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Provider Barriers Prevent Recommended Sexually Transmitted Disease Screening of HIV-Infected Men Who Have Sex With Men

Carter, Jarvis W. Jr PhD*; Hart-Cooper, Geoffrey D. BA*; Butler, Mary O. PhD; Workowski, Kimberly A. MD*‡; Hoover, Karen W. MD, MPH*

doi: 10.1097/OLQ.0000000000000067
The Real World of STD Prevention

Background HIV-infected men who have sex with men (MSM) are at increased risk for transmitting and acquiring sexually transmitted diseases (STDs). Guidelines recommend at least annual screening of HIV-infected MSM for syphilis and for chlamydia and gonorrhea at exposed anatomical sites, to protect their health and their sexual partners’ health. Despite these guidelines, STD screening has been suboptimal, with very low nongenital chlamydia and gonorrhea testing rates. Our objective was to better understand barriers encountered by HIV care providers in adhering to STD screening guidelines for HIV-infected MSM.

Methods We conducted 40 individual semistructured interviews with health care providers (physicians, midlevel providers, nurses, and health educators) of HIV-infected MSM at 8 large HIV clinics in 6 US cities. Providers were asked about their STD screening practices and barriers to conducting sexual risk assessments of their patients. Emerging themes were identified by qualitative data analysis.

Results Although most health care providers reported routine syphilis screening, screening for chlamydia and gonorrhea at exposed anatomical sites was less frequent. Obstacles that prevented routine chlamydia and gonorrhea screening included time constraints, difficulty obtaining a sexual history, language and cultural barriers, and patient confidentiality concerns.

Conclusions Providers reported many obstacles to routine chlamydia and gonorrhea screening. Interventions are needed to help to mitigate barriers to STD screening, such as structural and patient-directed health services models that might facilitate increased testing coverage of these important preventive services.

health care providers of HIV-infected men who have sex with men described several barriers to routine sexually transmitted disease screening, including time constraints during a visit, discomfort taking a sexual history, and cultural differences with their patients.

From the *Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, GA; †Department of Anthropology, University of Maryland, College Park, MD; and ‡Emory University School of Medicine, Atlanta, GA

Conflict of interest: None declared.

Correspondence: Karen Hoover, MD, MPH, Centers for Disease Control and Prevention, 1600 Clifton Rd, NE MS E-80, Atlanta, GA 30333. E-mail:

Received for publication September 2, 2013, and accepted October 25, 2013.

Diagnosis, treatment, and prevention of sexually transmitted diseases (STDs) among HIV-infected persons are important for maintaining sexual health and preventing HIV transmission. Compared with other populations, HIV-infected men who have sex with men (MSM) are disproportionately burdened with STDs. In a study in a large US city, MSM had a 140-fold greater risk of HIV and syphilis when compared with men who have sex with women.1 Several studies have also found a high prevalence of chlamydia and gonorrhea at genital and nongenital sites in MSM.2–5 Sexually transmitted disease coinfection increases the risk of HIV transmission,6–9 making it essential for sexually active HIV-infected persons to be screened for STDs.

In the United States, several guidelines have been published that recommend routine STD screening of sexually active HIV-infected persons and MSM.10–12 These guidelines include recommendations to screen all sexually active persons in these populations at least annually for syphilis, urethral chlamydia and gonorrhea if insertive oral or anal sex was reported, rectal chlamydia and gonorrhea if receptive anal sex was reported, and pharyngeal gonorrhea if receptive oral sex was reported. More frequent screening intervals (i.e., 3–6 months) are suggested for MSM at higher risk for acquiring STDs based on their reported sexual risk behaviors, such as those with multiple or anonymous partners.13 These recommendations can only be implemented if a careful and complete sexual risk assessment is conducted at every clinical visit, to identify at-risk patients and anatomical sites of possible exposure to chlamydia and gonorrhea. Availability of sensitive tests, such as nucleic acid amplification tests, for diagnosis of chlamydia and gonorrhea at nongenital sites is also important to support adherence to these guidelines. However, lack of access to these tests can be a barrier to screening. These tests have not been Food and Drug Administration cleared, and many laboratories do not have this capacity to perform self-validated nucleic acid amplification tests.14

Despite evidence that STDs increase transmission and acquisition of HIV and longstanding recommendations for screening of sexually active HIV-infected persons and MSM, STD testing rates have been suboptimal.2,15,16 In this study, we assessed barriers encountered by health care providers that prevent STD screening of HIV-infected MSM.

