RESEARCH AND PRACTICE
Routine HIV Testing in Indiana Community Health Centers Beth E. Meyerson, MDiv, PhD, Shalini M. Navale, MPH, PhD(c), Anthony Gillespie, and Anita Ohmit, MPH
Community health centers (CHCs) have been important providers of primary and preventive care since the late 1960s for communities with uninsured or underinsured patients.1 The importance of CHCs is heightened for the millions who remain without insurance coverage because of the varied implementation of the Affordable Care Act, because almost half of US states have opted not to expand Medicaid,2 and because the federal government has delayed the implementation of the employer health insurance mandate until 2015.3 It has been argued that CHCs are uniquely positioned to provide community-based, nonstigmatized access to specialty services, such as HIV testing.1,4 Recent HIV testing recommendations by the US Preventive Services Task Force call for routine testing among adolescents and adults in clinical settings,5 echoing the 2006 Centers for Disease Control and Prevention recommendation.6 Such recommendations imply that testing services likely will be reimbursed—an important point for resource-constrained environments and a financial incentive to improve practitioner compliance around HIV testing. CHCs themselves have been the target of additional efforts to increase HIV testing to help fulfill the National HIV/AIDS Strategy to reduce new HIV infections.7---9 Understanding HIV testing in CHCs is important because it is now known that 20% of those living with HIV in the United States do not know their status,10 and 40% of those who learn it do so within a year of an AIDS diagnosis.11,12 Delayed HIV testing is particularly acute in rural populations,13,14 because barriers to testing such as stigma and fear of anonymity loss are more pronounced.15,16 Publicly funded HIV testing, while helpful to some communities, may not be sufficient to improve early HIV testing in all communities. A recent evaluation of HIV testing sites in a state with moderate HIV incidence found several important problems related to access: 20% of test attempts failed to result in a test, 48% of sites had reported confidentiality issues, and a little fewer than half of the sites received
Objectives. We assessed routine HIV testing in Indiana community health centers (CHCs). Methods. CHC medical directors reported HIV services, testing behaviors, barriers, and health center characteristics via survey from April to May 2013. Standard of care testing was measured by the extent to which CHCs complied with national guidelines for routine HIV testing in clinical settings. Results. Most (85.7%) CHCs reported HIV testing, primarily at patient request or if the patient was symptomatic. Routine HIV testing was provided for pregnant women by 60.7% of CHCs. Only 10.7% provided routine testing for adolescents to adults up to age 65 years. Routine testing was reported by 14.3% for gay and bisexual men, although 46.4% of CHCs reported asking patients about sexual orientation. Linkage to care services for HIV-positive patients, counseling for HIV treatment adherence, and partner testing generally was not provided. Conclusions. Most CHCs reported HIV testing, but such testing did not reflect the standard of care, because it depended on patient request or symptoms. One approach in future studies may be to allow respondents to compare current testing with standard of care and then reflect on barriers to and facilitators of adoption and implementation of routine HIV testing. (Am J Public Health. 2015;105:91–95. doi:10. 2105/AJPH.2014.302203)
a “no return” rating by test visitors (meaning that those evaluating the test site would not return for an HIV test if they needed one in the future).17 Given the delays in testing and the troubles experienced in some publicly funded testing sites, a tremendous need exists to understand whether and how routine HIV testing is offered in other public health settings such as CHCs. Despite the emerging federal interest in HIV testing in CHCs and the public health importance of understanding testing in these environments, not much is known about the level of services in CHCs, particularly in areas with moderate HIV incidence and in Midwestern settings. Studies evaluating routine HIV testing in CHCs have focused on patient acceptance of testing18,19 or on provider testing behavior.20---23 Implementation studies provided participating CHCs with training and HIV rapid test kits to facilitate participation and success. The most recent studies occurred in urban areas: one among patients in a Houston, Texas, CHC serving a predominantly Hispanic population21 and the other, the largest of extant studies, comparing the views of clinicians in 31 Boston, Massachusetts, health centers.23
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Notably, the Boston CHCs were rated as high performing in a recent national review of performance and may not reflect the performance of CHCs in other communities.24 Studies of HIV testing in CHCs have not yet included moderate HIV incidence states or focused on rural and urban areas. These communities tend to have lower levels of HIV prevention and public health investment, which heightens the need for strong HIV testing services in CHCs. The objective of this study was to identify the extent to which CHCs in Indiana implement routine HIV testing. Indiana is a Midwestern, moderate HIV incidence state with low public health investment. In 2014, Indiana ranked 50th in per capita funding from the Health Resources and Services Administration (federal funding source for HIV treatment and also for CHCs) and from the Centers for Disease Control and Prevention (the primary federal funding source for HIV prevention). Indiana ranked 37th for state per capita public health investment.25
METHODS The study applied community participatory research principles. The research goal, methods,
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and analysis plan were developed by a community-based research team composed of the Indiana University School of Public Health-Bloomington; the Rural Center for AIDS/STD Prevention; the Indiana Minority Health Coalition; minority health coalitions from Lake, Marion, St. Joseph, and Vigo counties; the American Indian Center of Indiana; the Indiana HIV Prevention Community Planning Group; the Midwest AIDS Training and Education Center; the Indiana Primary Health Care Association; and the Indiana State Department of Health Division of HIV/STD and Viral Hepatitis and the Office of Primary Care. Clarification of CHC categorization and inclusion was determined in conference with the Office of Primary Care of the Indiana State Department of Health and the Indiana Primary Health Care Association. We measured HIV testing in CHCs by a 42-question online survey of Indiana CHC medical directors from April to May 2013. Participants were recruited by e-mail invitation to clinic leadership from the state of Indiana’s Office of Primary Care. This office sent 2 reminder e-mails during the study period to encourage survey completion, and the final e-mail offered a telephone interview by a research staff member. The survey gathered both quantitative and qualitative data about current HIV services, testing expectations, clinician behaviors and beliefs, barriers to and facilitators of services, and characteristics of the health center. We measured clinic expectations for HIV testing for adults aged 65 years or younger, pregnant women, and gay or bisexual men. The phrase “testing expectations” was used in the survey as a proxy for clinic policy guiding HIV testing because it was thought that many CHCs would not have a written policy about HIV testing but might operate with some type of expressed expectation. We measured standard of care testing by the extent to which CHCs complied with current 2012 US Preventive Services Task Force guidelines for routine HIV testing in clinical settings for adolescents to adults aged 65 years and for pregnant women.8 Although quite recent, this guidance essentially reflected the 2006 Centers for Disease Control and Prevention recommendations for routine testing in clinical settings.9 We described quantitative data and then evaluated for associations with key
infrastructure and demographic indicators such as Federally Qualified Health Center designation, Rural Health Center designation, Ryan White Comprehensive AIDS Resources Emergency Act funding, clinic categorization (multisite, hospital, county, unaffiliated), and census designation (rural or urban). We gathered qualitative data to provide explanation to quantitative responses. These were coded textually for emerging themes, verified by a second and independent coder, and quantitated to assist statistical comparison with reported testing behaviors and clinic indicators.
RESULTS Indiana has a total of 40 CHCs operating 134 clinic sites. CHCs were classified into 4 types: (1) multisite CHCs (of which there are 18 CHCs with 93 sites), (2) county government---associated networks (of which there are 3 CHCs with 11 sites), (3) hospital-associated networks (of which there are 10 CHCs with 22 sites), and (4) unaffiliated CHCs (of which there are 9 CHCs or clinics). Completed surveys were returned by 28 CHCs for a response rate of 70%, with representation from each classification: multisite (61.1%), county government (100%), hospital (63.6%), and unaffiliated (77.8%; Table 1). Of the CHCs in the sample, 28.6% had a Federally Qualified Health Center designation, and 32.1% had a Rural Health Center designation. More than half of the CHCs (67.9%) primarily served metropolitan areas, 14.3% served micropolitan areas, and 17.9% served rural communities.
