Molecular network-based intervention brings us closer to ending the HIV pandemic
Xiaoxu Han1,2,3, Bin Zhao1,2,3, Minghui An1,2,3, Ping Zhong1,4, Hong Shang1,2,3()
1. Key Laboratory of AIDS Immunology of National Health Commission, Department of Laboratory Medicine, The First Affiliated Hospital, China Medical University, Shenyang 110001, China 2. Key Laboratory of AIDS Immunology, Chinese Academy of Medical Sciences, Shenyang 110001, China 3. Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Hangzhou 310003, China 4. Department of AIDS and STD, Shanghai Municipal Center for Disease Control and Prevention, Shanghai 200336, China
Precise identification of HIV transmission among populations is a key step in public health responses. However, the HIV transmission network is usually difficult to determine. HIV molecular networks can be determined by phylogenetic approach, genetic distance-based approach, and a combination of both approaches. These approaches are increasingly used to identify transmission networks among populations, reconstruct the history of HIV spread, monitor the dynamics of HIV transmission, guide targeted intervention on key subpopulations, and assess the effects of interventions. Simulation and retrospective studies have demonstrated that these molecular network-based interventions are more cost-effective than random or traditional interventions. However, we still need to address several challenges to improve the practice of molecular network-guided targeting interventions to finally end the HIV epidemic. The data remain limited or difficult to obtain, and more automatic real-time tools are required. In addition, molecular and social networks must be combined, and technical parameters and ethnic issues warrant further studies.
. [J]. Frontiers of Medicine, 2020, 14(2): 136-148.
Xiaoxu Han, Bin Zhao, Minghui An, Ping Zhong, Hong Shang. Molecular network-based intervention brings us closer to ending the HIV pandemic. Front. Med., 2020, 14(2): 136-148.
R Machuca, LB Jørgensen, P Theilade, C Nielsen. Molecular investigation of transmission of human immunodeficiency virus type 1 in a criminal case. Clin Diagn Lab Immunol 2001; 8(5): 884–890
pmid: 11527797
4
T Leitner, D Escanilla, C Franzén, M Uhlén, J Albert. Accurate reconstruction of a known HIV-1 transmission history by phylogenetic tree analysis. Proc Natl Acad Sci USA 1996; 93(20): 10864–10869 https://doi.org/10.1073/pnas.93.20.10864
pmid: 8855273
5
SA Trask, CA Derdeyn, U Fideli, Y Chen, S Meleth, F Kasolo, R Musonda, E Hunter, F Gao, S Allen, BH Hahn. Molecular epidemiology of human immunodeficiency virus type 1 transmission in a heterosexual cohort of discordant couples in Zambia. J Virol 2002; 76(1): 397–405 https://doi.org/10.1128/JVI.76.1.397-405.2002
pmid: 11739704
6
DM Smith, SJ May, S Tweeten, L Drumright, ME Pacold, SL Kosakovsky Pond, RL Pesano, YS Lie, DD Richman, SD Frost, CH Woelk, SJ Little. A public health model for the molecular surveillance of HIV transmission in San Diego, California. AIDS 2009; 23(2): 225–232 https://doi.org/10.1097/QAD.0b013e32831d2a81
pmid: 19098493
7
JL Aldous, SK Pond, A Poon, S Jain, H Qin, JS Kahn, M Kitahata, B Rodriguez, AM Dennis, SL Boswell, R Haubrich, DM Smith. Characterizing HIV transmission networks across the United States. Clin Infect Dis 2012; 55(8): 1135–1143 https://doi.org/10.1093/cid/cis612
pmid: 22784872
8
SJ Little, SL Kosakovsky Pond, CM Anderson, JA Young, JO Wertheim, SR Mehta, S May, DM Smith. Using HIV networks to inform real time prevention interventions. PLoS One 2014; 9(6): e98443 https://doi.org/10.1371/journal.pone.0098443
pmid: 24901437
9
EM Volz, S Le Vu, O Ratmann, A Tostevin, D Dunn, C Orkin, S O’Shea, V Delpech, A Brown, N Gill, C Fraser; UK HIV Drug Resistance Database. Molecular epidemiology of HIV-1 subtype B reveals heterogeneous transmission risk: implications for intervention and control. J Infect Dis 2018; 217(10): 1522–1529 https://doi.org/10.1093/infdis/jiy044
pmid: 29506269
National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention; Division of HIV/AIDS. Prevention Detecting and Responding to HIV Transmission Clusters: A Guide for Health Department. 2018.
