272
Views
2
CrossRef citations to date
0
Altmetric
Review Articles

How the evolving epidemics of opioid misuse and HIV infection may be changing the risk of oral sexually transmitted infection risk through microbiome modulation

, , &
Pages 49-60 | Received 04 Oct 2019, Accepted 07 Jan 2020, Published online: 30 Jan 2020

References

  • Administration SAaMHS. 2017. Key substance use and mental health indicators in the United States: Results from the 2016 National Survey on Drug Use and Health (HHS Publication No. SMA 17-5044, NSDUH Series H-52). Rockville, MD: Center for Behavioral Health Statistics and Quality SAaMHSA.
  • Administration SAaMHS. 2018. Key substance use and mental health indicators in the United States: Results from the 2017 National Survey on Drug Use and Health (HHS Publication No. SMA 18-5068, NSDUH Series H-53). Rockville, MD: Quality CfBHSa.
  • Allen-Vercoe E, Jobin C. 2014. Fusobacterium and Enterobacteriaceae: important players for CRC? Immunol Lett. 162(2):54–61.
  • Anschuetz GL, Paulukonis E, Powers R, Asbel LE. 2016. Extragenital screening in men who have sex with men diagnoses more Chlamydia and Gonorrhea cases than urine testing alone. Sex Transm Dis. 43(5):299–301.
  • Bandera A, De Benedetto I, Bozzi G, Gori A. 2018. Altered gut microbiome composition in HIV infection: causes, effects and potential intervention. Curr Opin HIV AIDS. 13(1):73–80.
  • Beck JM, Schloss PD, Venkataraman A, Twigg H, 3rd, Jablonski KA, Bushman FD, Campbell TB, Charlson ES, Collman RG, Crothers K, Lung HIV Microbiome Project. et al. 2015. Multicenter comparison of lung and oral microbiomes of HIV-infected and HIV-uninfected individuals. Am J Respir Crit Care Med. 192(11):1335–1344.
  • Belkaid Y, Hand TW. 2014. Role of the microbiota in immunity and inflammation. Cell. 157(1):121–141.
  • Benyamin R, Trescot AM, Datta S, Buenaventura R, Adlaka R, Sehgal N, Glaser SE, Vallejo R. 2008. Opioid complications and side effects. Pain Physician. 11(2 Suppl):S105–S120.
  • Bergmann OJ. 1988. Oral infections and septicemia in immunocompromised patients with hematologic malignancies. J Clin Microbiol. 26(10):2105–2109.
  • Borrow P. 2011. Innate immunity in acute HIV-1 infection. Curr Opin HIV AIDS. 6(5):353–363.
  • Butler J, Kalogeropoulos AP, Anstrom KJ, Hsue PY, Kim RJ, Scherzer R, Shah SJ, Shah SH, Velazquez EJ, Hernandez AF, et al. 2018. Diastolic dysfunction in individuals with human immunodeficiency virus infection: literature review, rationale and design of the Characterizing Heart Function on Antiretroviral Therapy (CHART) study. J Card Fail. 24(4):255–265.
  • Cabral GA. 2006. Drugs of abuse, immune modulation, and AIDS. J Neuroimmune Pharm. 1(3):280–295.
  • Centers for Disease Control and Prevention. 2019a. HIV in the United States and dependent areas. [accessed 2019 Sep 10]. https://www.cdc.gov/hiv/statistics/overview/ataglance.html.
  • Centers for Disease Control and Prevention. 2019b. HIV risk behaviors [accessed 10 Sep 2019]. https://www.cdc.gov/hiv/risk/estimates/riskbehaviors.html.
  • Centers for Disease Control and Prevention. 2017a. Sexually transmitted disease surveillance. [accessed 2019 Sep 10]. https://www.cdc.gov/std/stats17/default.htm.
  • Centers for Disease Control and Prevention. 2016. STD risk and oral sex - CDC fact sheet [accessed 2019 Sep 10]. https://www.cdc.gov/std/healthcomm/stdfact-stdriskandoralsex.htm.
