Epidemiology and Social: Concise Communication
Transmission of HIV-1 during primary infection: relationship to sexual risk and sexually transmitted infections
Pao, Davida; Fisher, Martina; Hué, Stephaneb,e; Dean, Gilliana; Murphy, Garye; Cane, Patricia Ad,e; Sabin, Caroline Ac; Pillay, Deenanb,e
aDepartment of GU Medicine, Brighton and Sussex University Hospitals, Brighton, UK
bCentre of Virology, Division of Infection and Immunity
cDepartment of Primary Care and Population Sciences, Royal Free and University College Medical School, University College London, London, UK
dHPA Antiviral Susceptibility Reference Unit, University of Birmingham Medical School, and Birmingham HPA, Heartlands Hospital, Birmingham, UK
eCentre for Infections, Health Protection Agency, Colindale, UK
Received 22 June, 2004
Revised 20 September, 2004
Accepted 7 October, 2004
Correspondence to Deenan Pillay, Centre of Virology, Division of Infection and Immunity, Royal Free and University College Medical School, Windeyer Institute, 46 Cleveland Street, London W1P 6DF, UK. E-mail: firstname.lastname@example.org
Objective: To study primary HIV-1 infections (PHI) using molecular and epidemiological approaches in order to assess correlates of transmission in this population.
Methods: Individuals with PHI were recruited prospectively from a discrete cohort of 1235 individuals under follow-up in a well-defined geographical area between 1999 and 2003. PHI was diagnosed by one of the following: negative HIV antibody test within 18 months, evolving antibody response, or application of the serological testing algorithm for recent HIV seroconversion. The pol gene was sequenced to identify genotypic resistance and facilitate molecular epidemiological analysis. Clinical data were collected and linked in an irretrievable fashion when informed consent was obtained.
Results: A total of 103 individuals with PHI diagnosed between 1999 and 2003 were included in the study; 99 (96%) were male and 90 (91%) were men who have sex with men. Viruses from 35 out of 103 (34%) appeared within 15 phylogenetically related clusters. Significant associations with clustering were: young age, high CD4 cell count, number of sexual contacts, and unprotected anal intercourse (UAI) in the 3 months before diagnosis (P < 0.05 for all). High rates of acute sexually transmitted infections (STI) were observed in both groups with a trend towards higher rates in those individuals with viruses within a cluster (42.9 versus 27.9%; P = 0.13).
Conclusion: High rates of partner change, UAI and STI are factors that facilitate onward transmission during PHI. More active identification of individuals during PHI, the management of STI and highly active antiretroviral therapy may all be useful methods to break transmission networks.
Worldwide, 4.2 million adults were estimated to have new HIV-1 infection in 2003 , although it is unclear whether these represent new diagnoses of chronic infection or recently acquired infections; nevertheless it is clear that strategies to interrupt the sexual transmission of HIV-1 are key to reducing the worldwide burden of HIV disease. Within the UK, most new diagnoses now represent imported infections ; however, continual incident infections among men who have sex with men (MSM) are evident . Taken as a single disease stage, the overall efficiency of sexual transmission of HIV is low, but numerous biological and mathematical modelling studies predict much higher infectiousness during primary HIV infection (PHI) compared with chronic HIV infection.
Biologically, the high plasma viral load seen during PHI [4–6], which probably parallels semen viral load [7–10], is strongly correlated with the risk of sexual transmission  and therefore epidemic growth. Other factors that may increase transmission include sexually transmitted infections (STI) and host susceptibility [12,13]. The recent finding of higher concentrations of HIV-1 RNA in rectal mucosa than in blood or semen is also pertinent .
Mathematical models estimate the average probability of male–female transmission of HIV-1 per unprotected coital act to be between 0.0005 and 0.003% during chronic HIV infection , which in itself would not sustain an epidemic. By contrast, when the high viral load of PHI is taken into account, men with average semen viral load, without concurrent STI, would be expected to infect 7–24% of susceptible female partners during the first 2 months of infection (an eight to 10-fold increase from chronic HIV infection) . According to male–male models, between 25 and 47% of new HIV infections may be transmitted during this period of initial HIV infection [16,17], possibly within steady as opposed to casual relationships . In addition, these individuals are infectious before symptoms of PHI , may not even show symptoms of disease  (and therefore be unaware of the risk they pose to partners), and often engage in high-risk sexual practices [21,22] with a higher number of sexual contacts .
There is also increasing evidence that any decrease in the per-contact risk as a result of the increased availability of antiretroviral therapy appears to have been counterbalanced or overwhelmed by increases in risky sexual behaviour [24,25]. This is reflected in the transmission of primary resistant HIV strains, the prevalence of which approaches 20% in the UK and elsewhere [26–29].
In order to understand further the role played by PHI in sexual transmission we carried out phylogenetic characterization of PHI and collected relevant epidemiological data regarding sexual behaviour, clinical features and STI.
