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JAIDS Journal of Acquired Immune Deficiency Syndromes:
doi: 10.1097/QAI.0b013e318162afcb
Epidemiology and Social Science

Tenofovir DF Plus Lamivudine or Emtricitabine for Nonoccupational Postexposure Prophylaxis (NPEP) in a Boston Community Health Center

Mayer, Kenneth H MD*†; Mimiaga, Matthew J ScD, MPH*‡; Cohen, Daniel MD*; Grasso, Chris MPH*; Bill, Ronn AS*; VanDerwarker, Rodney BA*§; Fisher, Alvan MD∥

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Author Information

From the *Fenway Institute, Fenway Community Health, Boston, MA; †Brown University/the Miriam Hospital, Providence, RI; ‡Harvard University School of Public Health, Boston, MA; §Boston University School of Public Health, Boston, MA; and ∥Gilead Sciences, Foster City, CA.

Received for publication April 25, 2007; accepted November 19, 2007.

Dr. Alvan Fisher is deceased.

Supported by educational grants from Gilead Sciences and the Lifespan/Tufts/Brown Center for AIDS Research, a National Institutes of Health-funded program (#P30 AI42853). The authors did not have any other conflicts of interest.

Correspondence to: Kenneth H. Mayer, MD, The Miriam Hospital, 164 Summit Avenue, Providence, RI 02906 (e-mail: Kenneth_Mayer@Brown.edu).

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Abstract

Background: Nonoccupational postexposure prophylaxis (NPEP) has been used to decrease HIV transmission after high-risk exposures. However, suboptimal adherence in completing the recommended 28-day course has resulted in prophylaxis failures. Fenway Community Health, the largest center caring for HIV-infected and high-risk men who have sex with men (MSM) in New England, began an NPEP program in 1997, initially using zidovudine-based regimens.

Methods: Two phase 4 studies, using tenofovir DF regimens combined with either lamivudine or emtricitabine, were conducted. This paper evaluates the experience of those who used tenofovir-based NPEP regimens, comparing the subjects to historical controls who used zidovudine-containing regimens.

Results: Between May 2004 and March 2005, 44 individuals who presented after high-risk sexual exposure were prescribed tenofovir DF/lamivudine for NPEP. Between March 2005 and March 2006, 68 individuals with 72 high-risk experiences received tenofovir DF/emtricitabine, and were compared to122 historical controls who were prescribed 126 courses of zidovudine plus lamivudine between January 2000 and May 2004. Seventy-two percent of those who took tenofovir DF and emtricitabine, and 87.5% of the participants who took tenofovir DF and lamivudine, for NPEP completed their regimens as prescribed, whereas only 42.1% of those who took zidovudine plus lamivudine did so (P < 0.0001). Participants who took tenofovir DF-containing regimens were more likely to report diarrhea or abdominal discomfort; patients who took zidovudine-containing regimens were more likely to report nausea and vomiting, which was often severe enough to lead to product discontinuation.

Conclusions: Tenofovir DF-containing regimens for NPEP are generally well tolerated with high completion rates. Tolerability and adherence compared favorably to zidovudine-containing regimens used previously. Tenofovir DF-containing regimens should be considered for PEP to enhance adherence and regimen completion.

Multiple primate model studies have established the efficacy of (R)-9-(2-phosphomethoxypropyl) adenine (PMPA) or its derivative, tenofovir DF, in preventing SIV and SHIV transmission after significant exposures.1-5 More recent animal data has suggested that the combination of tenofovir DF and emtricitabine may be particularly effective for antiretroviral chemoprophylaxis.6 However, United States Public Health Service guidelines7,8 for the prevention of HIV transmission after high-risk exposures have generally recommended using zidovudine as one of the basic drugs of the postexposure prophylaxis (PEP) regimen, because of the drug's documented efficacy in preventing mother-to-child transmission,9 and because zidovudine use was associated with an 80% decrease in HIV transmission among HIV-exposed health care workers in a retrospective case-control analysis.10 However, completion rates after exposed individuals used zidovudine-containing regimens have been suboptimal, which could mean that many exposed individuals would not have completed the recommended 4-week course of antiretroviral therapy after a high-risk exposure, based on the animal model data.11 Because of the relative inefficiency of HIV transmission12 and the frequent uncertainty about the HIV-status of the sources of high-risk exposures which was indicated has not been feasible to do randomized controlled trials comparing the efficacy and tolerability of different PEP regimens. Sample size calculations would suggest that many thousands of individuals would have to be enrolled and followed to accurately determine the relative improved efficacy of different regimens.

