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EPIDEMIOLOGY AND SOCIAL: CONCISE COMMUNICATIONS

A new method to assign country of HIV infection among heterosexuals born abroad and diagnosed with HIV

Rice, Brian D.a,b; Elford, Jonathanb; Yin, Zhenga; Delpech, Valerie C.a

Author Information
doi: 10.1097/QAD.0b013e3283578b80
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Abstract

Introduction

In the United Kingdom (UK), as elsewhere in western Europe, a substantial number of HIV diagnoses over the past decade have been among persons infected heterosexually originating from countries with generalized HIV epidemics [1–4]. To better understand the impact of migration on HIV in the UK, a person's likely place of infection is collected by a clinician or health advisor at the time of HIV diagnosis.

In most instances, assignment of likely place of infection is based on the patient's sexual history. Because HIV infection often remains asymptomatic for a long time, and a person's sexual history may span many years and countries, this assessment can prove difficult. Over the past decade, the majority of HIV infections diagnosed in the UK among heterosexual persons born abroad were believed to have been acquired abroad, mainly in sub-Saharan Africa [1,2]. However, a recent study conducted in 15 London HIV treatment centres suggested that national HIV surveillance underestimates heterosexual transmission of HIV within the UK, particularly among persons born in Africa [5].

In this study we apply a new method to assign likely place of HIV infection among heterosexual men and women born abroad using routinely available surveillance data. We compare our estimates from this new method with previously published national estimates based on clinic reports.

Methods

Data sources

The national new HIV diagnoses database, established in 1982, receives voluntary and confidential reports of HIV diagnoses in England, Wales and Northern Ireland [6]. Information on CD4 cell counts at diagnosis (within 91 days of HIV diagnosis) is augmented through linkage to reports of CD4 cell counts received from laboratories [7].

In both systems, held at the Health Protection Agency [8], strict attention to confidentiality is maintained. No names are collected or held, instead a soundex code (a four character coding of the surname) [9], together with sex and date of birth, provide a unique identifier.

Study population

Of 18 911 adults (≥15 years of age at diagnosis), infected heterosexually, born abroad, and diagnosed with HIV in England, Wales and Northern Ireland between 2004 and 2010 (reported to end June 2011), 10 612 were included in the analyses as both CD4 cell count at diagnosis and year of arrival in the UK were available. The characteristics of the study population (n = 10 612) were similar to those of the adults excluded because of missing information (n = 8 299) (data available on request).

Estimated year of infection

To estimate year of HIV infection, we used data from a detailed analysis of CD4-cell decline among seroconverters identified in the national HIV database with at least two CD4 cell counts prior to commencement of antiretroviral therapy or death. The method is described in full elsewhere [10]. In summary, multilevel linear models with random effects were applied to the square-root of 28 613 CD4 cell counts from date of first count to date of last count for 3133 adults diagnosed with HIV between 1996 and 2010. A proxy date of infection was calculated for each adult based on the midpoint between date of last negative HIV test and date of first HIV diagnosis [median 9.5 months; interquartile range (IQR) 5–15 months]. An individuals CD4 cell count at infection was estimated by extrapolating the parameters of the multilevel linear models to the proxy dates of infection [10]. In multivariate analysis, the rate of CD4 cell decline and CD4 cell count at infection differed significantly by ethnicity. The rate of CD4 cell decline also differed significantly by age at diagnosis.

Likely place of HIV infection: new CD4 cell-based method

We estimated year of infection for each of the 10 612 adults in the study population by applying an estimated rate of CD4 cell decline, according to the person's ethnicity and age, between their CD4 cell count at diagnosis and estimated CD4 cell count at infection [10]. An adult was assigned as having acquired HIV while living in the UK (assigned as UK acquired) when estimated year of infection was after their year of arrival in the UK, and as acquired abroad when estimated year of infection was prior to, or at the same time as, their arrival in the UK. Central, lower and upper estimates of UK-acquired HIV were attained by applying three estimates of CD4 cell count at infection. The square-root of CD4 cell decline and median and IQR CD4 cell counts at infection (all per cells/μl) were, respectively, as follows: white 0.73 + 0.02 × age and 569 (IQR 448–711); black-African, black-Caribbean and black-other 0.20 + 0.02 × age and 487 (IQR 377–619); other ethnicity 0.55 + 0.02 × age and 538 (IQR 403–701) [10].

Likely place of HIV infection: clinic-based data

The CD4 cell-based estimates were compared to clinic-based data. When completing the clinic report, clinicians or health advisors indicate whether the patient is presumed to have been infected in the UK and, if not, the country(ies) where infection was likely to have occurred.

Pearson χ2 values and confidence intervals are at the 99% level. STATA 12.0 (Stata Corp., College Station, Texas, USA) was used for analyses.

Results

Likely, place of HIV infection was assigned for 10 612 adults infected heterosexually, born abroad, and diagnosed with HIV in England, Wales and Northern Ireland between 2004 and 2010. Of these, 85% (9065) were of black-African ethnicity.

CD4 cell-based method

Of the 10 612 adults, we estimate that 33% (3452) probably acquired HIV while living in the UK (range: 22%; 2351–44%; 4685). This percentage increased from 25% (466/1858) in 2004 (range: 16–36%) to 44% (543/1245) in 2010 (range: 33–54%) (P < 0.01) (Table 1). The percentage of adults of black-African ethnicity estimated to have acquired HIV while living in the UK was 31% (range 21–43%), increasing from 24% in 2004 to 43% in 2010. In a multivariate analysis, the percentage of adults assigned as UK acquired differed significantly by year of HIV diagnosis, age at diagnosis, and ethnicity (Table 1).