Individuals were recruited from a cohort of 1235 HIV-positive patients attending a single genitourinary medicine unit for follow-up from 1999 to 2003. This prospective cohort included over 2100 patients with HIV infection, with 1235 being seen during the study period. Of these, 86% were caucasian, 89% were men, and the predominant route of transmission was sex between men (79%). The department is the sole local provider of HIV and STI care, and national surveillance data confirm that over 90% of individuals with HIV infection resident in the area attend this institution.
Individuals with PHI were identified by one or more of the following: previous negative HIV antibody test within 18 months, evolving Western blot or HIV antibody response, or application of the serological testing algorithm for recent HIV seroconversion (STARHS) assay. STARHS is a dual testing strategy in which specimens that are confirmed anti-HIV positive after detection by a sensitive screening assay are tested on an assay that has been altered to make it less sensitive. Specimens that are unreactive on this less sensitive assay are deemed to be recent infections, whereas specimens that are reactive in both assays are deemed to come from infections that are long standing . At the time of HIV diagnosis the majority of individuals underwent a full STI screen.
Clinical data collection
In those from whom written informed consent was obtained, information regarding clinical status was collected from clinic case notes: the date of diagnosis, CD4 cell count, CD4 cell percentage, HIV viral load, the presence and nature of STI in the 3 months before the diagnosis of PHI (gonorrhoea, chlamydia, non-specific urethritis, early syphilis, herpes simplex), and the absence or presence of PHI symptoms. Information relating to the individual's HIV acquisition risk group, sexual behaviour (including estimated number and nature of sexual contacts in the 3 months before diagnosis of PHI) was also recorded. These data are routinely collected for all new HIV-1 diagnoses within this clinic.
Serological testing algorithm for recent HIV seroconversion and analysis
STARHS testing was performed using the bioMérieux Vironostika HIV-1 assay (bioMérieux UK Ltd., Basingstoke, UK) as previously described . A standardized optical density for each specimen was determined. For this study a standardized optical density of less than 1.0 was used to identify recent infections, and this cut-off equates to an estimated seroconversion within the previous 4–6 months.
The HIV pol gene was sequenced from plasma obtained at the time of HIV diagnosis. These sequences were used for phylogenetic analysis, a method previously shown by this group to have utility in reconstructing transmission events . Full-length sequences from the protease gene (295 nt) and the first 230 codons of reverse transcriptase were aligned using the program Clustal X (available from http://www-igbmc.u-strasbg.fr/BioInfo/ClustalX/Top.html) and then adjusted manually with the software BioEdit (available from http://www.mbio.ncsu.edu/BioEdit/bioedit.html). Sequences that could not be unambiguously aligned or were of insufficient length were excluded from the study. Phylogenetic relationships between the pol sequences were reconstructed using the neighbour-joining followed by maximum likelihood methods. An initial neighbour-joining tree was built under the Hasegawa–Kishino–Yang (HKY85) model of evolution with a ratio of transversion to transitions of 2:1 using the tree-building software Paup* (available from http://paup.csit.fsu.edu/about.html).
The best fitting model of nucleotide substitution was estimated on the basis of the neighbour-joining tree topology using a maximum likelihood ratio test with Modeltest version 3.0 (available from http://bioag.byu.edu/zoology/crandall_lab/modeltest.htm). The derived parameters of the selected model were then used to perform a heuristic search for a maximum likelihood tree with Paup*. The construction of the tree was done according to the general time reversible (GTR) model of evolution, with a proportion of invariable sites and gamma distribution. An HIV-1 subtype K sequence (Genbank accession number AJ249239) retrieved from the Los Alamos HIV database (http://hiv-web.lanl.gov/) was used as an outgroup and six pairs of follow-up sequences from the same individuals were used as controls. The robustness of the neighbour-joining trees was evaluated by bootstrap analysis, with 1000 rounds of replication.
Statistical comparisons of those in a cluster with those not in a cluster were performed using Chi-squared tests, Fisher's exact tests or Mann–Whitney U tests, as appropriate. Multivariable logistic regression was used to identify factors independently associated with belonging to a cluster. All statistical analyses were performed using SAS version 8 (available from http://v8doc.sas.com/sashtml/). The study was approved by the Brighton and Hove Local Research Ethics Committee and the Health Protection Agency Ethics Committee. Confidentiality and anonymity were protected by irreversibly unlinking clinic and laboratory from the study ID number using a firewall system managed by the local public health laboratory. Written, informed consent was obtained from all participants.