12
AS Fauci, RR Redfield, G Sigounas, MD Weahkee, BP Giroir. Ending the HIV epidemic: a plan for the United States. JAMA 2019; 321(9): 844–845 https://doi.org/10.1001/jama.2019.1343
pmid: 30730529
13
S Hué, JP Clewley, PA Cane, D Pillay. HIV-1 pol gene variation is sufficient for reconstruction of transmissions in the era of antiretroviral therapy. AIDS 2004; 18(5): 719–728 https://doi.org/10.1097/00002030-200403260-00002
pmid: 15075506
14
G Yebra, EB Hodcroft, ML Ragonnet-Cronin, D Pillay, AJ Brown; PANGEA_HIV Consortium; ICONIC Project. Using nearly full-genome HIV sequence data improves phylogeny reconstruction in a simulated epidemic. Sci Rep 2016; 6(1): 39489 https://doi.org/10.1038/srep39489
pmid: 28008945
15
S Yerly, S Vora, P Rizzardi, JP Chave, PL Vernazza, M Flepp, A Telenti, M Battegay, AL Veuthey, JP Bru, M Rickenbach, B Hirschel, L Perrin; Swiss HIV Cohort Study. Acute HIV infection: impact on the spread of HIV and transmission of drug resistance. AIDS 2001; 15(17): 2287–2292 https://doi.org/10.1097/00002030-200111230-00010
pmid: 11698702
16
N Saitou, M Nei. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4(4): 406–425
pmid: 3447015
17
G Baele, P Lemey, T Bedford, A Rambaut, MA Suchard, AV Alekseyenko. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 2012; 29(9): 2157–2167 https://doi.org/10.1093/molbev/mss084
pmid: 22403239
18
G Baele, WL Li, AJ Drummond, MA Suchard, P Lemey. Accurate model selection of relaxed molecular clocks in bayesian phylogenetics. Mol Biol Evol 2013; 30(2): 239–243 https://doi.org/10.1093/molbev/mss243
pmid: 23090976
19
R Bouckaert, TG Vaughan, J Barido-Sottani, S Duchêne, M Fourment, A Gavryushkina, J Heled, G Jones, D Kühnert, N De Maio, M Matschiner, FK Mendes, NF Müller, HA Ogilvie, L du Plessis, A Popinga, A Rambaut, D Rasmussen, I Siveroni, MA Suchard, CH Wu, D Xie, C Zhang, T Stadler, AJ Drummond. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2019; 15(4): e1006650 https://doi.org/10.1371/journal.pcbi.1006650
pmid: 30958812
20
MA Suchard, P Lemey, G Baele, DL Ayres, AJ Drummond, A Rambaut. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 2018; 4(1): vey016 https://doi.org/10.1093/ve/vey016
pmid: 29942656
21
AM Dennis, S Hué, R Billock, S Levintow, J Sebastian, WC Miller, JJ Eron. Human immunodeficiency virus type 1 phylodynamics to detect and characterize active transmission clusters in North Carolina. J Infect Dis 2019 Apr 27. [Epub ahead of print] doi: 10.1093/infdis/jiz176 https://doi.org/10.1093/infdis/jiz176
pmid: 31028702
22
E Wilkinson, DM Junqueira, R Lessells, S Engelbrecht, G van Zyl, T de Oliveira, M Salemi. The effect of interventions on the transmission and spread of HIV in South Africa: a phylodynamic analysis. Sci Rep 2019; 9(1): 2640 https://doi.org/10.1038/s41598-018-37749-3
pmid: 30804361
23
AF Poon. Impacts and shortcomings of genetic clustering methods for infectious disease outbreaks. Virus Evol 2016; 2(2): vew031 https://doi.org/10.1093/ve/vew031
pmid: 28058111
24
JL Aldous, SK Pond, A Poon, S Jain, H Qin, JS Kahn, M Kitahata, B Rodriguez, AM Dennis, SL Boswell, R Haubrich, DM Smith. Characterizing HIV transmission networks across the United States. Clin Infect Dis 2012; 55(8): 1135–1143 https://doi.org/10.1093/cid/cis612
pmid: 22784872
25
BS Chin, A Chaillon, SR Mehta, JO Wertheim, G Kim, HS Shin, DM Smith. Molecular epidemiology identifies HIV transmission networks associated with younger age and heterosexual exposure among Korean individuals. J Med Virol 2016; 88(10): 1832–1835 https://doi.org/10.1002/jmv.24523
pmid: 26990771
26
X Wang, Y Wu, L Mao, W Xia, W Zhang, L Dai, SR Mehta, JO Wertheim, X Dong, T Zhang, H Wu, DM Smith. Targeting HIV prevention based on molecular epidemiology among deeply sampled subnetworks of men who have sex with men. Clin Infect Dis 2015; 61(9): 1462–1468 https://doi.org/10.1093/cid/civ526