  • Centers for Disease Control and Prevention. 2017b. STDs at record high, indicating urgent need for prevention [accessed 2019 Sep 10]. https://www.cdc.gov/media/releases/2017/p0926-std-prevention.html.
  • Chan PA, Robinette A, Montgomery M, Almonte A, Cu-Uvin S, Lonks JR, Chapin KC, Kojic EM, Hardy EJ. 2016. Extragenital infections caused by Chlamydia trachomatis and Neisseria gonorrhoeae: a review of the literature. Infect Dis Obstet Gynecol. 2016:1–17.
  • Chung CY, Alden SL, Funderburg NT, Fu P, Levine AD. 2014. Progressive proximal-to-distal reduction in expression of the tight junction complex in colonic epithelium of virally-suppressed HIV + individuals. PLoS Pathog. 10(6):e1004198.
  • Coghill AE, Pfeiffer RM, Shiels MS, Engels EA. 2017. Excess mortality among HIV-infected individuals with cancer in the United States. Cancer Epidemiol Biomarkers Prev. 26(7):1027–1033.
  • Cohen S, Janicki-Deverts D, Miller GE. 2007. Psychological stress and disease. JAMA. 298(14):1685–1687.
  • Cohen S, Janicki-Deverts D, Doyle WJ, Miller GE, Frank E, Rabin BS, Turner RB. 2012. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc Natl Acad Sci USA. 109(16):5995–5999.
  • Coleman DC, Bennett DE, Sullivan DJ, Gallagher PJ, Henman MC, Shanley DB, Russell RJ. 1993. Oral Candida in HIV infection and AIDS: new perspectives/new approaches. Crit Rev Microbiol. 19(2):61–82.
  • Cooper HL, Bossak B, Tempalski B, Des Jarlais DC, Friedman SR. 2009. Geographic approaches to quantifying the risk environment: drug-related law enforcement and access to syringe exchange programmes. Int J Drug Policy. 20(3):217–226.
  • Culhane JF, Rauh VA, Goldenberg RL. 2006. Stress, bacterial vaginosis, and the role of immune processes. Curr Infect Dis Rep. 8(6):459–464.
  • da Fonseca DM, Hand TW, Han SJ, Gerner MY, Zaretsky AG, Byrd AL, Harrison OJ, Ortiz AM, Quinones M, Trinchieri G, et al. 2015. Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell. 163(2):354–366.
  • Dang AT, Cotton S, Sankaran-Walters S, Li C-S, Lee C-Y, Dandekar S, Paster BJ, George MD. 2012. Evidence of an increased pathogenic footprint in the lingual microbiome of untreated HIV infected patients. BMC Microbiol. 12(1):153.
  • Dart RC, Surratt HL, Cicero TJ, Parrino MW, Severtson SG, Bucher-Bartelson B, Green JL. 2015. Trends in opioid analgesic abuse and mortality in the United States. N Engl J Med. 372(3):241–248.
  • Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR, Yu WH, Lakshmanan A, Wade WG. 2010. The human oral microbiome. J Bacteriol. 192(19):5002–5017.
  • Docktor MJ, Paster BJ, Abramowicz S, Ingram J, Wang YE, Correll M, Jiang H, Cotton SL, Kokaras AS, Bousvaros A, et al. 2012. Alterations in diversity of the oral microbiome in pediatric inflammatory bowel disease. Bowel Dis. 18(5):935–942.
  • Doitsh G, Greene W. 2016. Dissecting how CD4 T cells are lost during HIV infection. Cell Host Microbe. 19(3):280–291.
  • Donahoe RM, Vlahov D. 1998. Opiates as potential cofactors in progression of HIV-1 infections to AIDS. J Neuroimmunol. 83(1-2):77–87.
  • Dubourg G. 2016. Impact of HIV on the human gut microbiota: challenges and perspectives. Human Microbiome J. 2:3–9.
  • Eastment MC, McClelland RS. 2018. Vaginal microbiota and susceptibility to HIV. AIDS. 32(6):687–698.
