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Rapid and Complicated HIV Genotype Expansion Among High-Risk Groups

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Rapid and Complicated HIV Genotype Expansion Among High-Risk Groups Zhou et al. BMC Infectious Diseases (2019) 19:185 https://doi.org/10.1186/s12879-019-3788-7 RESEARCH ARTICLE Open Access Rapid and complicated HIV genotype expansion among high-risk groups in Guangdong Province, China Ping-Ping Zhou1, Guolong Yu2, Yi-Qun Kuang1,3, Xu-He Huang1, Yan Li2, Xiaobing Fu2, Peng Lin2, Jin Yan2* and Xiang He1* Abstract Background: Guangdong Province is one of the most developed and populous provinces in southern China, with frequent foreign exchanges and large transient population. The annual number of cases of HIV/AIDS reported in Guangdong has been higher than most of provinces in China for several successive years. HIV infection by heterosexual transmission occurs across the province, with transmission among men who have sex with men occurring mainly in larger urban centers. There is a lack of widespread and representative data on the distribution of HIV subtypes in Guangdong. This study aimed to thoroughly investigate and estimate the prevalence and distribution of HIV-1 subtypes using a city-based sampling strategy to better understand the characteristics of HIV transmission in Guangdong. Methods: Archived plasma samples (n = 1205) from individuals diagnosed as HIV-1 infection in 2013 were selected randomly from all 21 cities in Guangdong Province. Genotypes were determined using env and/or gag sequences using phylogenetic analysis. The distributions of HIV genotypes in different risk groups and different cities were analyzed. Results: A total of 15 genotypes, including six discordant genotypes, were identified. The four main HIV-1 subtypes in Guangdong were CRF01_AE (43.2%), CRF07_BC (26.3%), CRF55_01B (8.5%), and CRF08_BC (8.4%). CRF01_AE was the predominant subtype in all risk populations. The high mobility of people shaped the complexity of the HIV genotypes, while the switch of risk factors affected the distribution and future trend of HIV-1 genotypes in Guangdong. Another epicenter located in the western region in addition to the known epicenter cities in the Pearl River Delta region of Guangdong may exist. Conclusions: Our study provides a comprehensive molecular epidemiologic dataset to understand the diversity and distribution of HIV genotypes in Guangdong, as well as to clarify the unique region- and risk group-specific transmission dynamics. The results provide critical and insightful information for more effective intervention strategies to limit HIV transmission in the future. Keywords: HIV-1, Genotype, Risk factor, Molecular epidemiology, Guangdong, China * Correspondence: [email protected]; [email protected] 2Guangdong Provincial Center for Disease Control and Prevention, 160 Qunxian Road, Panyu District, Guangzhou 511430, China 1Guangdong Provincial Institute of Public Health, Guangdong Provincial Center for Disease Control and Prevention, 160 Qunxian Road, Panyu District, Guangzhou 511430, China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhou et al. BMC Infectious Diseases (2019) 19:185 Page 2 of 10 Background archived by Guangdong Provincial Center for Disease Guangdong Province (hereafter referred to as Guang- Control and Prevention, based on the reported case num- dong) is located on the southern coast of China. It was ber of each city in Guangdong in 2013 (Table 1). The epi- one of the first provinces to establish relationships with demiological data of the patients, including their risk the outside world, starting in 1978. The first imported group, gender, age, ethnicity, marital status, and education, case of human immunodeficiency virus (HIV) was iden- were acquired from China Information System for Disease tified in 1986 in Guangdong. Local HIV cases were re- Control and Prevention. There were no significant differ- ported in injection drug users (IDU) in 1996, with a ences in the risk groups between genotyped samples and subsequent rapid spread among drug users, with the reported cases for each city (all p > 0.05 using the χ2 test, number of cases reaching a peak in 2006 [1–3]. The sex- Additional file 1: Table S1). ual transmission of HIV began to increase in 2005 and by 2009 this route had become the predominant means RNA extraction, amplification, and sequencing of transmission, exceeding transmissions via IDU. It is Viral RNA was extracted from 200 μl of plasma using noteworthy that HIV cases in men who have sex with the MagPure Viral Nucleic Acid KF Kit (Magen, men (MSM) accounted for over 10% of the infected Guangzhou, China) with a KingFisher Flex Purification population by 2013 [3]. The switch of major risk factors System (Thermo Fisher Scientific, Waltham, MA, USA) may have affected the distribution