pmid: 26129754
27
R Rose, SL Lamers, JJ Dollar, MK Grabowski, EB Hodcroft, M Ragonnet-Cronin, JO Wertheim, AD Redd, D German, O Laeyendecker. Identifying transmission clusters with cluster picker and HIV-TRACE. AIDS Res Hum Retroviruses 2017; 33(3): 211–218 https://doi.org/10.1089/aid.2016.0205
pmid: 27824249
28
MC Prosperi, M Ciccozzi, I Fanti, F Saladini, M Pecorari, V Borghi, S Di Giambenedetto, B Bruzzone, A Capetti, A Vivarelli, S Rusconi, MC Re, MR Gismondo, L Sighinolfi, RR Gray, M Salemi, M Zazzi, A De Luca; ARCA collaborative group. A novel methodology for large-scale phylogeny partition. Nat Commun 2011; 2(1): 321 https://doi.org/10.1038/ncomms1325
pmid: 21610724
29
M Ragonnet-Cronin, E Hodcroft, S Hué, E Fearnhill, V Delpech, AJ Brown, S Lycett; UK HIV Drug Resistance Database. Automated analysis of phylogenetic clusters. BMC Bioinformatics 2013; 14(1): 317 https://doi.org/10.1186/1471-2105-14-317
pmid: 24191891
D Paraskevis, E Magiorkinis, G Magiorkinis, VG Kiosses, P Lemey, AM Vandamme, A Rambaut, A Hatzakis. Phylogenetic reconstruction of a known HIV-1 CRF04_cpx transmission network using maximum likelihood and Bayesian methods. J Mol Evol 2004; 59(5): 709–717 https://doi.org/10.1007/s00239-004-2651-6
pmid: 15693627
32
J Esbjörnsson, M Mild, A Audelin, J Fonager, H Skar, L Bruun Jørgensen, K Liitsola, P Björkman, G Bratt, M Gisslén, A Sönnerborg, C Nielsen; SPREAD/ESAR Programme, P Medstrand, J Albert. HIV-1 transmission between MSM and heterosexuals, and increasing proportions of circulating recombinant forms in the Nordic Countries. Virus Evol 2016; 2(1): vew010 https://doi.org/10.1093/ve/vew010
pmid: 27774303
33
CA Bruhn, AM Audelin, M Helleberg, K Bjorn-Mortensen, N Obel, J Gerstoft, C Nielsen, M Melbye, P Medstrand, MT Gilbert, J Esbj�rnsson. The origin and emergence of an HIV-1 epidemic: from introduction to endemicity. AIDS 2014; 28(7): 1031–1040 https://doi.org/10.1097/QAD.0000000000000198
pmid: 24451158
34
L Jovanović, M Šiljić, V Ćirković, D Salemović, I Pešić-Pavlović, M Todorović, J Ranin, D Jevtović, M Stanojević. Exploring evolutionary and transmission dynamics of HIV epidemic in Serbia: bridging socio-demographic with phylogenetic approach. Front Microbiol 2019; 10: 287 https://doi.org/10.3389/fmicb.2019.00287
pmid: 30858834
35
N Bbosa, D Ssemwanga, RN Nsubuga, JF Salazar-Gonzalez, MG Salazar, M Nanyonjo, M Kuteesa, J Seeley, N Kiwanuka, BS Bagaya, G Yebra, A Leigh-Brown, P Kaleebu. Phylogeography of HIV-1 suggests that Ugandan fishing communities are a sink for, not a source of, virus from general populations. Sci Rep 2019; 9(1): 1051 https://doi.org/10.1038/s41598-018-37458-x
pmid: 30705307
36
M Ragonnet-Cronin, C Jackson, A Bradley-Stewart, C Aitken, A McAuley, N Palmateer, R Gunson, D Goldberg, C Milosevic, AJ Leigh Brown. Recent and rapid transmission of HIV among people who inject drugs in Scotland revealed through phylogenetic analysis. J Infect Dis 2018; 217(12): 1875–1882 https://doi.org/10.1093/infdis/jiy130
pmid: 29546333
37
D Paraskevis, A Beloukas, K Stasinos, N Pantazis, C de Mendoza, N Bannert, L Meyer, R Zangerle, J Gill, M Prins, A d’Arminio Montforte, AB Kran, K Porter, G Touloumi; CASCADE collaboration of EuroCoord. HIV-1 molecular transmission clusters in nine European countries and Canada: association with demographic and clinical factors. BMC Med 2019; 17(1): 4 https://doi.org/10.1186/s12916-018-1241-1
pmid: 30616632
38
T de Oliveira, AB Kharsany, T Gräf, C Cawood, D Khanyile, A Grobler, A Puren, S Madurai, C Baxter, QA Karim, SS Karim. Transmission networks and risk of HIV infection in KwaZulu-Natal, South Africa: a community-wide phylogenetic study. Lancet HIV 2017; 4(1): e41–e50 https://doi.org/10.1016/S2352-3018(16)30186-2
pmid: 27914874
39
