Heroin type, injecting behavior, and HIV transmission. A simulation model of HIV incidence and prevalence

Autoři: Georgiy Bobashev aff001;  Sarah Mars aff002;  Nicholas Murphy aff002;  Clinton Dreisbach aff001;  William Zule aff003;  Daniel Ciccarone aff002
Působiště autorů: Center for Data Science, RTI International, Research Triangle Park, NC, United States of America aff001;  University of California, San Francisco, Department of Family and Community Medicine, San Francisco, CA, United States of America aff002;  Center for Global Health, RTI International, Research Triangle Park, NC, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0215042


Background and aims

Using mathematical modeling to illustrate and predict how different heroin source-forms: “black tar” (BTH) and powder heroin (PH) can affect HIV transmission in the context of contrasting injecting practices. By quantifying HIV risk by these two heroin source-types we show how each affects the incidence and prevalence of HIV over time. From 1997 to 2010 PH reaching the United States was manufactured overwhelmingly by Colombian suppliers and distributed in the eastern states of the United States. Recently Mexican cartels that supply the western U.S. states have started to produce PH too, replacing Colombian distribution to the east. This raises the possibility that BTH in the western U.S. may be replaced by PH in the future.


We used an agent-based model to evaluate the impact of use of different heroin formulations in high- and low-risk populations of persons who inject drugs (PWID) who use different types of syringes (high vs. low dead space) and injecting practices. We obtained model parameters from peer-reviewed publications and ethnographic research.


Heating of BTH, additional syringe rinsing, and subcutaneous injection can substantially decrease the risk of HIV transmission. Simulation analysis shows that HIV transmission risk may be strongly affected by the type of heroin used. We reproduced historic differences in HIV prevalence and incidence. The protective effect of BTH is much stronger in high-risk compared with low-risk populations. Simulation of future outbreaks show that when PH replaces BTH we expect a long-term overall increase in HIV prevalence. In a population of PWID with mixed low- and high-risk clusters we find that local HIV outbreaks can occur even when the overall prevalence and incidence are low. The results are dependent on evidence-supported assumptions.


The results support harm-reduction measures focused on a reduction in syringe sharing and promoting protective measures of syringe rinsing and drug solution heating.

Klíčová slova:

Agent-based modeling – Heroin – HIV epidemiology – HIV infections – Simulation and modeling – Tar – Viral load


1. Unick GJ, Rosenblum D, Mars S, Ciccarone D. Intertwined epidemics: national demographic trends in hospitalizations for heroin- and opioid-related overdoses, 1993–2009. PLoS One. 2013;8(2): e54496. doi: 10.1371/journal.pone.0054496 23405084

2. Ciccarone D. Fentanyl in the US heroin supply: A rapidly changing risk environment. Int J Drug Policy. 2017 Aug;46: 107–111. doi: 10.1016/j.drugpo.2017.06.010 28735776

3. Martins SS, Sarvet A, Santaella-Tenorio J, Saha T, Grant BF, Hasin DS. Changes in US Lifetime Heroin Use and Heroin Use Disorder: Prevalence From the 2001–2002 to 2012–2013 National Epidemiologic Survey on Alcohol and Related Conditions. JAMA psychiatry. 2017 May 1;74(5): 445–455. doi: 10.1001/jamapsychiatry.2017.0113 28355458

4. Lansky A, Finlayson T, Johnson C, Holtzman D, Wejnert C, Mitsch A, et al. Estimating the number of persons who inject drugs in the United States by meta-analysis to calculate national rates of HIV and hepatitis C virus infections. PLoS One. 2014;9(5): e97596. doi: 10.1371/journal.pone.0097596 24840662

5. Des Jarlais DC, Dehne K, Casabona J. HIV surveillance among injecting drug users. AIDS. 2001;15: S13–S22.

6. Ciccarone D, Bourgois P. Explaining the geographical variation of HIV among injection drug users in the United States. Subst Use Misuse. 2003 Dec;38(14): 2049–2063. doi: 10.1081/JA-120025125 14677781

7. Centers for Disease Control and Prevention. HIV infection and HIV-associated behaviors among injecting drug users—20 cities, United States, 2009. J Am Med Assoc. 2012;308(4): 332–335.

8. Tempalski B, Lieb S, Cleland CM, Cooper H, Brady JE, Friedman SR. HIV prevalence rates among injection drug users in 96 large US metropolitan areas, 1992–2002. J Urban Health. 2009 Jan;86(1): 132–154. doi: 10.1007/s11524-008-9328-1 19015995

9. Holmberg SD. The estimated prevalence and incidence of HIV in 96 large US metropolitan areas. Am J Public Health. 1996 May;86(5): 642–654. doi: 10.2105/ajph.86.5.642 8629714

10. Ciccarone D. Heroin in brown, black and white: structural factors and medical consequences in the US heroin market. Int J Drug Policy. 2009 May;20(3): 277–282. doi: 10.1016/j.drugpo.2008.08.003 18945606

11. US Drug Enforcement Administration. National Drug Threat Assessment. Washington, DC: 2017 DEA-DCT-DIR-040-17.

12. Clatts MC, Heimer R, Abdala N, Goldsamt LA, Sotheran JL, Anderson KT, et al. HIV-1 transmission in injection paraphernalia: heating drug solutions may inactivate HIV-1. J Acquir Immune Defic Syndr Hum Retrovirol. 1999 Oct 1;22(2): 194–199.

