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Frequency and Implications of HIV Superinfection

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Frequency and Implications of HIV Superinfection Review Frequency and implications of HIV superinfection Andrew D Redd, Thomas C Quinn, Aaron A R Tobian* HIV superinfection occurs when an individual with HIV is infected with a new distinct HIV viral strain. Superinfection Published Online has been reported throughout the world, and studies have recorded incidence rates of 0–7∙7% per year. Use of next- May 31, 2013 generation sequencing has improved detection of superinfection, which can be transmitted by injecting drug use and http://dx.doi.org/10.1016/ S1473-3099(13)70066-5 sexual intercourse. Superinfection might have incidence rates comparable to those of initial HIV infection. Clinicians Division of Intramural should encourage safe sexual and injecting drug use practices for HIV-infected patients because superinfection has Research, National Institute of detrimental eff ects on clinical outcomes and could pose a concern for large-scale antiretroviral treatment plans. The Allergy and Infectious Diseases, occurrence of superinfection has implications for vaccine research, since it seems initial HIV infection is not fully National Institutes of Health, protective against a subsequent infection. Additional collaborative research could benefi t care of patients and inform Bethesda, MD, USA (A D Redd PhD, future vaccine design. Prof T C Quinn MD); Department of Pathology, Introduction Detection of HIV superinfection School of Medicine, Johns HIV superinfection occurs when an individual with The investigators in initial studies that identifi ed indi- Hopkins University, Baltimore, MD (A A R Tobian MD) HIV becomes infected with a new, phylogenetically distinct viduals dually infected with HIV-1 and HIV-2 used Correspondence to: viral HIV strain. This diff ers from HIV dual infection, serological assays that could easily distinguish between Dr Aaron Tobian, Department of which is defi ned as being infected with two or more distinct the two viral species;3 however, this approach cannot Pathology, Johns Hopkins viral strains at one point in time. Dual infection can be distinguish between diff erent HIV-1 subtypes or strains. University, Carnegie 437, caused by superinfection as well as co-infection, which is The initial cases of HIV superinfection were identifi ed in 600 North Wolfe Street, Baltimore, MD 21287, USA initial infection with two or more strains. The possibility of injecting drug users in Thailand by restriction fragment [email protected] superinfection was fi rst discovered after the observation of analysis on amplifi ed viral sequences from longitudinal co-infection with both HIV-1 and HIV-2, which are samples followed by confi rmatory viral sequencing.9 At evolutionarily distinct viral species that share about 42% of the same time, two separate super infection cases were nucleotide homology in their envelope genes.1–3 identifi ed in two men who have sex with men who were Additional evidence for superinfection came from HIV-1 being monitored as part of larger clinical studies after recombinant forms, which are HIV virions that contain they had unexplained spikes in their set-point viral separate genomic sections from distinct HIV-1 subtypes. loads.7,8 Samples from these individuals before and after HIV-1 is diff erentiated by genetic sequence into nine the spike were subsequently analysed by subtype-specifi c subtypes—A, B, C, D, F, G, H, J, and K, which have been asso- PCR amplifi cation7 or direct sequencing8 to confi rm the ciated with diff erent rates of disease progression, viral presence of new viral populations. Other groups sub- load, detection method assay sensitivity, and distinct sequently used these strategies of screening populations geographical regions.4,5 HIV-1 virions are diploid and viral for spikes in viral load10–14 or subsequent restriction strains are able to recombine when two distinct subtypes fragment analysis15 followed by direct sequencing to infect a single cell. If this new recombinant strain is identify HIV superinfection. transmitted it can become a circulating recombinant After these initial studies, three diagnostic strategies form. Roughly 10% of all HIV-1 infections involve re- were used to screen for HIV superinfection in popu- combinant viruses, providing further evidence of lations: heteroduplex mobility assays,16–18 multiregion superinfection.6 hybridisation assays,19 and bulk viral sequence analysis20–25 Although HIV superinfection has been strongly followed by selective cloning of those samples that suspected for many years, whether individuals were suggested emergence of new viral variants. Multiregion infected by two distinct HIV-1 viruses simultaneously hybridisation assays can identify only inter-subtype (co-infection or dual infection), or whether a secondary superinfection. Heteroduplex mobility assays, however, infection occurred after the initial infection (super- can detect samples with greater than 1∙5% genetic infection), has been diffi cult to distinguish. Insuffi cient diff erence but are susceptible to false positives caused by well documented