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To evaluate barriers to STD screening of HIV-infected MSM in clinical care, we conducted interviews of their health care providers at 8 HIV clinics in 6 US cities in 2007 to 2008. A convenience sample of clinics were selected to include clinics that provided health care for at least 200 HIV-infected MSM annually and were located in cities with high historic rates of syphilis based on national surveillance data.17 We included a public clinic, clinics that were part of academic centers, private clinics, and a clinic that was part of a health care maintenance organization. Providers at these clinics (n = 118) who completed a quantitative survey of their knowledge, attitudes, and practices regarding STD care for HIV-infected MSM were asked if they would be willing to participate in an interview. Characteristics of these providers were estimated, including age, sex, race and ethnicity, and sexual identity.18 All 118 invited providers consented to be interviewed, and among these 40 were randomly selected to participate in the qualitative study.

We conducted 40 individual, semistructured interviews with the health care providers, including physicians, physician assistants, nurse practitioners, registered nurses, medical assistants, HIV counselors, and disease intervention specialists. Interview domains included their sexual risk assessment practices, STD screening practices, and barriers to screening. Examples of open-ended questions we asked providers included the following: (1) Tell me how you think the clinician’s comfort or skill in asking about sexual and injection-related behaviors might influence how revealing patients are? (2) How are asymptomatic patients screened for infections such as syphilis, gonorrhea, chlamydia, or hepatitis? (3) What do you believe are the most significant barriers to providing STD risk reduction counseling? (4) How might cultural and language differences between providers and patients influence how (HIV and STD prevention) services are accepted or rejected? and (5) How could patients’ perceptions of confidentiality in the clinic affect their care seeking behaviors or what they say to the provider?

Interviews were conducted by 4 facilitators, with either a health care provider (1) interviewed separately by 2 facilitators or (2) interviewed by 2 facilitators simultaneously. The interviews lasted 60 to 90 minutes, were audiorecorded, and transcribed verbatim by a transcription service. All transcribed interviews were formatted and uploaded into files for analyses using NVivo 8 (QSR International Pty Ltd, Doncaster, Victoria, Australia) qualitative data management software to organize interview content and to determine emerging themes. Data were initially coded using a constant comparison method,19,20 to generate general categories. Subsequently, subcategories were generated to identify emerging phenomena. Because sequential interviews were coded, comparison between the identified phenomena was kept constant. Using these codes, relationships were identified within and between codes, which were then merged into categories to develop an explanation of the phenomena. Two researchers reviewed transcripts to identify general categories to ensure congruency in assigning text to code. After this process, one researcher was responsible for generating subcategories within broader categories to identify the emerging themes for this study. The study protocol was reviewed and approved by institutional review boards at the Centers for Disease Control and Prevention and participating clinics, and it was determined that the activity was not human subjects research.

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Providers described the ease of routine syphilis testing and the challenges of routine chlamydia and gonorrhea testing. Our analyses also identified various themes associated with barriers to STD testing, including time constraints and competing priorities, challenges conducting a sexual history, cultural and language barriers, and patient privacy and confidentiality concerns. Table 1 provides detailed demographic information on the characteristics of 118 health care providers, from which 40 were randomly selected for this study. Table 2 provides a summary of selected quotes from providers for each emerging theme identified.





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Ease of Routine Syphilis Screening

Our analysis found that most health care providers encountered few barriers to routine screening of HIV-infected MSM for syphilis. Providers described the ease and feasibility of screening for syphilis with testing of sera that were collected for monitoring HIV, with inclusion of syphilis screening as part of the clinic’s standard operating procedures. One provider in San Francisco remarked, “We screen practically every time that we draw blood, so we screen them for syphilis.” In addition to the ease of collection, providers found that increases in the prevalence of syphilis in the community served as a strong motivator to ensure screening to control outbreaks.

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Challenges of Routine Chlamydia and Gonorrhea Testing

Most providers noted that annual screening of patients for chlamydia and gonorrhea was suboptimal. One clinician in Los Angeles indicated that the clinic’s testing rates for urethral chlamydia and gonorrhea were “less than 60%.” Routine screening at nongenital sites was even less frequent with many barriers encountered (see Table 2). Some providers said that reviewing their clinic’s testing data increased awareness of the high prevalence of chlamydia and gonorrhea at nongenital sites and prompted interventions to increase adherence to recommendations such as electronic medical record reminders.

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Time Constraints and Competing Priorities

The most common barrier to STD screening was time, with providers describing the challenge of balancing the many pertinent clinical priorities during an encounter of a limited period. Providers said that office visits for medically complex HIV-infected patients were focused on management of complicated medication regimens. Providers described more urgent medical issues diverting their attention, such as assessment for other opportunistic infections besides STDs.

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Challenges Conducting a Sexual History

We observed differences in the comfort level among providers in obtaining a sexual history from a patient. HIV counselors and health educators described greater comfort taking a sexual history than clinical providers. According to an HIV counselor in New York, clinical providers were not as skillful in taking a sexual history because they had a “different type of training.” This counselor felt that the ability to communicate effectively on these sensitive issues was challenging for clinicians, and even after directed training, clinicians can “still come across as insincere.” Providers echoed this barrier, with one nurse from San Francisco succinctly stating that “all providers—let’s face it—are not trained equally or [are] equally comfortable with sensitive topics.” One clinician from New York said that physicians were “not comfortable talking to patients much about anything except really about their HIV.” An HIV counselor from New York said that it is easier for patients to colloquially discuss sexual behavior with counselors because of the less formal environment when compared with encounters with providers. He noted that medical providers felt uncomfortable asking about insertive and receptive sexual behaviors, which is important in a sexual history to determine sites of possible exposure.

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Cultural and Language Barriers

During our analysis of the interviews, factors such as race and ethnicity, provider’s sexual identity, and provider language skills emerged as barriers to STD screening. Some providers encountered difficulty when working with patients of different cultural backgrounds. Providers perceived that among different racial and ethnic populations, there are varying degrees of stigma associated with HIV infection and same-sex behavior. Providers indicated that these perceptions exacerbated discomfort discussing sensitive issues with their patients. The role of the provider’s sexual identity was also cited as a barrier, with several providers believing that patients would prefer nonheterosexual providers. A physician assistant in New York said, “As far as the gay men are concerned, well, there’s the gayness. Some of them only want to be seen by gay male providers.” A heterosexual physician assistant in Miami felt that patients “might be less inclined to tell all the things they do with their friends because they’re afraid of what [I] might think.” Providers also cited language barriers in conducting a sexual history, describing the requirement for a translator to communicate with patients as an added complexity to conducting a risk assessment.

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Patient Privacy and Confidentiality Concerns

Providers indicated that patients were concerned about the confidentiality of medical records and about any sensitive information that they disclose to providers such as sexual behaviors. Providers perceived that these patient concerns hinder an accurate sexual history. According to a medical assistant in Chicago, “some people just don’t trust the system, so they don’t tell us and we won’t get an accurate history.” An HIV counselor in New York noted that some patients felt a detailed sexual history was “an intrusion into their privacy.” Providers also expressed concern that patients feared being recognized at a clinic in their community and that patients might forego receiving more convenient care because of the clinic’s location in their neighborhood.

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We found that most health care providers of HIV-infected MSM adhered to recommendations for syphilis screening but encountered several barriers that resulted in only suboptimal chlamydia and gonorrhea screening. A study that assessed syphilis, chlamydia, and gonorrhea screening rates by reviewing medical records supports these findings.2 Providers attributed their high syphilis screening rates to awareness of the high rates of infection in the community. They also described the ease of ordering a blood draw for a syphilis test that can be added to orders for routine, periodic monitoring of CD4 cell counts and HIV viral loads. Unlike screening for chlamydia and gonorrhea, which requires a detailed sexual history, syphilis screening does not depend on the quality of a provider’s history-taking skills or the patient’s trust and willingness to discuss sexual behaviors. Similar to studies that have found that structural interventions such as placement of a swab alongside Papanicolaou test kits increased chlamydia screening,21 the providers in our study reported that structural interventions for syphilis screening were very effective, such as standing orders for automated syphilis testing with blood draws.

Providers reported several barriers to chlamydia and gonorrhea screening, in addition to the need for a detailed sexual history to identify anatomical sites of exposure to be tested. Providers described time constraints and many competing priorities during a brief clinical encounter. One study found that clinicians do not have enough time to adhere to all US Preventative Services Task Force screening recommendations because completing all recommended services is not feasible in a typically brief clinical encounter.22 For a busy clinician, STD risk assessment is only one of many important clinical issues that should be addressed during the encounter. Because taking a sexual history seems to be a frequent barrier to chlamydia and gonorrhea testing, universal, opt-out rectal or pharyngeal screening of all MSM at clinical encounters might increase testing coverage. It is essential that MSM be tested for chlamydia and gonorrhea at nongenital sites, with one study finding that screening at the urethra alone would miss 84% of infections.23

Several providers in our study perceived language and cultural barriers that they believed limit their patients’ willingness to discuss sexual behaviors and described varying comfort levels with taking a comprehensive and culturally sensitive sexual history. Among providers, health counselors reported greater comfort with STD risk assessment. A discussion of sexual behavior requires a sensitive conversation with open, nuanced communication, and health counselors have received training to develop these skills as part of the core curriculum in their education. Diversity training can help clinicians modify their history-taking skills to conduct effective, culturally appropriate sexual risk assessments.

Accurate risk assessment, facilitated by diversity training and the implementation of culturally appropriate sexual history tools such as “A Clinician’s Guide to Sexual History Taking” and Ask, Screen, and Intervene,24,25 can guide a comprehensive sexual history to help providers identify patients who require STD screening and behavioral interventions. Such tools encourage appropriate STD screening while easing the provider’s burden by helping them to overcome potential barriers to effective communication about these sensitive topics. As providers cultivate relationships with patients, they should also be aware that their sexual identity as perceived by patients can be a barrier to open communication. Interventions could help providers to develop skills necessary for establishing a nonjudgmental office environment that fosters trust and effective communication with their patients, while providing reassurance of confidentiality if they share their sexual behavior history.

Our study findings increase understanding of barriers that must be overcome to increase screening. Novel health services models might also help to increase chlamydia and gonorrhea screening, such as patient-driven models. Self-risk assessment, along with self-collected specimens for gonorrhea and chlamydia testing at nongenital anatomical sites of exposure, can be effective in increasing screening rates.26,27 Such health services models promote screening but without adding an additional task for a busy clinician to perform, and overcome several of the barriers we identified such as the lack of time, skill, and comfort needed to conduct a risk assessment.

Few qualitative studies have assessed barriers to STD screening, but one small study found that providers reported not conducting a sexual behavior assessment because they were uncomfortable, lacked understanding of patients’ cultural differences, and encountered time constraints in gathering the necessary information to evaluate patients’ risk.28 Our study included a geographically diverse sample of multidisciplinary providers, with an evaluation of provider barriers that is more reflective of clinics throughout the United States. Our study has some limitations. The convenience sample of clinics included resulted in a sample of health care providers in 8 urban HIV clinics and might not be representative of all urban clinics or rural ones. Although the clinics we selected were geographically dispersed, there might have been different barriers in clinics not included in our study. The urban clinics in our study provided health care for a high volume of HIV-infected MSM, possibly restricting the generalizability of our observations to clinics that care for fewer numbers of patients in this population. Our random sample of providers in the 8 clinics might not have been representative of all providers in these clinics.

Understanding barriers to STD screening is essential to guide the development of tools and interventions to increase testing rates. Promoting culturally sensitive risk assessment skills and tools and developing and piloting structural models that promote self-assessment and screening without placing burden on busy clinicians have the potential to overcome the barriers we identified. Based on prior studies and recommendations, optimal screening for STDs among HIV-infected MSM can lead to increased diagnosis and treatment of STDs, an important intervention to reduce HIV transmission.10–12

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