Study population description
A total of 103 individuals with PHI diagnosed between 1999 and 2003 were included in the epidemiological and phylogenetic analysis. Of these, 73 (71%) had a STARHS antibody test suggestive of infection within the previous 4–6 months. Almost all (99, 96.1%) were men and 90 (90.9%) were MSM. All the men and two out of four women were Caucasian with a median age of 36 years (range 21–67). The median age was 36 years (range 21–67). Six individuals (6.1%) reported a history of injecting drug use (two MSM, two heterosexual men and two heterosexual women). The median CD4 cell count (available in 101/103) was 526 copies/ml (range 195–1477) and the median CD4 cell percentage (available in 81/103) was 28 (7–42). The median HIV viral plasma load was log 4.95 copies/ml (2.03–6.00). Thirteen MSM (12.6% of total patients) were infected with viruses that contained primary antiretroviral resistance-associated mutations. STI were diagnosed concurrently with PHI in 34 of the 89 individuals (38.2%) for whom information was available. Among the 90 MSM, 61 (68%) reported unprotected anal intercourse (UAI) in the 3 months before PHI diagnosis; no information was available regarding sexual practices in the period preceding this.
Viruses from 35 out of 103 individuals (34%) appeared within 15 transmission clusters, comprising one cluster of five individuals, two of three and 12 of two (full results shown in Table 1 and Fig. 1). All were men and 32 (97%) were MSM. For individuals within 11 out of 15 clusters, the diagnosis of PHI was made within 12 months of each other, giving supporting evidence that transmission occurred during the PHI period. Those in the cluster group had a higher CD4 cell count (P = 0.005), higher CD4 cell percentage (P = 0.003), were younger (P = 0.05), reported a higher number of different sexual contacts in the previous 3 months (P = 0.006), and were more likely to have engaged in UAI in the 3 months before the PHI diagnosis (P = 0.05) in comparison to those individuals not within a cluster. High rates of STI at the time of PHI were observed in both groups, with a trend towards higher rates in those individuals with viruses in a cluster (42.9 versus 27.9%, P = 0.13). Multivariable logistic regression analyses identified the CD4 cell percentage [odds ratio (OR) 1.14, 95% confidence interval (CI) 1.04–1.23, P = 0.003] and having more than five sexual partners (OR 3.38, 95% CI 1.13–10.10, P = 0.03) as the only independent predictors of belonging to a cluster. Six individuals (17%) had antiretroviral-associated resistance mutations, of whom two (both T215D in reverse transcriptase) belonged to a linkage pair.
In conclusion, the high rates of clustering observed within our study support the assertion that PHI may be associated with an increased risk of onward transmission. The associations we found with younger age, high rates of UAI, and sexual partner change identify this as a high-risk group for HIV transmission. There was a trend towards higher rates of STI in the cluster group on a background of extremely high STI rates in the study population, supporting the argument for increased STI surveillance, particularly of high-risk groups.
The highly significant correlation with CD4 cell counts may represent the early disease stage, or rapid contact tracing and testing of sexual partners of individuals diagnosed with PHI. The plasma viral load at diagnosis was not predictive of clustering, and it is possible that the seminal viral load in men is a more consistent correlate of infectiousness, particularly in the context of genital tract inflammation, with plasma/genital tract discordance playing an important role [7–10]. The presence of the same antiretroviral resistance mutation in one cluster pair, neither of whom had received antiretroviral therapy, illustrates the potential for the secondary spread of such resistant strains, as we have previously documented [33,34]. Our results do not exclude the possibility of a common source for each cluster, rather than transmission within clusters. However, a phylogenetic tree comprising viruses from these 103 primary infections, together with more than 2000 pol sequences from prevalent infections throughout the UK only identified one further potential linkage, and that involved a primary infection case not within an existing cluster (data not shown).
Only 31 of the non-cluster group (64.6%) reported UAI, but it should be noted that this is only in the time window 3 months before diagnosis with PHI. Interestingly, routinely collected data on recent sexual contacts only confirmed three of the linkage pairs that were revealed in the phylogenetic analysis, emphasizing the high rates of anonymous sexual partners and the difficulty in obtaining a reliable sexual history.
Our results provide further evidence that the active management of primary infection will reduce HIV transmission. HIV prevention programmes have been heavily focused on protecting susceptible individuals, but accumulating biological and modelling data suggest that reducing the infectiousness of HIV-positive individuals may also be an effective strategy. A large proportion of PHI remains undiagnosed in the community [35,36], and these findings support the view that as a disease stage PHI represents a major public health threat. Efforts should be re-focused on improving rates of diagnosis of individuals during PHI, timely contact tracing, risk reduction, the management of STI, and possibly early treatment with antiretroviral agents in an effort to break transmission networks during this unique and possibly crucial stage of HIV infection . Furthermore, consideration should be given in information and awareness campaigns to highlight the possible symptoms of PHI in groups with high rates of onward transmission, to encourage such individuals to present to appropriate healthcare providers to enable the timely diagnosis and management of early infection.
M.F. and D. Pillay devised the study. D. Pao, M.F. and G.D. recruited patients for the study. D. Pao, M.F., S.H., C.S. and D. Pillay wrote the manuscript. P.A.C. undertook sequencing and curated the sequences. S.H. undertook the phylogenetic analyses. G.M. undertook the STARHS analysis. C.S. undertook statistical analyses.
The authors would like to thank the Health Protection Agency for funding, and the patients for agreeing to enter this study.
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