Tenofovir DF has been approved for more than 5 years as an antiretroviral drug and has been demonstrated to be safe and effective,13 comparing favorably to other reverse transcriptase inhibitors. Tenofovir DF is now one of the most commonly prescribed antiretroviral medications, with close to 1 million people currently using it as part of combination therapy. Thus, it is reasonable to think that tenofovir DF might be useful as part of a regimen for postexposure prophylaxis. There is considerable debate whether 2 versus 3 drugs are optimal for use for PEP, with a decision analysis study suggesting that in most situations, the increased adherence with 2-drug regimens would favor the use of simplified regimens.14 Tenofovir DF coformulated with emtricitabine, given as 1 pill once a day, seemed like an optimal PEP regimen, given the favorable side effect profile and convenient dosing schedule.

Fenway Community Health, the largest center caring for HIV-infected and at-risk MSM in New England, first began conducting studies of nonoccupational postexposure prophylaxis (NPEP) in 1997, initially through a surveillance grant from the Centers for Disease Control and Prevention. Since that time, more than 500 individuals have called a 24-hour hotline that Fenway maintains to handle emergencies, with an average of approximately 1 call per week related to NPEP. In 2004, Fenway began the first of 2 phase 4 studies, supported by Gilead Pharmaceuticals, to assess the safety and tolerability of tenofovir DF, first with lamivudine and then coformulated with emtricitabine, as part of an NPEP regimen. The current paper represents the first comparison of earlier NPEP regimens using zidovudine with those that utilized tenofovir DF.

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METHODS

Study Design

Data from participants who were enrolled in either phase 4 study that evaluated tenofovir DF/lamivudine or tenofovir DF/emtricitabine for NPEP were compared with historical controls, who were NPEP recipients who received zidovudine and lamivudine with or without a third drug (usually a protease inhibitor).

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Study Sample

Participants were HIV-uninfected people at least 18 years of age who presented within 72 hours of a potential sexual exposure to HIV-1, including anal, vaginal, oral, or mucosal exposure to ejaculate, cervicovaginal secretions, or rectal secretions from an HIV-infected partner or high-risk partner of unknown HIV status. Individuals who presented after an exposure in the protocol-defined highest risk category (unprotected anal or vaginal sex with exposure to ejaculate with a partner known to be HIV-infected) were offered a 3-drug regimen that included zidovudine and lamivudine. Individuals whose partner's HIV status was unknown, or who presented after an exposure of lesser risk (eg, unprotected anal or vaginal sex without exposure to ejaculate or receptive oral sex) were offered a 2-drug regimen. All participants enrolled in these studies gave written informed consent allowing for the collection of demographic, behavioral, and clinical information. The protocols and informed consent forms were approved by the independent Institutional Review Board (IRB) of Fenway Community Health.

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Data Collection

After making contact with a specially trained Fenway clinician, who was available 24 hours a day by pager, participants who reported an exposure that qualified for NPEP were asked to come to the clinic. After giving informed consent, participants were interviewed about their exposures and completed a survey that asked them about specific demographic variables, risk behaviors at the time of exposure, and the source of their exposure. After being educated about NPEP, participants received study medication and were given a diary for collecting adverse experiences; this diary was reviewed with study staff at follow-up visits. If participants complained of any residual symptoms, a medical provider performed a focused physical examination. HIV antibody testing was done by enzyme-linked immunosorbent assay at baseline and days 28 and 84, and positive results were confirmed by Western blot. If symptoms suggestive of acute retroviral syndrome were present, HIV RNA testing was also performed to identify early infections.