  • Ethan Morgan HT, Ryan D, D’Aquila R, Mustanski B. 2018. Systemic inflammation is elevated among both HIV-uninfected and -infected young men who have sex with men. AIDS. 33(4):757–759.
  • Fichorova RN, Chen P-L, Morrison CS, Doncel GF, Mendonca K, Kwok C, Chipato T, Salata R, Mauck C. 2015. The contribution of cervicovaginal infections to the immunomodulatory effects of hormonal contraception. MBio. 6(5):e00221–00215.
  • Filardo S, Di Pietro M, Tranquilli G, Sessa R. 2019. Biofilm in genital ecosystem: a potential risk factor for Chlamydia trachomatis infection. Can J Infect Dis Med Microbiol. 2019:1–6.
  • Gao L, Xu T, Huang G, Jiang S, Gu Y, Chen F. 2018. Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell. 9(5):488–500.
  • Goulart LS, Souza WWR, Vieira CA, Lima JS, Olinda RA, Araujo C. 2018. Oral colonization by Candida species in HIV-positive patients: association and antifungal susceptibility study. Einstein. 16(3):eAO4224.
  • Gruenewald TL, Cohen S, Matthews KA, Tracy R, Seeman TE. 2009. Association of socioeconomic status with inflammation markers in black and white men and women in the Coronary Artery Risk Development in Young Adults (CARDIA) study. Soc Sci Med. 69(3):451–459.
  • Habel MA, Leichliter JS, Dittus PJ, Spicknall IH, Aral SO. 2018. Heterosexual anal and oral sex in adolescents and adults in the United States, 2011-2015. Sex Transm Dis. 45(12):775–782.
  • Haro C, Rangel-Zúñiga OA, Alcalá-Díaz JF, Gómez-Delgado F, Pérez-Martínez P, Delgado-Lista J, Quintana-Navarro GM, Landa BB, Navas-Cortés JA, Tena-Sempere M, et al. 2016. Intestinal microbiota is influenced by gender and body mass index. Plos One. 11(5):e0154090.
  • Hester RA, Kennedy SB. 2003. Candida infection as a risk factor for HIV transmission. J Womens Health (Larchmt). 12(5):487–494.
  • Holbrook AM, Baxter JK, Jones HE, Heil SH, Coyle MG, Martin PR, Stine SM, Kaltenbach K. 2012. Infections and obstetric outcomes in opioid-dependent pregnant women maintained on methadone or buprenorphine. Addiction. 107(1):83–90.
  • Hove-Skovsgaard M, Gaardbo JC, Kolte L, Winding K, Seljeflot I, Svardal A, Berge RK, Gerstoft J, Ullum H, Trøseid M, et al. 2017. HIV-infected persons with type 2 diabetes show evidence of endothelial dysfunction and increased inflammation. BMC Infect Dis. 17(1):234.
  • Hser YI, Evans E, Grella C, Ling W, Anglin D. 2015. Long-term course of opioid addiction. Harv Rev Psychiatry. 23(2):76–89.
  • Jenkins WD, Nessa LL, Clark T. 2014. Cross-sectional study of pharyngeal and genital chlamydia and gonorrhoea infections in emergency department patients. Sex Transm Infect. 90(3):246–249.
  • Ji Y, Zhang F, Zhang R, Shen Y, Liu L, Wang J, Yang J, Tang Q, Xun J, Qi T, et al. 2018. Changes in intestinal microbiota in HIV-1-infected subjects following cART initiation: influence of CD4+ T cell count. Emerg Microbes Infect. 7(1):1–4.
  • Kahn JO, Walker BD. 1998. Acute human immunodeficiency virus type 1 infection. N Engl J Med. 339(1):33–39.
  • Kang M, Mischel RA, Bhave S, Komla E, Cho A, Huang C, Dewey WL, Akbarali HI. 2017. The effect of gut microbiome on tolerance to morphine mediated antinociception in mice. Sci Rep. 7(1):42658.