HIV Testing Expectations and Practice Most CHCs reported HIV testing (85.7%), but routine HIV testing was not the norm
among CHCs in this sample. As noted in Table 2, HIV testing at standard of care was reported for pregnant women most often (60.7%). Only 10.7% of CHCs tested at standard of care for adolescents to adults aged 65 years, and 14.3% tested at standard of care for gay or bisexual men. CHCs in metropolitan areas were more likely to report standard of care testing for pregnant women and the only CHCs to report standard of care testing for gay or bisexual men. CHCs that provided standard of care testing for pregnant women did not necessarily report standard of care testing for gay and bisexual men or for other adults aged 65 years or younger. Participants were asked to identify the clinic expectations for HIV testing—when, under what conditions, and for what populations testing would be offered. Three populations were presented to respondents, with several options related to the conditions for testing (only at patient request, only if patient is symptomatic, patient circumstance such as trimester timing) and related to timing (e.g., annual, every 3 years). Table 3 reports clinic expectations for HIV testing for each of 3 populations: adolescents to adults aged 65 years or younger, pregnant women, and gay or bisexual men. As reported, HIV testing was generally offered only at patient request or when patients were symptomatic. This was reported for more than half of the CHCs for adults aged 65 years or younger and for about 40% of CHCs for gay and bisexual male patients. More than half (57.1%) reported offering testing to pregnant women at first trimester. Notably, several CHCs reported lack of knowledge about HIV testing expectations and practices for gay or bisexual men (35.7%) and for pregnant women (28.6%).
TABLE 1—Indiana Community Health Center (CHC) Characteristics (n = 28): April–May 2013 CHC Type
Metropolitan
Rural or Micropolitan b
Sample, No. (% of Classification) 3 (100)
County affiliated
1
2
Hospital affiliated
3
4b
6 (63.6)
Multisite
9a
2b
11 (61.1)
Unaffiliated
6a
1
10 (77.8)
Total
19
9
28
a
Federally Qualified Health Center designations for 5 multisite CHCs and 3 unaffiliated CHCs. Rural Health Center designations for 2 county government–affiliated CHCs, 5 hospital-affiliated CHCs, and 2 multisite CHCs.
b
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TABLE 2—Standard of Care HIV Testing by Population and Selected Community Health Center Characteristics (n = 28): Indiana, April–May 2013 Adults Aged £ 65 Years, No. (% Category)
Characteristic
Pregnant Women, No. (% Category)
Gay or Bisexual Men, No. (% Category)
Results, Partner Services, and Linkage to Care
Federally qualified health center Yes (8 clinics)
1 (12.5)
6 (75.0)
2 (25.0)
No (20 clinics) Rural Health Center
2 (10.0)
11 (55.0)
2 (10.0)
Yes (9 clinics)
1 (11.1)
4 (44.4)
...
No (19 clinics)
2 (10.5)
13 (68.4)
4 (21.0)
Yes (19 clinics)
2 (10.5)
13 (68.4)
4 (21.1)
No (9 clinics)
1 (11.1)
4 (44.4)
...
1 (33.3) ...
2 (66.7) 2 (28.6)
... ...
Most CHCs (90.9%) reported encouraging patients to refer partners for testing and treatment, but 89.3% indicated that they do not provide on-site counseling, risk reduction, or testing for partners; however, 50.0% reported that they would do so if partners were patients of the health center. HIV treatment generally was not provided by CHCs, because 72.7% of the participants reported referring patients elsewhere for HIV treatment “all of the time.” Participants did not indicate how they evaluated or ensured patient access to HIV treatment or adherence to antiretroviral medications once patients were referred elsewhere for treatment.