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Analyses

Descriptive statistics on χ2 significant tests were performed using SPSS (SPSS, Chicago, IL).15

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Results

Between January 2000 and May 2004, 122 individuals presented after 126 potential exposures to HIV and received NPEP consisting of 300 mg of zidovudine and 150 mg of lamivudine given as a fixed-dose tablet taken twice daily. During the same time period, 119 individuals reporting 129 high-risk experiences received zidovudine/lamivudine and a third drug, usually a protease inhibitor. Between May 2004 and March 2005, 68 individuals reporting 72 high-risk exposures received a regimen containing 300 mg of tenofovir DF and 300 mg of lamivudine, each given as 1 pill once a day. Between March 2005 and March 2006, 44 individuals received 44 courses of 300 mg of tenofovir DF and 200 mg of emtricitabine, given as a single fixed-dose tablet once daily for NPEP.

The participants ranged in age between 18 and 61 years, and the median ages ranged from 31.0 to 33.8 years between the groups, with no statistically significant differences in ages between any of the groups (Table 1). The majority of the individuals in the study were white, and there were no significant racial or ethnic differences by regimen. The majority of participants receiving NPEP were homosexual or bisexual males, although a larger percent of female participants were prescribed zidovudine-containing regimens (Table 1). The majority of individuals who presented for NPEP reported anal intercourse, either receptive (65.9%) or insertive (50.1%) (Fig. 1). However, 13.6% reported receptive oral intercourse as their main reason for presenting for NPEP, and 9.1% reported vaginal intercourse as the reason for presenting for NPEP. There were no significant differences in the presenting exposures and the regimens selected for NPEP use, although those who knew that their source was HIV-infected were more likely to be offered and to take 3 drugs (P = 0.0001). Eleven participants who elected to use a tenofovir DF-based regimen indicated that they had sex with an HIV-infected individual. Of these 11 participants, 4 had unprotected anal receptive sex and 1 had anal receptive sex with the condom breaking, but none of them reported exposure to ejaculate. The other 6 participants who reported sex with an HIV-infected individual described either oral exposure or protected anal intercourse.

Table 1
Table 1
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Figure 1
Figure 1
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Almost three quarters of the participants who used tenofovir DF and emtricitabine (72.7%) and 87.5% of those who used tenofovir DF and lamivudine completed their 4-week course of NPEP as prescribed, compared to only 42.1% of those who used zidovudine and lamivudine and 38.8% of those who used zidovudine and lamivudine with a third drug for NPEP (P < 0.0001) (Fig. 2). Of the 6 tenofovir DF/emtricitabine recipients who did not complete the full regimen as prescribed, 3 reported at least 90% adherence to their regimen while they were taking it. Those who used zidovudine-containing regimens were much less likely to follow up at 28 days, with almost 50% of the participants being lost to follow-up during that time.

Figure 2
Figure 2
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Abdominal complaints were the most common side effects among those who took tenofovir DF-containing regimens. Diarrhea was reported by 37.5% of those taking tenofovir/emtricitabine and 31.3% of those taking tenofovir DF and lamivudine, compared to only 9.8% of those who took zidovudine and lamivudine (P < 0.01) (Table 2). Participants who used zidovudine, lamivudine, and a third drug tended to report higher rates of diarrhea (58.8%), probably because the most commonly used third drug was nelfinavir. Of note, 47.5% of the participants who used tenofovir DF/emtricitabine reported abdominal discomfort, pain, or bloating, compared to 20.3% of those who used tenofovir/lamivudine and only 3.3% of those who used zidovudine and lamivudine (P < 0.001). However, abdominal discomfort tended to be mild, resulting in no regimen discontinuations. More than half of the zidovudine/lamivudine group (55.7%) reported nausea or vomiting, compared with only 22.5% of those who used tenofovir DF/emtricitabine and 18.8% of those who used tenofovir and lamivudine (P < 0.01). Those who used tenofovir DF-based regimens were also more likely to report dizziness, lightheadedness, and myalgia or joint pain compared to those who used zidovudine-based regimens (P < 0.01). However, these side effects did not result in product discontinuation and tended to be self-limited within the first few days of tenofovir-based regimen initiation.