  • Kapadia F, Vlahov D, Donahoe RM, Friedland G. 2005. The role of substance abuse in HIV disease progression: reconciling differences from laboratory and epidemiologic investigations. Clin Infect Dis. 41(7):1027–1034.
  • Kilian M, Chapple ILC, Hannig M, Marsh PD, Meuric V, Pedersen AML, Tonetti MS, Wade WG, Zaura E. 2016. The oral microbiome - an update for oral healthcare professionals. Br Dent J. 221(10):657–666.
  • Kistler JO, Arirachakaran P, Poovorawan Y, Dahlen G, Wade WG. 2015. The oral microbiome in human immunodeficiency virus (HIV)-positive individuals. J Med Microbiol. 64(9):1094–1101.
  • Klatt N R, Cheu R, Birse K, Zevin A S, Perner M, Noël-Romas L, Grobler A, Westmacott G, Xie I Y, Butler J, et al. 2017. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science. 356(6341):938–945.
  • Koay WLA, Siems LV, Persaud D. 2018. The microbiome and HIV persistence: implications for viral remission and cure. Curr Opin HIV AIDS. 13(1):61–68.
  • Lacy P, Stow JL. 2011. Cytokine release from innate immune cells: association with diverse membrane trafficking pathways. Blood. 118(1):9–18.
  • Lamont RJ, Koo H, Hajishengallis G. 2018. The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol. 16(12):745–759.
  • Lam-Ubol A, Rungsiyanont S, Vacharotayangul P, Sappayatosok K, Chankanka O. 2019. Oral manifestations, salivary flow rates and Candida species in Thai HIV-infected patients. J Clin Exp Dent. 11(2):e138–e145.
  • Lansky A, Finlayson T, Johnson C, Holtzman D, Wejnert C, Mitsch A, Gust D, Chen R, Mizuno Y, Crepaz N, et al. 2014. 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. 9(5):e97596.
  • Li SX, Sen S, Schneider JM, Xiong K-N, Nusbacher NM, Moreno-Huizar N, Shaffer M, Armstrong AJS, Severs E, Kuhn K, et al. 2019. Gut microbiota from high-risk men who have sex with men drive immune activation in gnotobiotic mice and in vitro HIV infection. Plos Pathog. 15(4):e1007611.
  • Liang X, Liu R, Chen C, Li JF. 2016. T. Opioid system modulates the immune function: a review. Transl Perioper Pain Med. 1(1):5–13.
  • Lozupone CA, Rhodes ME, Neff CP, Fontenot AP, Campbell TB, Palmer BE. 2014. HIV-induced alteration in gut microbiota: driving factors, consequences, and effects of antiretroviral therapy. Gut Microbes. 5(4):562–570.
  • Marquez M, Fernandez Gutierrez del Alamo C, Giron-Gonzalez JA. 2016. Gut epithelial barrier dysfunction in human immunodeficiency virus-hepatitis C virus coinfected patients: Influence on innate and acquired immunity. World J Gastroenterol. 22(4):1433–1448.
  • Martinez FO, Gordon S. 2014. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6:13.
  • McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. 2010. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol. 10(1):11–23.
  • Meng J, Yu H, Ma J, Wang J, Banerjee S, Charboneau R, Barke RA, Roy S. 2013. Morphine induces bacterial translocation in mice by compromising intestinal barrier function in a TLR-dependent manner. PLoS One. 8(1):e54040.
  • Moyes DL, Saxena D, John MD, Malamud D. 2016. The gut and oral microbiome in HIV disease: a workshop report. Oral Dis. 22:166–170.
  • Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, et al. 2006. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microb. 72(2):1027–1033.
  • Naidoo CC, Nyawo GR, Wu BG, Walzl G, Warren RM, Segal LN, Theron G. 2019. The microbiome and tuberculosis: state of the art, potential applications, and defining the clinical research agenda. Lancet Respir Med. 7:892–906.
  • National Committee for Quality Assurance. Chlamydia screening in women (CHL) [accessed 2019 Sep 10]. https://www.ncqa.org/hedis/measures/chlamydia-screening-in-women/.