NR Faria, A Rambaut, MA Suchard, G Baele, T Bedford, MJ Ward, AJ Tatem, JD Sousa, N Arinaminpathy, J Pépin, D Posada, M Peeters, OG Pybus, P Lemey. The early spread and epidemic ignition of HIV-1 in human populations. Science 2014; 346(6205): 56–61 https://doi.org/10.1126/science.1256739
pmid: 25278604
40
A Waruru, TNO Achia, JL Tobias, J Ngʼangʼa, M Mwangi, J Wamicwe, E Zielinski-Gutierrez, T Oluoch, E Muthama, T Tylleskär. Finding hidden HIV clusters to support geographic-oriented HIV interventions in Kenya. J Acquir Immune Defic Syndr 2018; 78(2): 144–154 https://doi.org/10.1097/QAI.0000000000001652
pmid: 29474269
41
Z Butt, S Grady, M Wilkins, E Hamilton, D Todem, J Gardiner, M Saeed. Spatial epidemiology of HIV-hepatitis co-infection in the State of Michigan: a cohort study. Infect Dis (Lond) 2015; 47(12): 852–861 https://doi.org/10.3109/23744235.2015.1066931
pmid: 26179757
42
M Stecher, M Hoenigl, AM Eis-H�binger, C Lehmann, G Fätkenheuer, JC Wasmuth, E Knops, JJ Vehreschild, S Mehta, A Chaillon. Hotspots of transmission driving the local human immunodeficiency virus epidemic in the Cologne-Bonn Region, Germany. Clin Infect Dis 2019; 68(9): 1539–1546 https://doi.org/10.1093/cid/ciy744
pmid: 30169606
43
A Chaillon, A Essat, P Frange, DM Smith, C Delaugerre, F Barin, J Ghosn, G Pialoux, O Robineau, C Rouzioux, C Goujard, L Meyer, ML Chaix; on behalf the ANRS PRIMO Cohort Study. Spatiotemporal dynamics of HIV-1 transmission in France (1999–2014) and impact of targeted prevention strategies. Retrovirology 2017; 14(1): 15 https://doi.org/10.1186/s12977-017-0339-4
pmid: 28222757
44
JO Wertheim, AJ Leigh Brown, NL Hepler, SR Mehta, DD Richman, DM Smith, SL Kosakovsky Pond. The global transmission network of HIV-1. J Infect Dis 2014; 209(2): 304–313 https://doi.org/10.1093/infdis/jit524
pmid: 24151309
45
M Fisher, D Pao, AE Brown, D Sudarshi, ON Gill, P Cane, AJ Buckton, JV Parry, AM Johnson, C Sabin, D Pillay. Determinants of HIV-1 transmission in men who have sex with men: a combined clinical, epidemiological and phylogenetic approach. AIDS 2010; 24(11): 1739–1747 https://doi.org/10.1097/QAD.0b013e32833ac9e6
pmid: 20588173
46
DL Yirrell, H Pickering, G Palmarini, L Hamilton, A Rutemberwa, B Biryahwaho, J Whitworth, AJ Brown. Molecular epidemiological analysis of HIV in sexual networks in Uganda. AIDS 1998; 12(3): 285–290 https://doi.org/10.1097/00002030-199803000-00006
pmid: 9517991
47
KT Ng, KY Ng, JH Chen, OT Ng, A Kamarulzaman, KK Tee. HIV-1 transmission networks among men who have sex with men in Asia. Clin Infect Dis 2014; 59(6): 910–911 https://doi.org/10.1093/cid/ciu480
pmid: 24944233
48
SR Mehta, JO Wertheim, KC Brouwer, KD Wagner, A Chaillon, S Strathdee, TL Patterson, MG Rangel, M Vargas, B Murrell, R Garfein, SJ Little, DM Smith. HIV transmission networks in the San Diego-Tijuana Border Region. EBioMedicine 2015; 2(10): 1456–1463 https://doi.org/10.1016/j.ebiom.2015.07.024
pmid: 26629540
49
AM Oster, JO Wertheim, AL Hernandez, MC Ocfemia, N Saduvala, HI Hall. Using molecular HIV surveillance data to understand transmission between subpopulations in the United States. J Acquir Immune Defic Syndr 2015; 70(4): 444–451 https://doi.org/10.1097/QAI.0000000000000809
pmid: 26302431
50
M Ragonnet-Cronin, YW Hu, SR Morris, Z Sheng, K Poortinga, JO Wertheim. HIV transmission networks among transgender women in Los Angeles County, CA, USA: a phylogenetic analysis of surveillance data. Lancet HIV 2019; 6(3): e164–e172 https://doi.org/10.1016/S2352-3018(18)30359-X
pmid: 30765313
51
X Li, H Liu, L Liu, Y Feng, ML Kalish, SYW Ho, Y Shao. Tracing the epidemic history of HIV-1 CRF01_AE clusters using near-complete genome sequences. Sci Rep 2017; 7(1): 4024 https://doi.org/10.1038/s41598-017-03820-8
pmid: 28642469
52