of HIV subtypes in following the manufacturer’s instructions. Both gag Guangdong. (HXB2: 781–1836 nt) and env (HXB2: 7002–7645 nt) Before 2003, there were four prevalent HIV-1 genotypes fragments were amplified using the primers and amplifi- in Guangdong—CRF01_AE, CRF07_BC, CRF08_BC, and cation conditions as previously described [10] with the subtype B—with CRF07_BC and CRF01_AE found mainly PrimeScript One Step RT-PCR Kit and Premix Taq in IDU, CRF01_AE in cases of sexual transmission, and (Takara Bio, Dalian, China). PCR products were sent to subtype B in blood donors and transfusion recipients [1, a commercial company (Zixi Biotech, Beijing, China) for 4]. The examination of clinical samples in 2008 and 2009 sequencing. studies revealed similar genotype distribution in Guang- dong, with the exceptions of the newly detected subtype Sequence analysis and subtype determination C, CRF02_AG, and discordant genotypes [5, 6]. Two stud- The HIV sequences were aligned using the HIVAlign ies in Guangdong focused on the HIV genotypes for differ- tool [6](https://www.hiv.lanl.gov/content/sequence/VIR- ent risk populations in the cities of as Guangzhou [7]and ALIGN/viralign.html) and then merged with HIV-1 Shenzhen [8]. A recent publication described the genotype group M subtyping references from Los Alamos HIV Se- distribution and dynamics in HIV infected MSM in Shen- quence Database using BioEdit [11]. HIV-1 genotypes zhen, and reported the complex HIV genotypes and emer- were determined based on phylogenetic analysis. Neigh gence of new recombinants in this at-risk population [9]. bor-joining phylogenetic trees were reconstructed with However, the foregoing studies either involved limited the Kimura 2-parameter substitution model and evalu- sample sizes or focused on a specific location or risk ated by the bootstrap method with 1000 replicates using population, and thus are not representative of the HIV MEGA 5.2 [12]. The recombinants were screened by the genotype distribution across Guangdong. RIP 3.0 tool [13]. Here we report a comprehensive study using a city- The HIV-1 genotype of each patient was determined based sampling strategy to explore the geographic and based on the genotypes of both gag and env fragments. demographic distribution of HIV genotypes across If only one gene fragment was available, the genotype of Guangdong. We estimated the likely prevalence and dis- that gene was assigned. Samples with different genotypes tribution of HIV-1 genotypes in Guangdong using the identified from gag and env regions were deemed dis- genotypic data of 1205 archived specimens combined cordant genotypes and were assigned gag/env genotype with HIV case report data of various risk groups in designations, such as CRF01/C. prefecture-level cities in Guangdong. Our results provide a comprehensive dataset on the characteristics and di- Estimation of HIV genotypes in different cities and risk versity of HIV and acquired immunodeficiency syn- groups drome (AIDS) in Guangdong. The HIV genotypes in different prefecture cities and risk groups were estimated according to previously described Methods methods [6]. Briefly, the basic analysis unit in our study Study participants and sampling strategy was a specific risk population in a city. The number of A total of 1205 plasma specimens were randomly selected cases for each genotype in the unit was estimated by using the Random Sampling function in Excel software multiplying the proportion of that genotype in the unit from HIV-1 positive samples previously collected and with the total number of HIV cases reported in the unit. Zhou et al. BMC Infectious Diseases (2019) 19:185 Page 3 of 10 Table 1 HIV case reported in Guangdong in 2013 and sample selection City Number of Number of selected Sampling Number of Corrected number of represented Representation in reported cases samples Ratio genotyped samples cases in the study the study Guangzhou 1342 81 6.0% 77 1330 5.8% Shenzhen 1189 80 6.7% 65 1187 5.5% Dongguan 579 76 13.1% 67 575 11.7% Foshan 482 76 15.8% 61 481 12.7% Jiangmen 291 68 23.4% 60 291 20.6% Yangjiang 187 90 48.1% 58 183 31.7% Zhongshan 186 64 34.4% 60 186 32.3% Zhanjiang 174 127 73.0% 55 174 31.6% Huizhou 155 59 38.1% 59 154 38.3% Yunfu 149 59 39.6% 45 147 30.6% Maoming 147 59 40.1% 57 137 41.6% Qingyuan 146 59 40.4% 59 143 41.3% Zhaoqing 108 53 49.1% 50 108 46.3% Shantou 91 50 54.9% 49 88 55.7% Zhuhai 81 48 59.3% 48 81 59.3% Shaoguan 61 31 50.8% 31 60 51.7% Heyuan 48 33 68.8% 33 48 68.8% Meizhou 47 30 63.8% 29 45 64.4% Jieyang 40 20 50.0% 20 38 52.6% Shanwei 24 20 83.3% 18 23 78.3% Chaozhou 21 22 104.8% 20 21 95.2% Total 5548 1205 21.7% 1021 5500 18.6% For a unit in which no specimen was obtained, the 21.7% of the total reported HIV-1 cases in 2013 in number of reported cases was excluded from the cal- Guangdong.
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