13. Ciccarone D. Saying goodbye to high-dead-space syringes. Int J Drug Policy. 2013 Jan;24(1): 15–16. doi: 10.1016/j.drugpo.2012.09.011 23127666

14. Mars SG, Bourgois P, Karandinos G, Montero F, Ciccarone D. The textures of heroin: user perspectives on "black tar" and powder heroin in two U.S. cities. J Psychoactive Drugs. 2016 Sep-Oct;48(4): 270–278. doi: 10.1080/02791072.2016.1207826 27440088

15. Ciccarone D, Barnberger JD, Kral AH, Edlin BR, Hobart CJ, Moon A, et al. Soft tissue infections among injection drug users—San Francisco, California, 1996–2000. J Am Med Assoc. 2001;285(21): 2707–2709. doi: 10.1001/jama.285.21.2707-JWR0606-3-1

16. Bourgois P, & Schonberg J. Righteous dopefiend. Berkeley and Los Angeles, CA: University of California Press; 2009.

17. Rich JD, Dickinson BP, Carney JM, Fisher A, Heimer R. Detection of HIV-1 nucleic acid and HIV-1 antibodies in needles and syringes used for non-intravenous injection. AIDS. 1998 Dec 3;12(17): 2345–2350. doi: 10.1097/00002030-199817000-00017 9863878

18. Ciccarone D, Harris M. Fire in the vein: heroin acidity and its proximal effect on users' health. Int J Drug Policy. 2015 Nov;26(11): 1103–1110. doi: 10.1016/j.drugpo.2015.04.009 26077143

19. Heimer R, Kinzly ML, He H, Abdala N. The effect of acids on the survival of HIV during drug injection. J Acquir Immune Defic Syndr Hum Retrovirol. 2007 Jun 1;45(2): 144–150. doi: 10.1097/QAI.0b013e318042aede 17356472

20. Zule WA, Latypov A, Otiashvili D, Bangel S, Bobashev GV. Feasibility of needle and syringe programs in Tajikistan distributing low dead space needles. Harm Reduct J. 2018 Aug 31;15(1): 44. doi: 10.1186/s12954-018-0249-3 30170604

21. Zule WA, Pande PG, Otiashvili D, Bobashev GV, Friedman SR, Gyarmathy VA, et al. Options for reducing HIV transmission related to the dead space in needles and syringes. Harm Reduct J. 2018 Jan 15;15(1): 3. doi: 10.1186/s12954-017-0207-5 29334973

22. Zule WA, Ticknor-Stellato KM, Desmond DP, Vogtsberger KN. Evaluation of needle and syringe combinations. J Acquir Immune Defic Syndr Hum Retrovirol. 1997 Mar 1;14(3): 294–295. doi: 10.1097/00042560-199703010-00015 9117464

23. Bobashev GV, Zule WA. Modeling the effect of high dead-space syringes on the human immunodeficiency virus (HIV) epidemic among injecting drug users. Addiction. 2010 Aug;105(8): 1439–1447. doi: 10.1111/j.1360-0443.2010.02976.x 20528817

24. Hudgens MG, Longini IM, Halloran ME, Choopanya K, Vanichseni S, Kitayaporn D, et al. Estimating the transmission probability of human immunodeficiency virus in injecting drug users in Thailand. J Roy Stat Soc C-App. 2001;50(1): 1–14. doi: 10.1111/1467-9876.00216

25. Hudgens MG, Longini IM Jr., Vanichseni S, Hu DJ, Kitayaporn D, Mock PA, et al. Subtype-specific transmission probabilities for human immunodeficiency virus type 1 among injecting drug users in Bangkok, Thailand. Am J Epidemiol. 2002 Jan 15;155(2): 159–168. doi: 10.1093/aje/155.2.159 11790680

26. Kaplan EH, Heimer R. A model-based estimate of HIV infectivity via needle sharing. J Acquir Immune Defic Syndr Hum Retrovirol. 1992;5(11): 1116–1118.

27. Patel P, Borkowf CB, Brooks JT, Lasry A, Lansky A, Mermin J. Estimating per-act HIV transmission risk: a systematic review. AIDS. 2014 Jun 19;28(10): 1509–1519. doi: 10.1097/QAD.0000000000000298 24809629

28. Zule WA, Bobashev G. High dead-space syringes and the risk of HIV and HCV infection among injecting drug users. Drug Alcohol Depend. 2009 Mar 1;100(3): 204–213. doi: 10.1016/j.drugalcdep.2008.08.017 19004579

29. Stratfor. Criminal commodities series: black tar heroin 2012 [cited Austin, TX: Stratfor. Available: https://worldview.stratfor.com/article/criminal-commodities-series-black-tar-heroin.

