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The Characteristics of Pretreatment HIV-1 Drug Resistance in Western Yunnan, China Cambridge.Org/Hyg Epidemiology and Infection The characteristics of pretreatment HIV-1 drug resistance in western Yunnan, China cambridge.org/hyg Min Chen1,* , Qiongmei Zhu2,*, Hui Xing3,*, Huichao Chen1, Xiaomei Jin1, Lijuan Dong1, Jie Dai1, Min Yang1, Cuiyun Yang2, Manhong Jia1 Original Paper and Yanling Ma1 *These authors contributed equally to this work. 1Institute for AIDS/STD Control and Prevention, Yunnan Center for Disease Control and Prevention, Kunming, Yunnan, China; 2Division for AIDS/STD Control and Prevention, Lincang Center for Disease Control and Prevention, Cite this article: Chen M et al (2020). The Lincang, Yunnan, China and 3National Center for AIDS/STD Control and Prevention, Chinese Center for Disease characteristics of pretreatment HIV-1 drug Control and Prevention, Beijing, China resistance in western Yunnan, China. Epidemiology and Infection 148, e102, 1–6. https://doi.org/10.1017/S095026882000093X Abstract Received: 22 December 2019 HIV-1 drug resistance can compromise the effectiveness of antiretroviral therapy (ART). A Revised: 28 April 2020 survey of pretreatment HIV-1 drug resistance (PDR) was conducted in Lincang Prefecture Accepted: 29 April 2020 of Yunnan Province. From 372 people living with HIV/AIDS initiating ART for the first time during 2017–2018, 322 pol sequences were obtained, of which 11 HIV-1 strain types Key words: were detected. CRF08_BC (70.2%, 226/322) was the predominant strain, followed by URF Human immunodeficiency virus; pretreatment drug resistance strains (10.6%, 34/322). Drug resistance mutations (DRMs) were detected among 34.2% (110/322) of the participants. E138A/G/K/R (14.3%, 46/322) and V179E/D/T (13.7%, 47/ Author for correspondence: 322) were the predominant DRMs. Specifically, E138 mutations commonly occurred in Yanling Ma, E-mail: [email protected] CRF08_BC (19.9%, 45/226). Among the DRMs detected, some independently conferred resistance, such as K65R (1.6%, 5/322), Y188C/F/L (0.9%, 3/322), K103N (0.6%, 2/322) and G190A (0.3%, 1/322), which conferred high-level resistance. The prevalence of PDR was 7.5% (95% CI: 4.6–10.3%) and the prevalence of non-nucleotide reverse transcriptase inhibitor (NNRTI) resistance was 5.0% (95% CI: 2.6–7.4%), which is below the threshold (⩾10%) of initiating a public health response. In conclusion, HIV-1 genetic diversity and an overall moderate level of PDR prevalence were found in western Yunnan. PDR surveillance should be continually performed to decide whether a public health response to NNRTI resist- ance should be initiated. Introduction The core target of the 90–90–90 strategy is that at least 73% of people living with HIV (PLWH) have undetectable levels of HIV. The effectiveness of antiretroviral therapy (ART) is critical to achieve this target. Among the associated factors, HIV drug resistance (HIVDR) is increasingly concerning [1]. In response to the threat of HIVDR, it is necessary to monitor and assess HIVDR with the scaling up of ART. The surveillance of HIVDR in populations initiating ART provides evidence to inform the selection of effective first-line ATR regimens. During 2014–2016, the associated surveillance showed that the prevalence of pretreatment HIV-1 drug resistance (PDR) reached 10% or above in some low-income and middle-income countries [2–6]. The increased non-nucleotide reverse transcriptase inhibitor (NNRTI) resist- ance mostly contributed to the increase in PDR [1]. A systematic review and meta-regression analysis found that the yearly increases in the odds of pretreatment NNRTI resistance were 23% in southern Africa, 17% in eastern Africa and in western and central Africa, and 11% © The Author(s), 2020. Published by in Asia and in Latin America and the Caribbean [1]. A recent World Health Organization Cambridge University Press. This is an Open (WHO) drug resistance report showed that the prevalence of PDR to efavirenz (EFV) and Access article, distributed under the terms of the Creative Commons Attribution- nevirapine (NVP) reached levels above 10% in 12 of 18 countries [7]. Based on the WHO rec- NonCommercial-ShareAlike licence (http:// ommendation, when the prevalence of pretreatment NNRTI (EFV and NVP) resistance is creativecommons.org/licenses/by-nc-sa/4.0/), ⩾10% and NNRTI-containing regimen is used as first-line ART, a public health response which permits non-commercial re-use, should be initiated, such as using alternative first-line non-NNRTI-based regimens or introdu- distribution, and reproduction in any medium, cing pretreatment HIVDR testing to guide the selection of first-line ART regimens [8]. To provided the same Creative Commons licence is included and the original work is properly address the significantly increased pretreatment NNRTI resistance in low- and middle-income cited. The written permission of Cambridge countries, the WHO updated the guidelines of ART in 2019, in which non-NNRTI-containing University Press must be obtained for regimens were preferentially recommended [9]. commercial re-use. Following the global tendency, the prevalence of HIVDR in China is also increasing. The trend of HIVDR in ART-naive individuals increased from 3.75% in 2012 to 6.25% in 2017 and the prevalence of resistance to NNRTIs increased from 1.75% in 2012 to 5.0% in 2017 [10]. There was yet a whole nationwide survey of PDR in China. However, limited studies have shown that the prevalence of PDR reached or approached the threshold level in some areas, Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 28 Sep 2021 at 04:58:46, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S095026882000093X 2 M. Chen et al. such as 17.4% in Shanghai and 9.9% in Liangshan Prefecture of Drug resistance analysis Sichuan Province [11, 12]. These results suggest that region- Drug resistance mutations (DRM) and levels were analysed by specific investigations of HIV-1 PDR are necessary. submitting pol sequences to the Stanford HIVdb Program Yunnan is a southwest frontier province in China and shares a (https://hivdb.stanford.edu/hivdb/by-sequences/). The Stanford border with Myanmar, Laos and Vietnam. Yunnan is considered algorithm classifies HIVDR into five levels (susceptible, potential a predominant entry point for the HIV-1 epidemic into China low-level, low-level, intermediate or high-level drug resistance) and is most hit by HIV-1 [13]. By the end of 2016, the number [17]. According to the WHO-recommended judgement criteria of PLWH in Yunnan (91 986) ranked second in China, of for PDR, any HIVDR is defined as low-, intermediate- or high- which 70 577 (76.7%) were receiving ART. Among PLWH receiv- level resistance to the following drugs: two NNRTIs (EFV and ing ART, the rate of virological suppression was 85.2%. With the NVP), seven nucleotide reverse transcriptase inhibitors (NRTIs, scaling up of ART, the effect of PDR on the effectiveness of ART abacavir (ABC), zidovudine (AZT), stavudine (D4T), didanosine should be considered. Lincang Prefecture boarded Myanmar and (DDI), emtricitabine (FTC), lamivudine (3TC), tenofovir was also one of the areas severely affected by HIV-1 in Yunnan. (TDF)) and three proteinase inhibitors (PIs, atazanavir/r (ATV/r), By the end of 2016, the number of PLWH in Lincang darunavir/r (DRV/r) and lopinavir/r (LPV/r)) [18]. Prefecture was 7802. HIV control and prevention in the border area were also impacted by cross-border activities. The overall prevalence of transmitted HIV-1 drug resistance (TDR) remained Statistical analysis low in Yunnan Province [14]. However, a recent study found that Statistical analysis was conducted using the SPSS 19.0 package the occurrence ratio of HIVDR among HIV-1-infected entering (SPSS Inc. Chicago, IL). Categorical variables were compared travellers from Myanmar into Yunnan was up to 12.8% [15]. using chi-square analysis or Fisher’s exact test as appropriate. To thoroughly understand the prevalence of PDR in the border Fisher’s exact test was used when any expected frequencies were area and direct local antiretroviral therapy, surveillance of PDR less than five. All tests were two-tailed and a P-value <0.05 was was carried out in Lincang Prefecture. considered significant. Results Methods Demographic characteristics of the participants Study participants and sample collection A total of 372 PLWH were enrolled before initiating ART in During 2017–2018, a total of 372 PLWH initiating ART for the Lincang Prefecture during 2017–2018. Of them, 50 samples first time were enrolled at ART clinics in eight counties of were not successfully amplified and 322 partial pol gene sequences Lincang Prefecture, Yunnan Province. Blood samples were col- were obtained. The failure of amplification could be due to viral lected before taking antiretroviral drugs and demographic infor- RNA degradation caused by poor storage and transportation con- mation was collected. Written consent was obtained from all ditions of samples. However, the constituent of the 322 success- participants. The study was approved by the institutional review fully genotyped individuals was not significantly different with board of the National Center for AIDS/STD Control and that of the total 373 participants (Supplementary Table S1). Prevention, Chinese Center for Disease Control and Prevention. Among the individuals with pol sequences, 61.8% (199/322) were male and 38.2% (123/322) were female; the median age was 38 years (range: 15–79 years); 57.1% (184/322) of individuals were of Han ethnicity, while 42.9% (138/322) were minorities. Amplification of HIV-1 pol genes Among them, single, married and divorced/widowed accounted for 25.8% (83/322), 54.7% (176/322) and 19.6% (63/322), respect- Viral RNA was extracted with QIAsymphony SP (Qiagen GmbH, ively. For transmission routes, heterosexual contact, intravenous Hilden, Germany). Partial pol sequences (HXB: 2253–3553) were drug use and homosexual contact accounted for 93.8% (302/ amplified using in-house nested reverse transcription polymerase 322), 4.0% (13/322), 0.9% (3/322), respectively and the remaining chain reaction (PCR).
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