aCentre for Sexual Health and HIV Research, Research Department of Infection and Population Health, University College London, London, UK
bSociology, School of Social Sciences, University of Manchester, Manchester, UK.
Received 19 February, 2008
Revised 16 September, 2008
Accepted 29 September, 2008
Correspondence to Dr Fiona Burns, Centre for Sexual Health & HIV Research, Mortimer Market Centre, Off Capper Street, London WC1E 6JB, UK. Tel: +44 20 8451555000x8185; fax: +44 20 73809778; e-mail: firstname.lastname@example.org
In the UK, the majority of HIV infections acquired through heterosexual transmission are in persons born in Africa. Whilst most of these infections are diagnosed for the first time in the UK, acquisition is thought to have predominantly occurred in Africa .
Previous work suggests that national data may underestimate heterosexual transmission of HIV among African communities in the UK , undermining our potential for averting HIV amongst this population. Our aim in this study was to determine the extent to which acquisition of HIV infection in a UK-African population may have occurred within the UK.
A survey of newly diagnosed HIV-positive Africans, attending 15 HIV treatment centres across London [the study of newly diagnosed HIV infection among Africans in London (SONHIA) study], was conducted between April 2004 and February 2006. Participants were within 12 months of initial HIV diagnosis and aged 18 years or more. Eligible patients not referred for recruitment were classified as not approached.
The survey consisted of a self-completion pen and paper questionnaire, available in English or French, linked to clinical records. Established criteria  to assess possible region of infection was modified to utilize additional data collected in the SONHIA study (Table 1).
The data for all respondents were assessed by the lead author, (Fiona Burns) to rank the likelihood of HIV acquisition in UK or abroad. Every respondent who fulfilled criteria for ‘definitely or probably acquired HIV in Africa’ (categories 1 and 2) or ‘definitely acquired HIV in the UK’ (category 6) was classified as ‘determinate’; all others were classified as ‘indeterminate’. Two independent paid assessors (HIV clinicians) repeated the process on all indeterminate cases. This produced a range of estimates for region of acquisition. Apportionment of region of acquisition was also ascertained utilizing a measure based on CD4 band at the time of diagnosis and time in the UK .
To provide the most conservative estimate of UK acquisition, Categories 7 and 8 (unable to place/inadequate information) were assigned to ‘acquisition abroad’. The study was granted approval from the London Multicentre Research Ethics Committee (MREC/03/2/105).
Of 710 potentially eligible patients, 109 (15.4%) were lost for follow-up and 17 (2.3%) died before they could be approached. Sixty percent (352/584) of the remaining patients were approached. The response rate was 79.5% (280/352) and 263 questionnaires were available for analysis. The median CD4 cell count of those participating was 200 cells/μl, whilst for those not approached it was 260 cells/μl. The median time between HIV diagnosis and questionnaire completion was 3.5 months.
The median age of respondents was 34 years, 60.5% were women, and 50% had a CD4 more than 200 × 106 cells/μl at diagnosis. The median time in the UK prior to HIV diagnosis was 3.9 years; 92.5% respondents identified themselves as heterosexual and 93.5% as black African.
Of 263 respondents, 61 (23.2%) fulfilled criteria for ‘definitely acquired HIV abroad’, 44 (16.7%) ‘probably abroad’, and 16 (6.1%) ‘definitely in the UK’, leaving 142 (54.4%) ‘indeterminate cases’ for further analysis. The proportion of all (determinate and indeterminate cases) HIV infections assessed as UK acquired ranged between 25.1% and 35.4%, whilst 60.8–67.3% were assessed as acquired abroad. All cases acquired abroad indicated Africa as the region of acquisition. Utilizing the CD4/time in the UK criteria, 35.1% of HIV was UK acquired and 64.9% in Africa; however, there was only moderate agreement with the more detailed assessment (κ = 0.427, n = 262, P < 0.001).