30. Baggaley RF, Boily MC, White RG, Alary M. Risk of HIV-1 transmission for parenteral exposure and blood transfusion: a systematic review and meta-analysis. AIDS. 2006 Apr 4;20(6): 805–812. doi: 10.1097/01.aids.0000218543.46963.6d 16549963

31. Wilson DP, Law MG, Grulich AE, Cooper DA, Kaldor JM. Relation between HIV viral load and infectiousness: a model-based analysis. Lancet. 2008 Jul 26;372(9635): 314–320. doi: 10.1016/S0140-6736(08)61115-0 18657710

32. Passaro DJ, Werner SB, McGee J, Mac Kenzie WR, Vugia DJ. Wound botulism associated with black tar heroin among injecting drug users. Jama-J Am Med Assoc. 1998 Mar 18;279(11): 859–863. doi: 10.1001/jama.279.11.859 9516001

33. Zule WA, Desmond DP, Neff JA. Syringe type and drug injector risk for HIV infection: a case study in Texas. Soc Sci Med. 2002 Oct;55(7): 1103–1113. doi: 10.1016/s0277-9536(01)00256-8 12365524

34. Friedman SR, Kottiri BJ, Neaigus A, Curtis R, Vermund SH, Des Jarlais DC. Network-related mechanisms may help explain long-term HIV-1 seroprevalence levels that remain high but do not approach population-group saturation. Am J Epidemiol. 2000 Nov 15;152(10): 913–922. doi: 10.1093/aje/152.10.913 11092433

35. Zule WA, Latypov A, Otiashvili D, Kirtadze I, Ibragimov U, Bobashev GV. Factors that influence the characteristics of needles and syringes used by people who inject drugs in Tajikistan. Harm Reduct J. 2015 Oct 16;12: 37. doi: 10.1186/s12954-015-0069-7 26472669

36. Jacquez JA, Koopman JS, Simon CP, Longini IM Jr. Role of the primary infection in epidemics of HIV infection in gay cohorts. J Acquir Immune Defic Syndr Hum Retrovirol. 1994 Nov;7(11): 1169–1184.

37. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, Peddada L, et al. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS. 2003 Sep 5;17(13): 1871–1879. doi: 10.1097/00002030-200309050-00005 12960819

38. Bailey SL, Ouellet LJ, Mackesy-Amiti ME, Golub ET, Hagan H, Hudson SM, et al. Perceived risk, peer influences, and injection partner type predict receptive syringe sharing among young adult injection drug users in five U.S. cities. Drug Alcohol Depend. 2007 Nov;91 Suppl 1(Suppl 1): S18–29. doi: 10.1016/j.drugalcdep.2007.02.014 17434267

39. De P, Cox J, Boivin JF, Platt RW, Jolly AM. The importance of social networks in their association to drug equipment sharing among injection drug users: a review. Addiction. 2007 Nov;102(11): 1730–1739. doi: 10.1111/j.1360-0443.2007.01936.x 17935581

40. Centers for Disease Control and Prevention. Access to clean syringes. Atlanta, GA: 2016

41. Gibson DR, Flynn NM, Perales D. Effectiveness of syringe exchange programs in reducing HIV risk behavior and HIV seroconversion among injecting drug users. AIDS. 2001 Jul 27;15(11): 1329–1341. doi: 10.1097/00002030-200107270-00002 11504954

42. amfAR. Syringe services programs and the opioid epidemic. 2017 November 3 [cited 01/08/2019 New York: amfAR. Available: https://www.amfar.org/ssp-opioid-epidemic/

43. Mars SG, Bourgois P, Karandinos G, Montero F, Ciccarone D. "Every 'never' I ever said came true": transitions from opioid pills to heroin injecting. Int J Drug Policy. 2014 Mar;25(2): 257–266. doi: 10.1016/j.drugpo.2013.10.004 24238956

44. Broz D, Zibbell J, Foote C, Roseberry JC, Patel MR, Conrad C, et al. Multiple injections per injection episode: High-risk injection practice among people who injected pills during the 2015 HIV outbreak in Indiana. Int J Drug Policy. 2018 Feb;52: 97–101. doi: 10.1016/j.drugpo.2017.12.003 29278838

45. Peters PJ, Pontones P, Hoover KW, Patel MR, Galang RR, Shields J, et al. HIV Infection Linked to Injection Use of Oxymorphone in Indiana, 2014–2015. N Engl J Med. 2016 Jul 21;375(3): 229–239. doi: 10.1056/NEJMoa1515195 27468059

46. Zhong L, Zhang Q, Li X. Modeling the intervention of HIV transmission across intertwined key populations. Sci Rep. 2018 Feb 5;8(1): 2432. doi: 10.1038/s41598-018-20864-6 29402964

47. Dombrowski K, Curtis R, Friedman S, Khan B. Topological and historical considerations for infectious disease transmission among injecting drug users in Bushwick, Brooklyn (USA). World J AIDS. 2013 Mar 1;3(1): 1–9. doi: 10.4236/wja.2013.31001 24672745

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden