3   Postpubertal uncomplicated gonorrhoea
 B1.4c    Gonococcal and chlamydial pelvic
          inflammatory disease and epididymitis
 B1.4b    Gonococcal pelvic inflammatory disease and
          epididymitis
 B2       Prepubertal gonorrhoea
 B4       Epidemiological treatment of suspected
          gonorrhoea
 C1-3     Chancroid/donovanosis/lymphogranuloma
          venereum
 C10A     Herpes simplex--first attack
 C11A     Wart virus infection--first attack
 C13A     Antigen positive viral hepatitis B
 C13B     Other viral hepatitis
 C4A      Postpubertal uncomplicated chlamydia
 C4B      Other complicated chlamydia (excluding
          pelvic inflammatory disease and epididymitis)
 C4C      Prepubertal chlamydia
 C4E      Epidemiological treatment of suspected
          chlamydia
 C4F      Chlamydial pelvic inflammatory disease and
          epididymitis
 C4G      Non-specific pelvic inflammatory disease and
          epididymitis
 C4H      Non-specific urethritis (excluding pelvic
          inflammatory disease and epididymitis)
 C4I      Epidemiological treatment of non-specific
          urethritis and related disease
 C5       Chlamydial infection/non-specific urethritis
          with arthritis
 C6A      Trichomoniasis
 C8-9     Scabies/pediculosis

The proportion of clinically undetected HIV-1 infections fell with age for homosexual or bisexual men (²=14.49; df=1; P=0.0001; table 2), heterosexual men (²=7.93; df=1; P=0.0049), and heterosexual women (²=6.49; df=1; P=0.0108).

Table 2--Awareness of HIV infection by age in homosexual or bisexual men positive for
 antibody to HIV-1, 1990-3
--------------------------------------------------------------------------------------
                                <20     20-24    25-34     35-44     >/=45
Detail                         years    years    years     years     years    Unknown
--------------------------------------------------------------------------------------
Known positive                    9      93       492       272       95        17
New diagnosis                     6      42       148        53       26         8
Undetected infection              3      67       259       102       25         8
With acute sexually transmitted  17      33        29        24       17        24
 disease

Among homosexual or bisexual men the proportion of specimens positive for antibody to HIV-1 that were from attenders not known to be infected with HIV before the clinic episode and that remained undetected fell from 30% (108/359) in 1990 to 25% (110/440) in 1993 (² for linear trend=4.49; df=1; P=0.0341). This proportion also fell for heterosexual women from 57% (12/21) in 1990 to 33% (16/20) in 1993 (² for linear trend=4.53; df=1; P=0.0333), whereas for heterosexual men there was no significant trend.

There were 30380 (36%) attendances for which the diagnosis of sexually transmitted disease indicated a high probability of recent unprotected sexual intercourse. Overall, 651 (2.1%) specimens from these attenders were positive for antibody to HIV-1 compared with 1677 of 55061 (3.0%) of specimens from attendances for which there was no acute sexually transmitted disease diagnosed.

Of the 1725 specimens from homosexual or bisexual men that were positive for antibody to HIV-1, 522 (30%) were from attenders with diagnoses of sexually transmitted disease that indicated recent unprotected sexual intercourse (table 3). This proportion declined from 34% (122/359) in 1990 to 30% (134/451) in 1991 and 29% in both 1992 (138/475) and 1993 (128/440). This decline was not significant. There was, however, a significant decline with age in the proportion of homosexual or bisexual men who were infected with HIV and an acute sexually transmitted disease and who attended a clinic (table 2), from a peak of 42% (33) at age 20-24 years to 19% (17) at age 45 years and over (² for linear trend=23.84; P=0.0000).

