The demographics of individuals diagnosed with HIV in the United Kingdom (UK) has changed dramatically over the past decade. Whereas the majority of infections in the 1980s and 1990s were among homosexual men, heterosexual individuals formed the majority of HIV-infected patients seen for care in 2003 and 2004 . National HIV surveillance statistics show that heterosexuals accounted for 48% of individuals seen for care in 2004, an increase from 26% in 1998. The large increase in the number of individuals diagnosed with HIV between 1998 and 2004 was mainly caused by increased diagnoses of individuals infected through heterosexual sex, which more than tripled between 1998 and 2004 to over 4000 . Since 1999, the number of new HIV diagnoses among heterosexual individuals has exceeded the number of new diagnoses among homosexual men . In addition, a large proportion of heterosexuals living with HIV in the UK remain undiagnosed  representing a continuing challenge for HIV testing promotion and HIV testing policies.
Surveillance data from the UK show that three-quarters of heterosexual individuals diagnosed since 2000 were probably infected in Africa; most of these were black Africans who had migrated to the UK [1,2]. This has focused attention on the potential effect of migration on the heterosexual epidemic in the UK (although the transmission of HIV in the UK remains far more common between homosexual men). There are also concerns that the stigma of a positive diagnosis may discourage some individuals from testing, which may result in increased transmission rates as well as high levels of morbidity, mortality and associated healthcare costs. There is evidence that few HIV-infected migrants to the UK know that they are infected before their arrival, and that many are also distressed by concerns that are not health related, such as housing and financial problems [3,4].
Many individuals infected with HIV through heterosexual sex are diagnosed late in the UK, either with a low CD4 cell count or an AIDS-defining illness at the time of diagnosis [5–13]. Such individuals may not reap the full benefits of therapy and may experience increased morbidity as a result. Late diagnosis also means that options for avoiding ongoing transmission through clinical and behavioural preventive measures [14,15] are reduced. The costs of caring for individuals diagnosed late are substantial .
Using national surveillance data for heterosexual individuals diagnosed with HIV in England and Wales (E&W) between 2000 and 2004, we describe the proportion of heterosexual individuals diagnosed late and identify factors associated with this. We also estimate the level of short-term mortality that could have been prevented had heterosexual individuals been diagnosed earlier.
Since 1985, laboratories have voluntarily and confidentially reported HIV-positive test results to the Centre for Infections, London . Since January 2000, clinicians diagnosing individuals with HIV for the first time have also voluntarily and confidentially submitted reports (referred to as clinician reports) . Reports include ethnicity (e.g. black African or black Caribbean), how infection was probably acquired (e.g. from a high-risk partner or from a partner infected outside Europe), and where infection was probably acquired. Further enquiries are made when data are incomplete . Country of birth and year of first arrival in the UK are requested from clinicians but not from laboratories. No names are reported, but patient identifiers such as soundex code of surname , date of birth and sex are used to link multiple reports thought to be from the same individual to limit duplication within the surveillance system. Reports are matched to records of death certificates provided by the Office of National Statistics.
The CD4 Surveillance Scheme augments the epidemiological information collected through the reporting of HIV/AIDS cases with data on levels of immunosuppression. Over 60 laboratories in E&W that conduct CD4 cell counts participate in the scheme and report all CD4 cell counts of HIV-infected individuals .
The study population comprised HIV-infected heterosexual individuals (aged 15 years and over) newly diagnosed in E&W between January 2000 and December 2004 (reported by the end of June 2005). Heterosexual individuals presumed infected by injecting drug use or by the receipt of infected blood/organ/tissues were excluded. Patients' locally ascribed identifying number, soundex, forename initial, date of birth, location of HIV testing and sex were used to match case reports to CD4 cell counts recorded on the CD4 database (to December 2004). Records were linked when there was good evidence that reports related to the same person. Records with discordant information were manually checked and unlinked if there was doubt about whether they related to the same person.
The CD4 cell count at diagnosis was defined as the count closest to the date of HIV diagnosis measured within 30 days either side of diagnosis. CD4 cell counts were available from clinician reports as well as from the CD4 Surveillance Scheme. Recent arrivals in the UK were defined as those diagnosed less than 2 years after arrival. Late diagnosis was defined as a CD4 cell count below 200 cells/μl at diagnosis (CD4 cell counts being the strongest marker of the continuous, natural progression of infection). AIDS was defined according to the European case definition [21,22]. Short-term mortality was defined as death from any cause within a year of HIV diagnosis. Preventable short-term mortality was the estimated number of deaths within a year of diagnosis attributed to the late diagnosis of individuals who were not recent arrivals divided by the number of observed deaths within a year of diagnosis. We assumed that heterosexual indivduals coming to the UK did not receive treatment before their diagnosis in the UK and that late diagnosis and short-term mortality were not preventable among recent arrivals.
Women diagnosed antenatally (at an antenatal clinic or antenatal as a reason for test) were considered separately in the analysis, as most pregnant women in the UK have opportunistically been offered HIV tests during antenatal care since 1999 (86% in London in 2002 and 76% in the north west region of England in 2003/2004) [23,24].
Stata 8.0 software (Stata Corporation, College Station, Texas, USA) was used for data analysis. The following statistical methods were used to test for differences between groups: unpaired t-tests and one-way analysis of variance for differences in means; the chi-squared test for trends across ordered categorical variables; and logistic regression for trends across continuous variables. The percentages presented exclude not known or missing information unless otherwise stated.
Between January 2000 and December 2004 (reports received by June 2005), 16 375 heterosexual individuals were diagnosed with HIV in E&W. A total of 852 were excluded from the analysis because of an indication of a previous diagnosis, many of which were outside the UK. A lower proportion of black-African heterosexual individuals were excluded for this reason than white heterosexuals [5.0% (601/12 125) versus 7.7% (135/1765), respectively; P < 0.01]. Of the remaining 15 523 new diagnoses, 10 503 (68%) had a CD4 cell count at HIV diagnosis and these were proportionally representative of all heterosexual individuals newly diagnosed (Table 1).
Epidemiology of newly diagnosed heterosexuals
The majority (64%; 9919/15 523) of newly diagnosed heterosexual individuals were women, of whom 10% (1583/15 523) were diagnosed antenatally (Table 1). The median age at diagnosis of women diagnosed antenatally (28 years) was lower than that of other women (32 years) and men (35 years). Almost three-quarters (74%) of diagnoses were among black-African heterosexual individuals, 11% were white and 4% were black Caribbean (Table 1). Similar proportions of women were diagnosed through antenatal testing across ethnic groups. The median age at diagnosis was similar across ethnic groups, except that white men were older than black-African or black-Caribbean men (Table 2).
Almost all (95%) black-African heterosexual individuals were probably infected in Africa, of whom 44% were probably infected in Zimbabwe, 8% in Uganda, 7% in South Africa and 5% or less in other countries. Of the 7920 with a country of birth reported on a clinician report, 99% were born in Africa. Of the black-African heterosexual individuals born and infected in Africa, 40% had been in the UK less than 2 years before diagnosis, 21% 2–3 years, 7% 4 or 5 years and 8% more than 5 years; 24% had no year of arrival reported.
Late diagnosis among heterosexuals with a CD4 cell count at diagnosis
Forty-two per cent (4425/10 503) of heterosexual individuals were diagnosed late. Of those with clinician reports, 32% of late diagnoses had an AIDS-defining illness within 3 months of diagnosis compared with only 4% of those not diagnosed late. The percentage diagnosed late increased with age (P < 0.01; Table 1), with a similar trend observed for black-African, black-Caribbean and white heterosexual individuals (Fig. 1a). Thirty-eight per cent of all women were diagnosed late (20% of women diagnosed antenatally and 42% of other women) in comparison with 49% of men (Table 1). A higher percentage of black-African heterosexual individuals were diagnosed late (43%) than black-Caribbean (36%) or white (36%) heterosexual individuals (P < 0.01 for both). Differences by sex and ethnicity remained significant after controlling for age (shown separately in Fig. 1 and Table 2). The proportion of heterosexual individuals diagnosed late ranged from 34% of new diagnoses in the north east region, to 47% in the south west (Table 1).
A lower percentage (20%) of black-African heterosexual individuals infected in the UK were diagnosed late compared with heterosexuals infected in Africa (44%, P < 0.01; Table 3). The proportion of black-African heterosexual individuals born and infected in Africa who were diagnosed late varied according to how long they had been in the UK before diagnosis (available from clinician reports): This proportion was 44% among those in the UK less than 2 years (1,038/2384), 41% (514/1268) if 2 or 3 years, 48% (200/413) if 4 or 5 years and 60% (303/502) if more than 5 years. Of those with no year of arrival reported, 45% (590/1326) were diagnosed late.
The percentage of white heterosexual individuals diagnosed late varied considerably by their partners' risk factors for HIV acquisition (Table 3). Of white heterosexual individuals who were probably infected in the UK, those who had a heterosexual partner infected within Europe (including the UK) were over twice as likely to be diagnosed late as those who had partners infected outside Europe (P < 0.01), and the percentage of white heterosexual individuals diagnosed late was similar for those infected by a high-risk partner (a partner who was a gay or bisexual man or an injecting drug user) as for those infected in the UK to heterosexual partners infected outside Europe (P = 0.12).