Z Li, X He, Z Wang, H Xing, F Li, Y Yang, Q Wang, Y Takebe, Y Shao. Tracing the origin and history of HIV-1 subtype B′ epidemic by near full-length genome analyses. AIDS 2012; 26(7): 877–884 https://doi.org/10.1097/QAD.0b013e328351430d
pmid: 22269972
53
J Ye, H Lu, X Su, R Xin, L Bai, K Xu, S Yu, X Feng, H Yan, X He, Y Zeng. Phylogenetic and temporal dynamics of human immunodeficiency virus type 1B in China: four types of B strains circulate in China. AIDS Res Hum Retroviruses 2014; 30(9): 920–926 https://doi.org/10.1089/aid.2014.0074
pmid: 25050980
54
Z Meng, R Xin, P Zhong, C Zhang, YF Abubakar, J Li, W Liu, X Zhang, J Xu. A new migration map of HIV-1 CRF07_BC in China: analysis of sequences from 12 provinces over a decade. PLoS One 2012; 7(12): e52373 https://doi.org/10.1371/journal.pone.0052373
pmid: 23300654
55
X Chen, M Ye, W Pang, DM Smith, C Zhang, YT Zheng. First appearance of HIV-1 CRF07_BC and CRF08_BC outside China. AIDS Res Hum Retroviruses 2017; 33(1): 74–76 https://doi.org/10.1089/aid.2016.0169
pmid: 27392826
56
X Han, Y Takebe, W Zhang, M An, B Zhao, Q Hu, J Xu, H Wu, J Wu, L Lu, X Chen, S Liang, Z Wang, H Yan, J Fu, W Cai, M Zhuang, C Liao, H Shang. A large-scale survey of CRF55_01B from men-who-have-sex-with-men in China: implying the evolutionary history and public health impact. Sci Rep 2015; 5(1): 18147 https://doi.org/10.1038/srep18147
pmid: 26667846
57
X Han, M An, M Zhang, B Zhao, H Wu, S Liang, X Chen, M Zhuang, H Yan, J Fu, L Lu, W Cai, Y Takebe, H Shang. Identification of 3 distinct HIV-1 founding strains responsible for expanding epidemic among men who have sex with men in 9 Chinese cities. J Acquir Immune Defic Syndr 2013; 64(1): 16–24 https://doi.org/10.1097/QAI.0b013e3182932210
pmid: 23542640
58
M An, X Han, J Xu, Z Chu, M Jia, H Wu, L Lu, Y Takebe, H Shang. Reconstituting the epidemic history of HIV strain CRF01_AE among men who have sex with men (MSM) in Liaoning, northeastern China: implications for the expanding epidemic among MSM in China. J Virol 2012; 86(22): 12402–12406 https://doi.org/10.1128/JVI.00262-12
pmid: 22933290
59
X Li, Y Xue, Y Lin, J Gai, L Zhang, H Cheng, Z Ning, L Zhou, K Zhu, G Vanham, L Kang, Y Wang, M Zhuang, Q Pan, P Zhong. Evolutionary dynamics and complicated genetic transmission network patterns of HIV-1 CRF01_AE among MSM in Shanghai, China. Sci Rep 2016; 6(1): 34729 https://doi.org/10.1038/srep34729
pmid: 27698457
60
Z Zhu, Y Hu, W Xing, M Guo, R Zhao, S Han, B Wu. Identifying symptom clusters among people living with HIV on antiretroviral therapy in China: a network analysis. J Pain Symptom Manage 2019; 57(3): 617–626 https://doi.org/10.1016/j.jpainsymman.2018.11.011
pmid: 30465875
61
Z Zhang, L Dai, Y Jiang, K Feng, L Liu, W Xia, F Yu, J Yao, W Xing, L Sun, T Zhang, H Wu, B Su, M Qiu. Transmission network characteristics based on env and gag sequences from MSM during acute HIV-1 infection in Beijing, China. Arch Virol 2017; 162(11): 3329–3338 https://doi.org/10.1007/s00705-017-3485-z
pmid: 28726130
62
X Li, K Zhu, Y Xue, F Wei, R Gao, R Duerr, K Fang, W Li, Y Song, G Du, W Yan, TH Musa, Y Ge, Y Ji, P Zhong, P Wei. Multiple introductions and onward transmission of HIV-1 subtype B strains in Shanghai, China. J Infect 2017; 75(2): 160–168 https://doi.org/10.1016/j.jinf.2017.05.009
pmid: 28551370
63
M Chen, Y Ma, H Chen, J Dai, L Dong, C Yang, Y Li, H Luo, R Zhang, X Jin, L Yang, AKL Cheung, M Jia, Z Song. HIV-1 genetic transmission networks among men who have sex with men in Kunming, China. PLoS One 2018; 13(4): e0196548 https://doi.org/10.1371/journal.pone.0196548
pmid: 29698467
64
Y Shao. AIDS molecular network research and AIDS precision prevention and control. 2018 National Conference on HIV and Hepatitis C Prevention and Treatment. April 19, 2018
65