No significant differences were found in region of acquisition by sex or age. Individuals aged more than or equal to 30 years on arrival in the UK were less likely to have UK-acquired HIV than those aged less than 30 years [13.0% versus 36.8%, odds ratio (OR) = 0.21, 95% (confidence interval) CI = 0.11–0.42, P < 0.0001]. Persons defining themselves as homosexual or bisexual were more likely to have UK acquired HIV than heterosexuals (47.4% versus 24.4%, OR = 2.86, 95% CI = 1.11–7.39, P = 0.028) as were early compared with late presenters (35.6% versus 14.5%, OR = 2.87, 95% CI = 1.58–5.21, P = 0.001). The association between UK acquisition and early presentation remained when adjusted for sexual orientation [adjusted odds ratio (AOR) = 2.66 (95% CI = 1.45–4.88, P = 0.002)].
Agreement between assessors in allocating region of acquisition for indeterminate cases was 63.0% (95% CI = 54.2–70.6); rising to 79.0% (95% CI = 71.2–85.3) when including those cases in which two assessors had complete agreement but the third felt unable to assess. In 18.9% (95% CI = 12.9–26.4) of cases, the assessors differed on region of acquisition. The overall measure of agreement for the indeterminate cases (with cases unable to be assigned reclassified as likely acquired in Africa) was κ = 0.6 (n = 142, P < 0.001).
Our findings suggest that the proportion of UK-resident Africans acquiring HIV in the UK is substantially higher than previously estimated. Between a quarter to a third of all HIV-positive Africans currently resident in the UK, and nearly half of HIV-positive African men who have sex with men, were likely to have become HIV-infected in the UK.
National surveillance data reports that in individuals of black African ethnicity approximately 8% of newly diagnosed heterosexually acquired HIV infections in the UK were probably UK acquired . National data on country of acquisition are based primarily upon voluntary confidential reports by clinicians, with review and follow-up by national surveillance coordinators . The ability to draw upon richer sources of information in this study may account for the differences between our findings and those of the Health Protection Agency.
The higher rates of UK acquisition are not unexpected: there is high background HIV prevalence among UK Africans, many infections remain undiagnosed , and Africans are more likely to present with advanced disease than non-Africans [1,8,9]; factors facilitating onward disease transmission [10,11]. A situation exacerbated by highly assortative sexual mixing patterns [12,13]. Consequently, UK Africans are at substantially higher risk of HIV exposure than a non-African resident.
Our study has limitations, as reported previously . Acquisition of HIV in UK was negatively associated with late presentation; hence, our findings potentially underestimate infection acquired in UK. No evidence to support a shift in HIV testing patterns within African communities currently exists that could account for our findings.
Our findings have implications for HIV prevention policy and practice. User-friendly assessment tools to assist clinicians in allocating country of HIV acquisition need to be developed. However, there are trade-offs between comprehensiveness and utility, as clinicians are unlikely to use a complex questionnaire; also these tools remain prone to residual interpretive error. New technologies such as HIV-incidence testing and phylogenetic mapping, comprising technologies not yet routinely applied in UK, should support these measures. Without these developments, we are likely to continue overestimating the burden of imported infections.
There are still no culturally specific effective behavioural interventions for migrant Africans in UK , reflecting in part this broadly held assumption that acquisition has occurred abroad. Our findings challenge this assumption, and we hope that it will encourage efforts to develop intervention programmes that support African communities to raise HIV awareness and reduce HIV transmission.
The authors would like to thank all those who participated in the study. C.M. Mercer and A. Copas for statistical support, The African HIV Research Forum steering committee, staff at all participating centres: Archway Sexual Health Clinic: Denise Thorburn, Jo Baruah; Central Middlesex Hospital: Dr Gary Brook; Charing Cross Hospital: Dr John Wright, Dr Anil Rajkumar; Chelsea & Westminster Hospital: Dr Anton Pozniak; Homerton University Hospital: Nicky Hicky; Mortimer Market Centre: Dr Patrick French, Liz Kirkpatrick; Newham University Hospital: Cheryl Tawana; North Middlesex Hospital: Anele Waters, Fiona Young; St. Bartholomew's & the Royal London Hospitals: Are Isaksen; St. George's Hospital: Simone Ghosh, Ade Adebiyi; St. Mary's Hospital: Dr Harpal Lamba, Julie Fowler; University College Hospital: Dr Rob Miller, Peter McKenzie; Victoria Clinic for Sexual Health: Tony Kerley; Watford District General Hospital: Dr Pat Munday; Whittington Hospital: Patricia Whyte. Dr Fiona Burns was supported by a Wellcome Training Fellowship (Grant 066866).