A higher proportion of black-Caribbean heterosexual individuals infected in Latin America/Caribbean were diagnosed late than those who were infected in the UK (40 versus 28%, P = 0.05; Table 3).
Proportions diagnosed late were similar between black-African and white heterosexual individuals infected in Africa. They were also similar but lower, between black-African and white heterosexual individuals infected in the UK by a partner infected abroad (Table 3).
The short-term mortality of all heterosexual individuals, including those with no CD4 cell counts at diagnosis, was 3.2% (491/15,523; Table 1). The majority (87%, 271/312) of those who died within a year of diagnosis and who had CD4 cell counts at diagnosis were diagnosed late. The short-term mortality was 6.1% (271/4425) among those diagnosed late and 0.7% (41/6078) among others (P < 0.01).
Short-term mortality was lower among black-African compared with white heterosexual individuals [3.1 versus 4.5%; oddsratio (OR) 0.68, P < 0.01) although a higher proportion of black-African heterosexual individuals were diagnosed late (43 versus 36%; Table 1). This was mostly accounted for by the older age of the white men at diagnosis (adjusted for age at diagnosis OR 0.98, P = 0.88). The short-term mortality of black-Caribbean individual was not significantly different than either of the other two ethnic groups.
Estimation of preventable short-term mortality
Short-term mortality was 0.7% among those not diagnosed late. Therefore, we assumed that short-term mortality could be reduced to 0.7% if there were no late diagnoses among heterosexual individuals who were not recent arrivals. We estimated that, during the study period, 199 deaths within a year of diagnosis would have been expected among the three main ethnic groups rather than the 448 observed, a reduction of 56% (Table 4). This would have reduced all mortality for heterosexually acquired infection to approximately 595 between 2000 and 2004 from 880 (data reported to end of June 2005), a reduction of 32%. This assumes no effect on deaths occurring more than a year after diagnosis.
Our study has shown that in E&W, more than two-fifths of all heterosexual individuals were diagnosed late. In particular, a greater proportion of heterosexual individuals were diagnosed late among those who were older, infected abroad, and diagnosed outside of an antenatal setting. Almost two-fifths of heterosexual women were diagnosed late compared with almost half of men. The short-term mortality associated with late diagnosis was high (over nine times higher than that among heterosexual individuals diagnosed earlier). Given that many of those diagnosed late had been in the UK for two or more years before diagnosis, the potential for reducing this short-term mortality by earlier diagnosis is substantial.
Late diagnosis also varied by region of diagnosis, and it may be important to identify whether this is caused by differences between regional populations that are not apparent from these data, such as awareness of the benefits of HIV testing, or whether this is the result of differences in testing policy and practice, such as contact tracing and partner notification.
Our study suggests that groups at high risk of late diagnosis (including individuals born in the UK who may be exposed to HIV in high-prevalence countries) should be targeted for appropriate public health action. Such action might include health promotion, opportunistic screening, and the removal of any barriers to testing, when necessary. Although the proportion of heterosexual individuals attending genitourinary medicine clinics who accepted HIV testing increased to 75% in 2004, 35% of HIV-infected heterosexual individuals left the genitourinary medicine clinic undiagnosed . Perceptions of risk, accessibility of healthcare, fear of deportation and community stigma [25–28] may all reduce the success of current testing policies. In particular, there has been recent concern that the proposed exclusion of ‘irregular’ migrants, including failed asylum seekers and visa overstayers, from eligibility to free HIV treatment from the National Health Service is likely to create a barrier to HIV testing, and may hinder efforts to reduce transmission [29,30]. This problem may be compounded by social and economic insecurity among ‘irregular’ migrants whose life circumstances may consequently place them at greater risk of HIV infection.
Even if some undiagnosed HIV-infected heterosexual individualss are encouraged to seek a diagnosis through targeted HIV testing promotion campaigns, opportunistic screening in a variety of healthcare settings should be considered. Such opportunistic screening could be cost effective even without considering the benefits of prevented transmission . The intensification of antenatal HIV screening has been very successful . New patient checks in primary care may provide the earliest opportunity to diagnose infection among new entrants to the UK [26,27]. However, seeking an HIV test may not be the highest priority for these individuals who may also face financial, housing, immigration, relationship and discrimination problems in the UK . Short-term mortality may also be reduced by increasing awareness of the risks associated with late diagnosis among professionals carrying out health assessments for asylum seekers from Africa and the Caribbean (these professionals are already recommended to consider HIV [32,33]). This is suggested given the markedly increased numbers of applications for asylum from Zimbabweans and Jamaicans between 1999 and 2002  and the large number of HIV-infected heterosexual individuals with insecure immigration or asylum seeker status [35,36].
Recent arrivals may already have low CD4 cell counts before arrival in the UK, and an earlier diagnosis after arrival would therefore result in a lower proportional reduction in short-term mortality than would be possible among homosexual men (56 versus 84% for 2001 ). The absolute number of preventable deaths and the potential reduction in all mortality may, however, be larger than that among homosexual men because estimated short-term mortality accounts for a far higher proportion of deaths among heterosexual individuals (58%, 512/880) than among homosexual men (28%) .
Other studies in London have found that black Africans tend to present later than white individuals [6,9,12,13]. However, our focus on those infected through heterosexual sex allows a comparison of late diagnosis between those of different ethnicities without the bias of the majority of white individuals having been infected with HIV through homosexual sex. We have previously shown that homosexual men tend to be diagnosed earlier than the heterosexual individuals described here . In addition, we found that the difference in the proportion diagnosed late between ethnicities appears to be explained by the world region of infection (Table 3). Increasing age and male sex were consistently associated with late diagnosis in studies from other countries, but these did not consider heterosexual individuals separately and did not show a difference between heterosexuals and homosexual men [38–40]. However, two of the studies also took into account HIV testing history and aspects of sexual behaviour in multivariable analysis, which are likely to be associated with sexual orientation.
The use of AIDS-defining illnesses to define late diagnoses would be likely to introduce bias in this study. This is because only heterosexuals reported by clinicians can be identified as having AIDS, and clinicians are more likely to report if an individual has AIDS at HIV diagnosis (data not shown).
Our study has several limitations. First, CD4 cell counts were only available at diagnosis for two-thirds of heterosexual individuals. However, these individuals were representative of the total heterosexual population suggesting minimal bias. Second, the dataset contains some missing data, in particular, on ethnicity, how infection was acquired and year of arrival. However, we believe that this is unlikely to bias the results substantially. However, women diagnosed antenatally may not all have been identified through reports and may have contributed to the lower proportion of other women diagnosed late compared with men. Third, there were small numbers for all groups (except black-African heterosexual individuals born and infected in Africa) when stratified by other factors, which limited comparisons. Finally, further reports of diagnoses and deaths are expected, particularly among individuals who were diagnosed in 2004. However, we believe that these are unlikely to change our findings substantially.
There are substantial public health benefits associated with earlier diagnosis as well as the clinical benefits to patients. The Department of Health's National Strategy for Sexual Health and HIV for England  in 2001 aimed to reduce the prevalence of undiagnosed infection. Whereas estimates suggest that it may have fallen among heterosexual individuals from 43% in 2001 to 33% in 2004 [1,42], more needs to be done. Those who are diagnosed late with high viral loads may be a major source of new infections . As well as not benefiting from therapy, they form a reservoir for potential transmission and are not able to take measures to reduce the risk of transmission to their partners [14,15,44,45]. Both the National Strategy for Sexual Health and HIV for England  and the Chief Medical Officer's 2004 annual report , prioritized the uptake of HIV testing in a variety of healthcare settings as a core HIV prevention intervention. This has also been a recommendation in other countries since 2003 . This strategy aims to reduce the number of missed diagnoses [39,48,49] and numbers diagnosed as hospital inpatients [3,27,49], thus reducing costs . The development of HIV testing services in general medical practices, including for individuals from high prevalence countries [50–52], may reduce late diagnosis for HIV-infected heterosexual individuals who also may be less likely to access other healthcare services [8,28].
T.C. conceived the idea for the paper with key insight from Dr Noel Gill, Consultant Epidemiologist and Head of the HIV/STI Department, Centre for Infections, Health Protection Agency. T.C. undertook the main writing of the paper, with all authors involved in interpretation of the results and drafting of the paper. K.S. provided the new diagnoses data and T.C. the CD4 surveillance data from E&W. Dr Jane Jones, Consultant Epidemiologist, Travel Health Surveillance Section, Centre for Infections, Health Protection Agency provided valuable contributions to the final draft.
The authors gratefully acknowledge the continuing collaboration of clinicians, microbiologists, virologists, immunologists, public health practitioners, health advisers and other colleagues who contribute to the surveillance of HIV in the UK. They are grateful to the UK Department of Health for core funding of the HIV/AIDS Report Section, HIV/STI Department, Centre for Infections, Health Protection Agency. However, the views expressed here are those of the authors and are independent of funding sources.
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