X Wang, X He, P Zhong, Y Liu, T Gui, D Jia, H Li, J Wu, J Yan, D Kang, Y Han, T Li, R Yang, X Han, L Chen, J Zhao, H Xing, S Liang, J He, Y Yan, Y Xue, J Zhang, X Zhuang, S Liang, Z Bao, T Li, D Zhuang, S Liu, J Han, L Jia, J Li, L Li. Phylodynamics of major CRF01_AE epidemic clusters circulating in mainland of China. Sci Rep 2017; 7(1): 6330 https://doi.org/10.1038/s41598-017-06573-6
pmid: 28740095
66
EE Valverde, AM Oster, S Xu, JO Wertheim, AL Hernandez. HIV transmission dynamics among foreign-born persons in the United States. J Acquir Immune Defic Syndr 2017; 76(5): 445–452 https://doi.org/10.1097/QAI.0000000000001541
pmid: 28902072
67
EM Campbell, H Jia, A Shankar, D Hanson, W Luo, S Masciotra, SM Owen, AM Oster, RR Galang, MW Spiller, SJ Blosser, E Chapman, JC Roseberry, J Gentry, P Pontones, J Duwve, P Peyrani, RM Kagan, JM Whitcomb, PJ Peters, W Heneine, JT Brooks, WM Switzer. Detailed transmission network analysis of a large opiate-driven outbreak of HIV infection in the United States. J Infect Dis 2017; 216(9): 1053–1062 https://doi.org/10.1093/infdis/jix307
pmid: 29029156
68
AFY Poon, R Gustafson, P Daly, L Zerr, SE Demlow, J Wong, CK Woods, RS Hogg, M Krajden, D Moore, P Kendall, JSG Montaner, PR Harrigan. Near real-time monitoring of HIV transmission hotspots from routine HIV genotyping: an implementation case study. Lancet HIV 2016; 3(5): e231–e238 https://doi.org/10.1016/S2352-3018(16)00046-1
pmid: 27126490
69
DK Pasquale, IA Doherty, LA Sampson, S Hué, PA Leone, J Sebastian, SL Ledford, JJ Eron, WC Miller, AM Dennis. Leveraging phylogenetics to understand HIV transmission and partner notification networks. J Acquir Immune Defic Syndr 2018; 78(4): 367–375 https://doi.org/10.1097/QAI.0000000000001695
pmid: 29940601
70
D Avila, O Keiser, M Egger, R Kouyos, J Böni, S Yerly, T Klimkait, PL Vernazza, V Aubert, A Rauch, S Bonhoeffer, HF Günthard, T Stadler, BD Spycher; Swiss HIV Cohort Study. Social meets molecular: combining phylogenetic and latent class analyses to understand HIV-1 transmission in Switzerland. Am J Epidemiol 2014; 179(12): 1514–1525 https://doi.org/10.1093/aje/kwu076
pmid: 24821749
71
JO Wertheim, SL Kosakovsky Pond, LA Forgione, SR Mehta, B Murrell, S Shah, DM Smith, K Scheffler, LV Torian. Social and genetic networks of HIV-1 transmission in New York City. PLoS Pathog 2017; 13(1): e1006000 https://doi.org/10.1371/journal.ppat.1006000
pmid: 28068413
72
EG Kostaki, GK Nikolopoulos, E Pavlitina, L Williams, G Magiorkinis, J Schneider, B Skaathun, E Morgan, M Psichogiou, GL Daikos, V Sypsa, P Smyrnov, A Korobchuk, M Malliori, A Hatzakis, SR Friedman, D Paraskevis. Molecular analysis of human immunodeficiency virus type 1 (HIV-1)-infected individuals in a network-based intervention (Transmission Reduction Intervention Project): phylogenetics identify HIV-1-infected individuals with social links. J Infect Dis 2018; 218(5): 707–715 https://doi.org/10.1093/infdis/jiy239
pmid: 29697829
73
AJ Leigh Brown, SJ Lycett, L Weinert, GJ Hughes, E Fearnhill, DT Dunn; UK HIV Drug Resistance Collaboration. Transmission network parameters estimated from HIV sequences for a nationwide epidemic. J Infect Dis 2011; 204(9): 1463–1469 https://doi.org/10.1093/infdis/jir550
pmid: 21921202
74
AM France, N Panneer, CB Ocfemia, N Saduvala, E Campbell, WM Switzer, J Wertheim, AM Oster. Rapidly growing HIV transmission clusters in the Unites States, 2013–2016. 2018 Conference on Retroviruses and Opportunistic Infections. March 4–7, 2018
75
JO Wertheim, AM Oster, WM Switzer, C Zhang, N Panneer, E Campbell, N Saduvala, JA Johnson, W Heneine. Natural selection favoring more transmissible HIV detected in United States molecular transmission network. Nat Commun 2019; 10(1): 5788 https://doi.org/10.1038/s41467-019-13723-z
pmid: 31857582
76