  • National Institutes of Health. Collaborating consortium of cohorts producing NIDA opportunities [accessed 2019 Sep 17]. https://www.c3pno.org/C3PNOWebApplication.
  • National Institutes of Health. 2017. Grants awarded to address opioid crisis in rural regions [accessed 2019 Sep 17]. https://www.drugabuse.gov/news-events/news-releases/2017/08/grants-awarded-to-address-opioid-crisis-in-rural-regions.
  • Noguera-Julian M, Guillen Y, Peterson J, et al. 2017. Oral microbiome in HIV-associated periodontitis. Medicine. (12):96.
  • Novak N, Haberstok J, Bieber T, Allam JP. 2008. The immune privilege of the oral mucosa. Trends Mol Med. 14(5):191–198.
  • Nowak RG, Bentzen SM, Ravel J, Crowell TA, Dauda W, Ma B, Liu H, Blattner WA, Baral SD, Charurat ME, et al. 2017. Rectal microbiota among HIV-uninfected, untreated HIV, and treated HIV-infected in Nigeria. AIDS. 31(6):857–862.
  • Nowak P, Troseid M, Avershina E, Barqasho B, Neogi U, Holm K, Hov JR, Noyan K, Vesterbacka J, Svärd J, et al. 2015. Gut microbiota diversity predicts immune status in HIV-1 infection. AIDS. 29(18):2409–2418.
  • Nussbaum G, Ben-Adi S, Genzler T, Sela M, Rosen G. 2009. Involvement of Toll-like receptors 2 and 4 in the innate immune response to Treponema denticola and its outer sheath components. Infect Immunol. 77(9):3939–3947.
  • Ohkusa T, Yoshida T, Sato N, Watanabe S, Tajiri H, Okayasu I. 2009. Commensal bacteria can enter colonic epithelial cells and induce proinflammatory cytokine secretion: a possible pathogenic mechanism of ulcerative colitis. J Med Microbiol. 58(5):535–545.
  • Page GG. 2005. Immunologic effects of opioids in the presence or absence of pain. J Pain Symptom Manag. 29(5):25–31.
  • Pedro MN, Rocha GZ, Guadagnini D, et al. 2018. Insulin resistance in HIV patients: causes and consequences. Front Endocrinol. 9:514.
  • Phillips JF, Bonnie RJ. 2017. Pain management and the opioid epidemic: balancing societal and individual benefits and risks of prescription opioid use. Washington (DC): National Academies of Sciences, Engineering, and Medicine; Health and Medicine Division; Board on Health Sciences Policy; Committee on Pain Management and Regulatory Strategies to Address Prescription Opioid Abuse.
  • Picard M, McEwen BS. 2018. Psychological stress and mitochondria: a systematic review. Psychosom Med. 80(2):141–153.
  • Plein LM, Rittner HL. 2018. Opioids and the immune system - friend or foe. Br J Pharmacol. 175(14):2717–2725.
  • Presti RM, Handley SA, Droit L, Ghannoum M, Jacobson M, Shiboski CH, Webster-Cyriaque J, Brown T, Yin MT, Overton ET, et al. 2018. Alterations in the oral microbiome in HIV-infected participants after antiretroviral therapy administration are influenced by immune status. Aids. 32(10):1279–1287.
  • Rajakaruna GA, Umeda M, Uchida K, et al. 2012. Possible translocation of periodontal pathogens into the lymph nodes draining the oral cavity. J Microbiol. 50(5):827–836.
  • Relman DA. 2015. The human microbiome and the future practice of medicine. JAMA. 314(11):1127–1128.
  • Rouabhia M, Semlali A, Audoy J, Chmielewski W. 2012. Antagonistic effect of Candida albicans and IFN gamma on E-cadherin expression and production by human primary gingival epithelial cells. Cell Immunol. 280(1):61–67.
  • Roy S, Loh HH. 1996. Effects of opioids on the immune system. Neurochem Res. 21(11):1375–1386.