The SONHIA collaboration group included: J. Ainsworth, North Middlesex University Hospital NHS Trust; J. Anderson, L. Muromba, Homerton Hospital NHS Trust; M. Chikohora, North West London Hospitals NHS Trust; A. Fakoya, Newham University Hospital NHS Trust; A. Hughes, St. Mary's NHS Trust; E. Jungmann, N. Panahmand, Camden Primary Care Trust; S. Manney, Barts and The London NHS Trust; N. Nwokolo, R. Stack, A.K. Sullivan, Chelsea and Westminster Healthcare Foundation NHS Trust; S.T. Sadiq, St. George's, University of London; M. Slinn, West Herts Hospitals NHS Trust; I. Fakoya, Research Department of Infection and Population Health, University College London.
Fiona Burns helped design the study, was responsible for study coordination, data collection, statistical analysis, and was the lead writer of this paper. R.G. Arthur, Anne Johnson, James Nazroo, and Kevin Fenton participated in the design of this study and preparation of this manuscript. The SONHIA collaboration group were responsible for managing the study, data collection, and preparation of this manuscript. All authors have seen and approved the final version of this manuscript.
The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.
The guarantor of the study is Dr Fiona Burns.
1. The UK Collaborative Group for HIV and STI Surveillance. A complex picture. HIV and other sexually transmitted infections in the United Kingdom. London: Health Proctection Agency. Centre for Infections; 2006.
2. Sinka K, Mortimer J, Evans B, Morgan D. Impact of the HIV epidemic in sub-Saharan Africa on the pattern of HIV in the UK. AIDS 2003; 17:1683–1690.
3. Paine K, Nicoll A, Evans B, Molesworth A, Mortimer JY, Rogers P. HIV infection in Lambeth, Southwark and Lewisham attributed to sexual intercourse between men and women. London: PHLS Communicable Disease Surveillance Centre; 1997.
4. Satten GA, Longini IMJ. Markov chains with measurement error: estimating the ‘true’ course of a marker of the progression of human immunodeficiency virus disease. Appl Stat 1996; 45:275–309.
5. The UK Collaborative Group for HIV and STI Surveillance. Testing times. HIV and other sexually transmitted infections in the United Kingdom. London: Health Protection Agency, Centre for Infections; 2007.
6. Dougan S, Gilbart VL, Sinka K, Evans BG. HIV infections acquired through heterosexual intercourse in the United Kingdom: findings from national surveillance. BMJ 2005; 330:1303–1304.
7. Sadler KE, McGarrigle CA, Elam G, Ssanyu-Sseruma W, Davidson O, Nichols T, et al. Sexual behaviour and HIV infection in black-Africans in England: results from the Mayisha II survey of sexual attitudes and lifestyles. Sex Transm Infect 2007; 83:523–529.
8. Burns FM, Fakoya AO, Copas AJ, French PD. Africans in London continue to present with advanced HIV disease in the era of highly active antiretroviral therapy. AIDS 2001; 15:2453–2455.
9. Chadborn TR, Delpech VC, Sabin CA, Sinka K, Evans BG. The late diagnosis and consequent short-term mortality of HIV-infected heterosexuals (England and Wales, 2000–2004). AIDS 2006; 20:2371–2379.
10. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 2000; 342:921–929.
11. Marks G, Crepaz N, Janssen RS. Estimating sexual transmission of HIV from persons aware and unaware that they are infected with the virus in the USA. AIDS 2006; 20:1447–1450.
12. Barlow D, Daker-White G, Band B. Assortative sexual mixing in a heterosexual clinic population–a limiting factor in HIV spread? AIDS 1997; 11:1039–1044.
13. Ford K, Sohn W, Lepkowski J. American adolescents: sexual mixing patterns, bridge partners, and concurrency. Sex Transm Dis 2002; 29:13–19.
14. Burns FM, Johnson AM, Nazroo J, Ainsworth J, Anderson J, Fakoya A, et al. Missed opportunities for earlier HIV diagnosis within primary and secondary healthcare settings in the UK. AIDS 2008; 22:115–122.
15. Prost A. A review of research among black African communities affected by HIV in the UK and Europe [Occasional Paper no.15]. Glasgow: University of Glasgow, MRC Social and Public Health Sciences Unit; 2005.
© 2009 Lippincott Williams & Wilkins, Inc.