T1-13
Table 1:
Estimates and predictors of UK-acquired HIV infection among adults infected heterosexually, born abroad, and diagnosed with HIV in England, Wales and Northern Ireland 2004–2010.

CD4 cell-based versus clinic-based estimates

Among the 10 494 adults in the study population for whom place of infection was reported, 11% (1200) were assigned as having acquired HIV in the UK by the clinic. Over the study period, this percentage increased from 6.5% (121/1858) in 2004 to 18% (224/1245) in 2010 (P < 0.01).

The central CD4 cell-based estimate of 33% of adults acquiring HIV while living in the UK was three times the clinic-based estimate of 11% (P < 0.01) (Table 1), with the lower CD4 cell-based estimate of 22% double the clinic-based estimate (P < 0.01). For all subgroups presented in Table 1, the CD4 cell-based estimate of UK acquisition was significantly higher than the clinic-based estimate (all P < 0.01).

Concordance between the CD4 cell and clinic-based estimates in assigning place of infection was observed for 72% (7541/10 494) of adults (Table 2). Of the 9294 adults originally classified by the clinics as having acquired HIV abroad, 28% (2575) were subsequently assigned as UK acquired by the central CD4 cell-based method. In multivariate analysis, concordance between the clinic and CD4 cell-based estimates of place of infection differed significantly only by year of HIV diagnosis (P < 0.01) (data available from authors on request).

T2-13
Table 2:
Adults infected heterosexually, born abroad, and diagnosed with HIV in England, Wales and Northern Ireland 2004–2010: concordance between CD4 and clinic-based assignment of place of infection.

Discussion

To better understand HIV transmission dynamics among heterosexual adults born abroad, we applied a new method to assign place of infection based on routinely available data (CD4 cell count at diagnosis and year of arrival in the UK) and estimates of CD4 cell count at infection and CD4 cell decline over time. We estimate that 33% (range 22–44%) of heterosexual adults born abroad and diagnosed with HIV in the UK between 2004 and 2010 acquired their infection while living in the UK.

Although the estimated number of UK-acquired infections remained relatively stable over the study period (466 in 2004; 543 in 2010), proportionally UK-acquired infections increased from 25% in 2004 to 44% in 2010, largely due to a decline in infections acquired abroad. Among black-African adults (who accounted for the majority of the study population), almost one-third (31%) were estimated to have acquired HIV while living in the UK, increasing from 24% in 2004 to 43% in 2010.

The CD4 cell-based estimate of 33% is significantly higher than that of 11% ascertained via clinic reports of place of infection, based on an assessment of a person's sexual history. However, it is similar to the figure among newly diagnosed patients attending 15 HIV treatment centres in London between 2004 and 2006, where place of infection was assigned by the lead investigator having reviewed participant detailed histories and considered CD4 cell count at presentation [5].

Possible reasons for the misclassification of country of infection in clinics include clinic staff underestimating the risk of HIV transmission in the UK, the long incubation period of HIV [11], the underreporting of high-risk sexual behaviours due to social desirability bias or associated stigma [12], and multiple sexual partnerships over time [13,14]. During interviews, HIV treatment clinic staff have indicated that it is often unclear where a person has acquired infection due to complex sexual and migration histories spanning many years, which undoubtedly will contribute to misclassification [Health Protection Agency unpublished report: review of the completion of the national Clinic HIV Report form].

Another possible reason for differences between the CD4 cell-based and clinic-based estimates is that the CD4 cell-based method may overestimate UK-acquired infections. As adults in our study population were more likely to be assigned as ‘UK-acquired’ the longer they have lived in the country some persons may have been assigned as ‘UK-acquired’ when actually HIV was acquired while travelling abroad from the United Kingdom. Two studies among Africans living in England reported that nearly three quarters had had one or more sexual partners in the previous year [13,15].

We excluded approximately four in 10 eligible adults in our analyses due to missing information. As there were no major differences in the demographic or clinical characteristics of adults in the study population as compared to those with missing information, we believe our estimates are applicable to the overall national reported data.

To estimate year of infection, the CD4 cell-based method relies on robust population level estimates of CD4 cell-count at infection and of CD4 cell decline. In this article these estimates are based on the analysis of 28 613 CD4 cell counts among 3133 seroconverters [10]. Our estimates of CD4 cell decline and CD4 cell count at infection fall within the range of published models [16–19].

We have applied a new method to assign likely place of HIV infection that relies on the provision of objective, routinely collected surveillance data to identify communities most at risk of acquiring HIV heterosexually while living in the UK. We suggest that this method could be applied elsewhere, particularly in countries where the number of HIV diagnoses among migrant populations is high. Route of infection, date of diagnosis, CD4 cell counts, and country of birth are already collected routinely in many European countries as well as by the European Centre for Disease Control [20]. To assign likely place of infection using the CD4 cell-based method, we recommend the routine collection of year of arrival for persons born abroad. Our findings highlight the need for improved targeted prevention efforts to reduce the transmission of HIV among black-African communities living in the UK.

Acknowledgements

We would like to thank NHS HIV-related services in the UK and the many individuals who contribute to HIV surveillance. The views expressed in the publication are those of the authors and not necessarily those of the Health Protection Agency.

The surveillance of HIV and AIDS New Diagnoses, and the CD4 Surveillance Scheme are funded by the Department of Health. No article resembling the enclosed article has been or will be published elsewhere.

Conflicts of interest

There are no conflicts of interest.

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Keywords:

England; epidemiology; heterosexual; HIV surveillance; Wales and Northern Ireland

© 2012 Lippincott Williams & Wilkins, Inc.