PJ Peters, P Pontones, KW Hoover, MR Patel, RR Galang, J Shields, SJ Blosser, MW Spiller, B Combs, WM Switzer, C Conrad, J Gentry, Y Khudyakov, D Waterhouse, SM Owen, E Chapman, JC Roseberry, V McCants, PJ Weidle, D Broz, T Samandari, J Mermin, J Walthall, JT Brooks, JM Duwve; Indiana HIV Outbreak Investigation Team.HIV infection linked to injection use of oxymorphone in Indiana, 2014-–2015. N Engl J Med 2016; 375(3): 229–239 https://doi.org/10.1056/NEJMoa1515195
pmid: 27468059
77
A Monterosso, S Minnerly, S Goings, A Morris, AM France, S Dasgupta, AM Oster, M Fanning. Identifying and investigating a rapidly growing HIV transmission cluster in Texas. Conference on Retroviruses and Opportunistic Infections. March 8, 2017. Seattle, Washington
78
H Shang, J Xu, X Han, J Spero Li, KC Arledge, L Zhang. HIV prevention: bring safe sex to China. Nature 2012; 485(7400): 576–577 https://doi.org/10.1038/485576a
pmid: 22660303
79
JO Wertheim, B Murrell, SR Mehta, LA Forgione, SL Kosakovsky Pond, DM Smith, LV Torian. Growth of HIV-1 molecular transmission clusters in New York City. J Infect Dis 2018; 218(12): 1943–1953 https://doi.org/10.1093/infdis/jiy431
pmid: 30010850
80
SR Mehta, B Murrell, CM Anderson, SL Kosakovsky Pond, JO Wertheim, JA Young, L Freitas, DD Richman, WC Mathews, K Scheffler, SJ Little, DM Smith. Using HIV sequence and epidemiologic data to assess the effect of self-referral testing for acute HIV infection on incident diagnoses in San Diego, California. Clin Infect Dis 2016; 63(1): 101–107 https://doi.org/10.1093/cid/ciw161
pmid: 27174704
81
H Heesterbeek, RM Anderson, V Andreasen, S Bansal, D De Angelis, C Dye, KT Eames, WJ Edmunds, SD Frost, S Funk, TD Hollingsworth, T House, V Isham, P Klepac, J Lessler, JO Lloyd-Smith, CJ Metcalf, D Mollison, L Pellis, JR Pulliam, MG Roberts, C Viboud; Isaac Newton Institute IDD Collaboration. Modeling infectious disease dynamics in the complex landscape of global health. Science 2015; 347(6227): aaa4339 https://doi.org/10.1126/science.aaa4339
pmid: 25766240
82
T Stadler, R Kouyos, V von Wyl, S Yerly, J Böni, P Bürgisser, T Klimkait, B Joos, P Rieder, D Xie, HF Günthard, AJ Drummond, S Bonhoeffer; Swiss HIV Cohort Study. Estimating the basic reproductive number from viral sequence data. Mol Biol Evol 2012; 29(1): 347–357 https://doi.org/10.1093/molbev/msr217
pmid: 21890480
83
T Turk, N Bachmann, C Kadelka, J Büni, S Yerly, V Aubert, T Klimkait, M Battegay, E Bernasconi, A Calmy, M Cavassini, H Furrer, M Hoffmann, HF Günthard, RD Kouyos, V Aubert, M Battegay, E Bernasconi, J Böni, DL Braun, HC Bucher, A Calmy, M Cavassini, A Ciuffi, G Dollenmaier, M Egger, L Elzi, J Fehr, J Fellay, H Furrer, CA Fux, HF Günthard, D Haerry, B Hasse, HH Hirsch, M Hoffmann, I Hösli, C Kahlert, L Kaiser, O Keiser, T Klimkait, RD Kouyos, H Kovari, B Ledergerber, G Martinetti, B Martinez de Tejada, C Marzolini, KJ Metzner, N Müller, D Nicca, G Pantaleo, P Paioni, A Rauch, C Rudin, AU Scherrer, P Schmid, R Speck, M Stöckle, P Tarr, A Trkola, P Vernazza, G Wandeler, R Weber, S Yerly. Assessing the danger of self-sustained HIV epidemics in heterosexuals by population based phylogenetic cluster analysis. eLife 2017; 6: e28721 https://doi.org/10.7554/eLife.28721
pmid: 28895527
84
AM France, AM Oster. The promise and complexities of detecting and monitoring HIV transmission clusters. J Infect Dis 2019 Apr 27. [Epub ahead of print] doi: 10.1093/infdis/jiz177 https://doi.org/10.1093/infdis/jiz177
pmid: 31028707
85
V Novitsky, S Moyo, Q Lei, V DeGruttola, M Essex. Impact of sampling density on the extent of HIV clustering. AIDS Res Hum Retroviruses 2014; 30(12): 1226–1235 https://doi.org/10.1089/aid.2014.0173
pmid: 25275430
86
A Chaillon, C Delaugerre, B Brenner, A Armero, C Capitant, ML Nere, N Leturque, G Pialoux, E Cua, C Tremblay, DM Smith, C Goujard, L Meyer, JM Molina, ML Chaix. In-depth sampling of high-risk populations to characterize HIV transmission epidemics among young MSM using PrEP in France and Quebec. Open Forum Infect Dis 2019; 6(3): ofz080 https://doi.org/10.1093/ofid/ofz080