  • Sánchez-Vargas LO, Ortiz-López NG, Villar M, Moragues MD, Aguirre JM, Cashat-Cruz M, Lopez-Ribot JL, Gaitán-Cepeda LA, Quindós G. 2005. Point prevalence, microbiology and antifungal susceptibility patterns of oral Candida isolates colonizing or infecting Mexican HIV/AIDS patients and healthy persons. Rev Iberoam Micol. 22(2):83–92.
  • Scholl L, Seth P, Kariisa M, Wilson N, Baldwin G. 2018. Drug and opioid-involved overdose deaths – United States, 2013-2017. MMWR Morb Mortal Wkly Rep. 67(5152):1419–1427.
  • Segerstrom SC, Miller GE. 2004. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull. 130(4):601–630.
  • Sereti I, Krebs SJ, Phanuphak N, Fletcher JL, Slike B, Pinyakorn S, O'Connell RJ, Rupert A, Chomont N, Valcour V, et al. 2017. Persistent, albeit reduced, chronic inflammation in persons starting antiretroviral therapy in acute HIV infection. CLINID. 64(2):124–131.
  • Serrano-Villar S, Rojo D, Martínez-Martínez M, Deusch S, Vázquez-Castellanos JF, Bargiela R, Sainz T, Vera M, Moreno S, Estrada V, et al. 2016. Gut bacteria metabolism impacts immune recovery in HIV-infected Individuals. EBioMedicine. 8:203–216.
  • Shi N, Li N, Duan XW, Niu HT. 2017. Interaction between the gut microbiome and mucosal immune system. Mil Med Res. 4(1):14.
  • Slavich GM, Irwin MR. 2014. From stress to inflammation and major depressive disorder: a social signal transduction theory of depression. Psychol Bull. 140(3):774–815.
  • Slocum C, Kramer C, Genco CA. 2016. Immune dysregulation mediated by the oral microbiome: potential link to chronic inflammation and atherosclerosis. J Intern Med. 280(1):114–128.
  • Squinto SP, Mondal D, Block AL, Prakash O. 1990. Morphine-induced transactivation of HIV-1 Ltr in human neuroblastoma-cells. Aids Res Hum Retrov. 6(10):1163–1168.
  • Steele AK, Lee EJ, Manuzak JA, Dillon SM, Beckham J, McCarter MD, Santiago ML, Wilson CC. 2014. Microbial exposure alters HIV-1-induced mucosal CD4+ T cell death pathways ex vivo. Retrovirology. 11(1):14.
  • Steptoe A, Hackett RA, Lazzarino AI, Bostock S, La Marca R, Carvalho LA, Hamer M. 2014. Disruption of multisystem responses to stress in type 2 diabetes: investigating the dynamics of allostatic load. Proc Natl Acad Sci USA. 111(44):15693–15698.
  • Subramaniam GA, Stitzer ML, Woody G, Fishman MJ, Kolodner K. 2009. Clinical characteristics of treatment-seeking adolescents with opioid versus cannabis/alcohol use disorders. Drug Alcohol Depend. 99(1-3):141–149.
  • Sultan AS, Kong EF, Rizk AM, Jabra-Rizk MA. 2018. The oral microbiome: a Lesson in coexistence. PLoS Pathog. 14(1):e1006719.
  • Topcuoglu N, Erdem AP, Karacan I, Kulekci G. 2019. Oral microbial dysbiosis in patients with Kostmann syndrome. J Med Microbiol. 68(4):609–615.
  • Tovaglieri A, Sontheimer-Phelps A, Geirnaert A, Prantil-Baun R, Camacho DM, Chou DB, Jalili-Firoozinezhad S, de Wouters T, Kasendra M, Super M, et al. 2019. Species-specific enhancement of enterohemorrhagic E. coli pathogenesis mediated by microbiome metabolites. Microbiome. 7(1):43.
  • Tross S, Hanner J, Hu MC, Pavlicova M, Campbell A, Nunes EV. 2009. Substance use and high risk sexual behaviors among women in psychosocial outpatient and methadone maintenance treatment programs. Am J Drug Alcohol Abuse. 35(5):368–374.