longitudinal samples and absence of insertions or deletions.26 Bulk sequencing can be used to sensitive techniques for HIV superinfection detection examine for changes in the viral population by either prevented its documentation until 2002.7–9 Under- searching for new phylogenetic species at a later standing of both intra-subtype and inter-subtype HIV timepoint or quantifying the amount of degenerate bases superinfection is not only important for appropriate in a given sequence. The sensitivity of this strategy relies management, but could also provide insights into viral on the likelihood of amplifi cation of the new viral popula- evolution and host immune responses to repeat HIV tion and not only the original strain. Not surprisingly, challenges before and after superinfection. Such infor- examination of degenerate bases poorly detected minor mation could have substantial implications for HIV variants at levels of 20% or lower.26 Additionally, all vaccine development, global public health eff orts, and these methods need confi rmation with cloning and care of patients. sequencing.27–29 To avoid problems associated with less www.thelancet.com/infection Published online May 31, 2013 http://dx.doi.org/10.1016/S1473-3099(13)70066-5 1 Review sensitive screening techniques, a range of populations viral diversity than an approach based on amplifi cation of with diff ering risk behaviours were screened for HIV single-viral genomes at 40% of the cost and with 20% less superinfection by either single-viral genome amplifi - labour.29 Consequently, next-generation-sequencing is cation27,28 or cloning30,31 and then compared for evidence becoming the assay of choice for detection of super- of phylogenetically distinct species. The capacity of these infection. Determination of the timing of the two approaches to accurately identify superinfection superinfection events relies on the sampling intervals depends on the amount of sequences generated for each available for the cohorts being examined. However, as sample.28,29 The sensitivity of all sequence-based assays knowledge improves of the rates of evolution and for identifi cation of superinfection also depends on the recombination after superinfection, better esti mation of number of viral genomic regions investigated.28 The two the timing of superinfection by use of phylogenetic and approaches are therefore prohibitively expen sive and too evolutionary modelling analyses is possible. labour-intensive for large-scale studies.29,32 Because of these limitations, we and other researchers Epidemiology have designed and verifi ed next-generation-sequencing HIV superinfection has been documented in observational assays that can detect minor variants at 1% or less of the studies and case reports in the USA8,23,31,36–38 and Canada,39 total viral population in a high-throughput way.29,33,34 We Europe,7,10,13,22,40–42 Australia,11 Asia,9,15 and Africa17,20,21,27,28,35,43 subsequently used this assay to identify HIV super- (fi gure 2); although a small study in Brazil did not fi nd infection both in virally discordant couples and in a large HIV superinfection when detection methods less sensitive population of African HIV seroconverters34,35 (fi gure 1). than next-generation-sequencing were used.16 The Next-generation-sequencing assays allow one to combine widespread observation of superinfection suggests it is a screening and verifi cation, and can be done in a high- substantial problem and has been under-reported. throughput manner, allowing for the accurate and timely Superinfection is transmitted in various ways. Two assessment of large, at-risk populations or at an individual of the initial case reports and several observational patient level.35 Additionally, these assays can capture more studies23,37,40 were in men who have sex with men.7,8 Studies in Thailand and the USA have reported super- 9,15,31 Initial infecting viral population infection in intravenous drug users. Additionally, Viral population after two years many cases of superinfection among female sex workers have been reported.17,20,27,28,43 Although fi rst studied in high-risk populations, superinfection was recently found to occur among a heterosexual population in rural Africa.34,35 HIV superinfection incidence rates of 0% to 7∙7% per year have been recorded in several case reports and population-based studies.23,27,28,43–45 Incidence rates can vary substantially with population, the frequency of Adequate genetic antiretroviral drug use, the length of follow-up, and the distance from original strain to detection methods used. These diff erences in study design rule out natural have led to several studies reporting no superinfection.45–47 genetic drift However, a study using next-generation-sequencing assays in Uganda found superinfection incidence rates comparable to the rate of initial HIV-infection in the same area.35 The study also drew attention to the diffi culty of comparison between HIV superinfection and HIV Presence of a new primary incidence rates in a population because distinct population individuals with HIV are inherently at a higher-risk than consisting of 35 multiple unique the comparison group.
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