Table 2
Table 2
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Complete blood counts and liver and renal function tests were routinely monitored in participants after 4 weeks of medication. Two participants who used tenofovir DF/lamivudine developed grade 1 or 2 asymptomatic bilirubin elevations after 4 weeks of antiretroviral exposure. In both cases, bilirubin levels returned to normal after medication discontinuation. One other participant who took tenofovir DF/lamivudine had a grade 1 bilirubin elevation at his baseline evaluation, which did not change after 4 weeks of medication use. Another participant who took tenofovir DF/lamivudine had a grade 2 increase in transaminases at 4 weeks, but recent ingestion of alcohol may have been implicated, because the results began to normalize within 1 week of alcohol discontinuation. Another participant who used tenofovir DF/lamivudine developed grade 1 hyponatremia, which may have been associated with product-related diarrhea. The only laboratory abnormalities noted among participants who used tenofovir DF/emtricitabine were 1 grade 1 and 1 grade 2 transaminase elevation in 2 of the 44 persons who used this combination.

In the 6 months before baseline enrollment, 72.5% of participants engaged in unprotected anal sex with at least 1 male sex partner (60% unprotected anal insertive and 47.5% unprotected anal receptive). However, during the month of taking NPEP, unprotected anal sex decreased to 17.5% (12.5% unprotected anal insertive and 7.5% unprotected anal receptive) (P < 0.0001). People who presented for NPEP were likely to have used recreational drugs at the time of their exposure, with almost 60% reporting alcohol intake at the time of their risky behavior, 8.6% having used crystal methamphetamine, 11.8% having used inhaled nitrites (poppers), and 11.8% having used sildenafil (Viagra) (Fig. 3). No one in the tenofovir DF-containing NPEP groups became HIV-infected during the study period, whereas 3 individuals who used zidovudine-containing regimens became infected during or shortly after their course of NPEP (not statistically significant).

Figure 3
Figure 3
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DISCUSSION

These findings suggest that a once-daily regimen of tenofovir DF and emtricitabine or lamivudine is safe and well tolerated when used for the prevention of HIV-1 infection after high-risk sexual exposures. Those who took tenofovir DF and either emtricitabine or lamivudine were more likely to complete their prophylaxis compared to those who took zidovudine-containing regimens. None of the tenofovir DF/emtricitabine or tenofovir DF/lamivudine participants stopped or modified their regimen due to adverse events. The most common reason for regimen stopping in the tenofovir DF-containing groups was discovering that the source of the high-risk exposure was not HIV-infected. Conversely, a substantial number of the participants who took zidovudine-containing regimens reported product discontinuation because of adverse events and had much higher rates of loss to follow-up. Although symptoms were common with both tenofovir DF regimens, they tended to be better tolerated than zidovudine-containing regimens, leading to enhanced completion rates.

The data from this study have to be interpreted with some caution, given that participants who took tenofovir DF-containing regimens were enrolled in 2 phase 4 investigative new drug studies, in which there was a higher level of scrutiny and more structured collecting of adverse events than in Fenway's earlier NPEP observational study. Additionally, a subset of the participants who took zidovudine-based NPEP were taking more complex 3-drug regimens, involving a higher pill burden, and were at risk for potential side effects from the third drug, which was most often nelfinavir or lopinavir/ritonavir. This analysis did not address the issue of whether a third drug would have led to greater protection against HIV infection. Because of the relative inefficiency of HIV transmission, a randomized study much larger than the current one would be needed to assess the relative benefit of the addition of the third drug to an NPEP regimen. One Australian study16 reported on the use of tenofovir DF as part of a 3-drug regimen; however, the third drug was stavudine, and the regimen was associated with metabolic and other side effects that made it suboptimal. Future studies may be needed to evaluate whether newer protease inhibitors, entry inhibitors, or integrase inhibitors in a 3-drug PEP regimen with tenofovir DF and emtricitabine or lamivudine may be well tolerated and offer additional protection against HIV infection. Nonnucleoside reverse transcriptase inhibitors are not appropriate for NPEP,7 given the potential hepatotoxicity of nevirapine and the propensity for efavirenz to cause central nervous system side effects that might be poorly tolerated in individuals initiating NPEP.