pmid: 30899768
87
SL Kosakovsky Pond, S Weaver, AJ Leigh Brown, JO Wertheim. HIV-TRACE (Transmission Cluster Engine): a tool for large scale molecular epidemiology of HIV-1 and other rapidly evolving pathogens. Mol Biol Evol 2018; 35(7): 1812–1819 https://doi.org/10.1093/molbev/msy016
pmid: 29401317
88
AM Dennis, DK Pasquale, R Billock, S Beagle, V Mobley, A Cope, J Kuruc, J Sebastian, C Walworth, PA Leone. Integration of contact tracing and phylogenetics in an investigation of acute HIV infection. Sex Transm Dis 2018; 45(4): 222–228 https://doi.org/10.1097/OLQ.0000000000000726
pmid: 29465708
89
AG Fitzmaurice, L Linley, C Zhang, M Watson, AM France, AM Oster. Novel method for rapid detection of spatiotemporal HIV clusters potentially warranting intervention. Emerg Infect Dis 2019; 25(5): 988–991 https://doi.org/10.3201/eid2505.180776
pmid: 31002076
90
GK Hightower, SJ May, J Pérez-Santiago, ME Pacold, GA Wagner, SJ Little, DD Richman, SR Mehta, DM Smith, SL Pond. HIV-1 clade B pol evolution following primary infection. PLoS One 2013; 8(6): e68188 https://doi.org/10.1371/journal.pone.0068188
pmid: 23840830
91
J Hemelaar, R Elangovan, J Yun, L Dickson-Tetteh, I Fleminger, S Kirtley, B Williams, E Gouws-Williams, PD Ghys; WHO–UNAIDS Network for HIV Isolation Characterisation. Global and regional molecular epidemiology of HIV-1, 1990–2015: a systematic review, global survey, and trend analysis. Lancet Infect Dis 2019; 19(2): 143–155 https://doi.org/10.1016/S1473-3099(18)30647-9
pmid: 30509777
L Fabeni, C Alteri, G Berno, R Scutari, N Orchi, G De Carli, A Bertoli, L Carioti, C Gori, F Forbici, R Salpini, A Vergori, R Gagliardini, S Cicalini, A Mondi, C Pinnetti, L Mazzuti, O Turriziani, M Colafigli, V Borghi, F Montella, A Pennica, M Lichtner, E Girardi, M Andreoni, C Mussini, A Antinori, F Ceccherini-Silberstein, CF Perno, MM4 Santoro; SENDIH Study group. Characterisation of HIV-1 molecular transmission clusters among newly diagnosed individuals infected with non-B subtypes in Italy. Sex Transm Infect 2019; 95 (8): 619–625 https://doi.org/10.1136/sextrans-2019-054017
pmid: 31076456
94
I Bon, M Ciccozzi, G Zehender, C Biagetti, G Verrucchi, A Lai, A Lo Presti, D Gibellini, MC Re. HIV-1 subtype C transmission network: the phylogenetic reconstruction strongly supports the epidemiological data. J Clin Virol 2010; 48(3): 212–214 https://doi.org/10.1016/j.jcv.2010.03.021
pmid: 20400369
95
M Parczewski, M Leszczyszyn-Pynka, D Bander, A Urbanska, A Boroń-Kaczmarska. HIV-1 subtype D infections among Caucasians from Northwestern Poland—phylogenetic and clinical analysis. PLoS One 2012; 7(2): e31674 https://doi.org/10.1371/journal.pone.0031674
pmid: 22359615
MC Prosperi, A De Luca, S Di Giambenedetto, L Bracciale, M Fabbiani, R Cauda, M Salemi. The threshold bootstrap clustering: a new approach to find families or transmission clusters within molecular quasispecies. PLoS One 2010; 5(10): e13619 https://doi.org/10.1371/journal.pone.0013619
pmid: 21049051
98
I Vrbik, DA Stephens, M Roger, BG Brenner. The Gap Procedure: for the identification of phylogenetic clusters in HIV-1 sequence data. BMC Bioinformatics 2015; 16(1): 355 https://doi.org/10.1186/s12859-015-0791-x
pmid: 26538192
99
SL Kosakovsky Pond, S Weaver, AJ Leigh Brown, JO Wertheim. HIV-TRACE (TRAnsmission Cluster Engine): a tool for large scale molecular epidemiology of HIV-1 and other rapidly evolving pathogens. Mol Biol Evol 2018; 35(7): 1812–1819 https://doi.org/10.1093/molbev/msy016
pmid: 29401317
100
S Hué, JP Clewley, PA Cane, D Pillay. HIV-1 pol gene variation is sufficient for reconstruction of transmissions in the era of antiretroviral therapy. AIDS 2004; 18(5): 719–728 https://doi.org/10.1097/00002030-200403260-00002
pmid: 15075506