  • Turpin R, Brotman RM, Miller RS, Klebanoff MA, He X, Slopen N. 2019. Perceived stress and incident sexually transmitted infections in a prospective cohort. Ann Epidemiol. 32:20–27.
  • US Department of Health and Human Services. 2019a. HIV treatment: the basics [accessed 2019 Sep 10]. https://aidsinfo.nih.gov/understanding-hiv-aids/fact-sheets/21/51/hiv-treatment–the-basics.
  • US Department of Health and Human Services. 2019b. The stages of HIV infection [accessed 2019 Sep 10]. https://aidsinfo.nih.gov/understanding-hiv-aids/fact-sheets/19/46/the-stages-of-hiv-infection.
  • US Department of Veterans Affairs. 2019. AIDS-defining illnesses [accessed 2019 Sep 10]. https://www.hiv.va.gov/patient/diagnosis/OI-AIDS-defining-illnesses.asp.
  • Velloza J, Heffron R. 2017. The vaginal microbiome and its potential to impact efficacy of HIV pre-exposure prophylaxis for women. Curr HIV/AIDS Rep. 14(5):153–160.
  • Vujkovic-Cvijin I, Dunham RM, Iwai S, et al. 2013. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci Transl Med. 5(193):193ra91.
  • Wang F, Meng J, Zhang L, Johnson T, Chen C, Roy S. 2018. Morphine induces changes in the gut microbiome and metabolome in a morphine dependence model. Sci Rep. 8(1):3596.
  • Wang F, Roy S. 2017. Gut homeostasis, microbial dysbiosis, and opioids. Toxicol Pathol. 45(1):150–156.
  • Whitham HK, Hawes SE, Chu H, Oakes JM, Lifson AR, Kiviat NB, Sow PS, Gottlieb GS, Ba S, Sy MP, et al. 2017. A comparison of the natural history of HPV infection and cervical abnormalities among HIV-positive and HIV-negative women in Senegal, Africa. Cancer Epidemiol Biomarkers Prev. 26(6):886–894.
  • Wood SM, McGeary A, Wilson M, Taylor A, Aumaier B, Petsis D, Campbell K. 2019. Effectiveness of a quality improvement intervention to improve rates of routine Chlamydia trachomatis screening in female adolescents seeking primary preventive care. J Pediatr Adolesc Gynecol. 32(1):32–38.
  • Wu LT, Ling W, Burchett B, Blazer DG, Shostak J, Woody GE. 2010. Gender and racial/ethnic differences in addiction severity, HIV risk, and quality of life among adults in opioid detoxification: results from the National Drug Abuse Treatment Clinical Trials Network. Subst Abuse Rehabil. 2010(1):13–22.
  • Xu J, Boyd CM, Livingston E, Meyer W, Madden JF, Mitchell TG. 1999. Species and genotypic diversities and similarities of pathogenic yeasts colonizing women. J Clin Microbiol. 37(12):3835–3843.
  • Yan AF, Chiu YW, Stoesen CA, Wang MQ. 2007. STD-/HIV-related sexual risk behaviors and substance use among U.S. rural adolescents. J Natl Med Assoc. 99(12):1386–1394.
  • Yu G, Fadrosh D, Ma B, Ravel J, Goedert JJ. 2014. Anal microbiota profiles in HIV-positive and HIV-negative MSM. AIDS. 28(5):753–760.
  • Zaura E, Brandt BW, Prodan A, Teixeira de Mattos MJ, Imangaliyev S, Kool J, Buijs MJ, Jagers F L, Hennequin-Hoenderdos NL, Slot DE, et al. 2017. On the ecosystemic network of saliva in healthy young adults. Isme J. 11(5):1218–1231.
  • Zhang EY, Xiong J, Parker BL, Chen AY, Fields PE, Ma X, Qiu J, Yankee TM. 2011. Depletion and recovery of lymphoid subsets following morphine administration. Br J Pharmacol. 164(7):1829–1844.
  • Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y, et al. 2015. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 21(8):895–905.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.