It is also worth noting that although the majority of participants reported a decrease in risk-taking behavior during the time that they received NPEP, as has been noted elsewhere,17 5% of the individuals who presented for NPEP at Fenway requested it more than once. Thus, it is important that NPEP be administered in conjunction with risk-reduction counseling and other behavioral modification strategies to decrease risk-taking patterns. Although the efficacy of PEP in decreasing the likelihood of HIV transmission has been demonstrated in animal studies1-6 and 1 human cohort study,18 seroconversion events have occurred after NPEP use,18,19 as seen in the Fenway experience. In addition to engaging in risky sexual practices, the majority of individuals in the Fenway series who received NPEP had also been using recreational drugs. Behavioral interventions therefore need to encompass not only the specific sexual behaviors that put people at risk for HIV, but also the social environment and behavioral cofactors that might predispose individuals to engage in recurrent risks. Perhaps the greatest long-term benefit of providing NPEP is the opportunity for an “educable moment,” in which a motivated client receives counseling in a health care setting that he or she might not have otherwise utilized. Combining effective education and risk-reduction interventions will be necessary to maximize the chance of sustained behavior change. Tenofovir DF-containing regimens seem to result in improved adherence compared to zidovudine-containing regimes, but proof of the long-term effectiveness of using antiretroviral therapy to prevent HIV transmission will be evaluated in several studies of tenofovir DF with or without emtricitabine for pre-exposure prophylaxis (PREP). The data from the first completed PREP clinical trial20 and from the present study of PEP suggest that the use of tenofovir DF for chemoprophylaxis seems to be safe and well-tolerated, and its role in HIV prevention merits further investigation.

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ACKNOWLEDGMENTS

The authors would like to recognize the contributions of Roger Cuevas, Christina Jewell, Warren Beattie, Sarit Golub, Fumi Kamaya, Pam McMorrow, Marcy Gelman, Steven Boswell, Jonathan Appelbaum, Jim Rooney, Madeline Miller, Marianne Poblenz, and the entire medical staff at Fenway Community Health. The authors also want to recognize the untimely passing of Dr. Alvan Fisher, who was an invaluable member of the protocol team and a great advocate for people living with, and at risk for, HIV. We greatly acknowledge the assistance of Ms. Lola Wright in the preparation of this manuscript.

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REFERENCES

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3. Van Rompay KK, McChesney MB, Aguirre NL, et al. Two low doses of tenofovir protect newborn macaques against oral simian immunodeficiency virus infections. J Infect Dis. 2001;184:429-438.

4. Van Rompay KK, Miller MD, Marthas ML, et al. Prophylactic and therapeutic benefits of short-term 9-[2-(phosphonomethoxy)propyl] adenine (PMPA) administration to newborn macaques following oral inoculation with simian immunodeficiency virus with reduced susceptibility to PMPA. J Virol. 2000;74:1767-1774.

5. Subbarao S, Otten RA, Ramos A, et al. Chemoprophylaxis with tenofovir disoproxil fumarate provided partial protection against infection with simian human immunodeficiency virus in macaques given multiple virus challenges. J Infect Dis. 2006;194:904-911.

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13. Gallant JE, Staszewski S, Pozniak AL, et al. Efficacy and safety of tenofovir DF vs stavudine in combination therapy in antiretroviral-naive patients: a 3-year randomized trial. JAMA. 2004;292:191-201.

14. Bassett IV, Freedberg KA, Walensky RP. Two drugs or three? Balancing efficacy, toxicity, and resistance in postexposure prophylaxis for occupational exposure to HIV. Clin Infect Dis. 2004;39:395-401.

15. McKillip S. Statistics Explained: An Introductory Guide for Life Scientists. Cambridge: Cambridge University Press; 2006.

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Keywords:

postexposure prophylaxis; tenofovir; zidovudine; HIV transmission; sexual transmission

© 2008 Lippincott Williams & Wilkins, Inc.

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