Table 3--Proportion of patients with evidence of probable high risk sexual behaviour by
exposure category in specimens from those whose samples were positive for antibody to
HIV-1
-------------------------------------------------------------------------------------------------------------------
Exposure category      No with acute sexually transmitted disease indicating recent risk behaviour/
and knowledge of                      total No positive for antibody to HIV-1 (%)
HIV infection before   --------------------------------------------------------------------------------------------
clinic visit                      1990             1991               1992             1993             Total
-------------------------------------------------------------------------------------------------------------------
Homosexual or bisexual men*
Aware of infection            49/199 (25)       52/244 (21)       74/279 (27)       71/256 (28)     246+/978 (25)
Not aware                     73/160 (46)       82/207 (40)       64/196 (33)       57/184 (31)     276/747 (37)
Heterosexual men*
Aware of infection             0/6               0/13              0/6               1/19 (5)         1/44 (2)
Not aware                     15/26 (58)        11/25 (44)         3/17 (18)        20/52 (38)       49/120 (41)
Heterosexual women*
Aware of infection             1/6 (17)          0/12              2/17 (12)         2/20 (10)        5/55 (9)
Not aware                      2/15 (13)         4/20 (20)         4/25 (16)         5/28 (18)       15/88 (17)
Other/unknown exposure categories
Aware of infection             8/42 (19)         9/49 (18)        11/44 (25)         4/58 (7)        32/193 (17)
Not aware                      7/27 (26)        11/30 (37)         5/26 (19)         4/20 (20)       27/103 (26)
-------------------------------------------------------------------------------------------------------------------
*Excludes attenders known to have injected drugs.
+Diagnoses: for 204 attendances the diagnoses included at least one of gonorrhoea (75), non-specific
urethritis (74), or anogenital herpes or anogenital warts (66); 42 attendances were for other conditions.

Of the 522 specimens positive for HIV-1 from homosexual or bisexual men attending with acute sexually transmitted diseases, 246 (47%) were from men known to be infected with HIV-1 before the clinic visit; this proportion increased significantly from 40% (49/122) in 1990 to 55% (71/128) in 1993 (²=12.01; df=3; P=0.0074, table 3 and figure).

View larger version (13K): [in this window] [in a new window]   Fig 1--Proportion of homosexual and bisexual men with HIV infection and sexually transmitted disease who were aware of their HIV infection

Of the 8869 specimens negative for HIV-1 from homosexual or bisexual men, 30% (2656) were from attenders who had a coexisting "acute sexually transmitted disease," whereas 25% (246) of the 978 specimens positive for HIV-1 from known infected homosexual or bisexual men and 37% (276) of the 747 specimens positive for HIV-1 from infected homosexual or bisexual men who were not known to be infected before the clinic episode were from attenders who had a coexisting "acute sexually transmitted disease" (²=28.12; df=2; P=0.0000).

Fifty (30%) of the 164 specimens positive for HIV-1 from heterosexual men were from attenders with an acute sexually transmitted disease (table 3). Only one of these specimens was from a man known to be infected with HIV-1 before the clinic visit.

Twenty (14%) of the 143 specimens positive for HIV-1 from heterosexual women were from attenders with an acute sexually transmitted disease (table 3). Five of these 20 specimens were from women known to be infected with HIV-1 before the clinic visit.

Discussion

This survey provides evidence that the application of current policy on voluntary confidential HIV testing in genitourinary medicine clinics in England and Wales fails to identify a substantial proportion of infected patients, particularly heterosexuals, but also homosexual or bisexual men. Even among infected homosexual or bisexual men who had an acute sexually transmitted disease, 43% remained clinically undetected at the end of that clinic episode; although some of these attenders may have refused the offer of an HIV test. Testing all homosexual or bisexual men with an acute sexually transmitted disease would detect only 54% of all attenders with HIV-1 infection that were unknown at the start of the clinic episode. Thus all homosexual or bisexual male attenders should be tested if all HIV infections are to be detected. It is encouraging, however, that the proportion of HIV-1 infections among homosexual or bisexual men and heterosexual women that remained undetected at the end of a clinic episode fell between 1990 and 1993.

The low number of objectors in all exposure categories implies that participation bias is unlikely to have had a major impact on the results. The results of this survey will, however, probably underestimate the true proportion of those known to be infected with HIV attending the participating clinics as patients attending for HIV care may be less likely to be tested for syphilis than other attenders⁷; although this could be offset by people with known infection being more regular attenders than other people. Prevalence estimates in this survey may also be lowered by the tendency, noted at several London clinics, for patients known to be positive for antibody to HIV-1 to seek treatment for an acute sexually transmitted disease at another clinic, where they chose not to reveal their HIV infection. These effects will lead to an overestimation of the proportion of attenders positive for HIV-1 who are not known to be positive by the attending clinic.

This study provides evidence of continuing unsafe sexual behaviour among homosexual or bisexual men infected with HIV-1 attending genitourinary medicine clinics up to the end of 1993. This is consistent with other data indicating an increase in the incidence of sexually transmitted diseases, including HIV, within the male homosexual or bisexual community in England and Wales between 1988 and 1990.⁸

It is of concern that the proportion knowing themselves to be HIV infected among homosexual or bisexual men positive for HIV-1 and with an acute sexually transmitted disease increased between 1990 and 1993, from 40% to 55%. Some of the cases of "acute sexually transmitted disease" may have been acquired through "safer" sexual practice--for example, oral sex⁹--or represent longstanding infections that were acquired before diagnosis of HIV-1 infection (although anogenital warts and anogenital herpes accounted for only 27% of these cases) or represent transmission between men mutually aware of their infections. It is, however, unlikely that these represent more than a minority of cases.

The relatively small difference between the numbers of homosexual or bisexual men who were negative or positive for antibody to HIV-1 in the proportion that had an "acute sexually transmitted disease" (25% versus 30%) suggests that changes in sexual behaviour as a result of being diagnosed as infected with HIV are short lived or infrequent. This difference between those positive and negative for HIV could, however, be an underestimate, particularly if attenders are concealing their awareness of being infected or if infected people have an increased susceptibility for other sexually transmitted diseases. None the less, others have also found that knowledge of being positive for HIV does not necessarily result in the adoption of safer sexual practice.¹⁰ This suggests a failure to deliver effective health education messages to those at highest risk for acquiring HIV and to those who have been diagnosed as being infected with HIV.

The sexual health target for reduction of infection with gonorrhoea set in the government's Health of the Nation strategy has been achieved.¹¹ None the less, high levels of sexual ill health continue.^{12 13} New targets are needed for HIV prevention, particularly ones focusing on homosexual or bisexual men.^{12 13 14 15} The measures from this unlinked anonymous programme of unrecognised HIV infections seen in genitourinary medicine clinics and acute sexually transmitted diseases seen in men aware of their HIV infection would seem to be suitable targets for clinically relevant national control programmes.

This survey would not have been possible without the support of clinical, clerical, and laboratory staff at clinics and hospitals, whose help is gratefully acknowledged. The development of this survey and others in the HIV prevalence monitoring programme in England and Wales benefited from discussions with colleagues at the Scottish Centre for Infection and Environmental Health and with Dr A V Swan of the PHLS Statistics Unit.

The members of the survey group from 15 clinics and associated laboratories comprised J Anderson, P Carey, C Carne, D Carrington, L Claydon, A Codd, J Coleman, J Connelly, F Davidson, S Drake, G Kinghorn, G Kudesia, A Lawrence, N Lightfoot, R Maw, P R Mortimer, J Munro, S Murphy, K Mutton, J Pennington, A Pozniak, M Prince, K Radcliffe, N Sankar, M S Shafi, D Shanson, S Skidmore, C Sonnex, R Sparks, A Uttley, A Wade, P Watkins, P Wilson, T Wisdom, T Wreghitt, and G Zelin.

P Carey, C Carne, J Coleman, S Drake, A Lawrence, P R Mortimer, J Munro, K Mutton, D Shanson, C Sonnex, R Sparks, A Wade, and T Wreghitt contributed to the data presented in this analysis.

Funding: the Medical Research Council with funds provided by the Department of Health.

Conflict of interest: None.

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