Metro
Classification County (3 clinics) Hospital (7 clinics) Multisite (11 clinics)
1 (9.1)
8 (72.7)
3 (27.3)
Unaffiliated clinic (7 clinics)
2 (28.6)
4 (57.1)
1 (14.3)
Total at standard of care (28 clinics)
3 (10.7)
17 (60.7)
4 (14.3)
This is significant because 46.4% of CHCs reported asking patients about sexual orientation. Reported testing expectations and clinic classification, Federally Qualified Health Center or Rural Health Center status, and census designation were not found to be associated at the P < .05 level. When asked their perception of how well staff followed CHC HIV testing expectations, 37.9% indicated that clinicians followed expectations very well, 51.8% indicated well or most of the time, and 10.3% reported that compliance varied by clinician. Fewer than half
(46.7%) of the participants indicated that HIV screening recommendations were the most difficult to follow as compared with hepatitis C, sexually transmitted diseases (gonorrhea, chlamydia, syphilis), and cervical cancer. Most participants (73%) believed that no barriers to HIV testing existed for their CHCs, yet 20.9% reported barriers to HIV testing. Community discomfort with HIV, lack of HIV treatment options in the community, and cost including lack of reimbursement for testing were most commonly cited. Published protocols, guidelines, and policies facilitated staff adherence to
TABLE 3—Reported Expectations for HIV Testing in Indiana Community Health Centers by Population (n = 28): April–May 2013 Expectation
Adults Aged £ 65 Years, No. Clinics (%)
Gay or Bisexual Men, No. Clinics (%)
Pregnant Women, No. Clinics (%)
Only at patient request
17 (60.7)
12 (42.9)
2 (7.1)
Only if patient is symptomatic
14 (50.0)
11 (39.3)
2 (7.1)
3 (10.7)
4 (14.3)
...
... ...
... ...
... ...
Annual Every 3 y Every 5 y First trimester
...
...
16 (57.1)
Second trimester
...
...
1 (3.6)
Third trimester
...
...
2 (7.1)
Delivery
...
...
1 (3.6)
3 (10.7)
10 (35.7)
8 (28.6)
Do not know
clinic screening expectations for 50% of CHCs, and 15.4% of the respondents perceived that management guidance or clinician knowledge of protocols facilitated testing.
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Training Offered to or Expected of and Obtained by Clinic Staff CHCs were asked to indicate whether any of 4 nationally emphasized training topics were available and required of clinicians in 201226: offering and providing HIV testing, HIV screening guidelines, delivering prevention counseling to HIV-positive patients to reduce transmission, and retaining HIV-positive patients in care. A smaller sample of CHCs (n = 22) responded to related questions. More than half (60.0%, 12) of the CHCs reported that training about HIV screening guidelines and training focused on offering and providing HIV testing were available to clinicians in 2012, but neither was required of clinicians. Training about the HIV screening guidelines was available and required at only 3 (13.6%) CHCs, and only 2 (9.1%) required training about offering and providing HIV testing in 2012. Those CHCs where training was not available for one module tended also to report that training was not available for the other modules (Fisher P = .008). Associations were not significant between available or required training and clinic characteristics such as Federally Qualified Health Center status, metropolitan or nonmetropolitan, and clinic affiliation. However, associations with testing below standard of care for adults
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aged 65 years or younger and the lack of available training about HIV prevention counseling and retention of patients in care was significant at P £ .05. A significant association also was found between not testing at standard of care for gay and bisexual men and having training about HIV screening guidelines made available but not requiring it of clinicians in 2012.
DISCUSSION This study was a baseline study of CHC provision of routine HIV testing in a Midwestern, moderate HIV incidence state with low levels of public health investment. Most CHCs reported providing HIV testing, but such testing did not reflect the standard of care, because it depended on patient request or symptoms. Even though most CHCs reported no barriers to HIV testing, several indicated that the HIV guidelines were most difficult to follow. At the same time, a bit of confusion emerged, because respondents reported that most clinicians followed the guidelines well and that such guidelines were the basis of testing practice. Additional evaluation will help to make sense of this particular observation. It may be entirely possible that expectations for HIV testing (patient request or symptoms) were seen as appropriate because of the funding environment: public health funding for HIV testing is lacking in Indiana CHCs. Therefore, barriers to this reported testing approach under the current funding scenario were not perceived. This theory is further reinforced by the observation that resource constraints were not identified as barriers to HIV testing by most CHCs. Still, offering testing only at patient request or if symptomatic reflects a critical obliviousness to potential testing barriers faced by patients who are in need of HIV testing. One approach in future studies may be to allow respondents to compare their current testing with standard of care and then reflect on barriers to and facilitators of adoption and implementation of routine HIV testing to standard of care. As CHCs evolve more fully into their role as medical homes for all patients, including those with HIV, they will need to focus on services such as retention of patients in HIV medical care and especially antiretroviral treatment
adherence. This is important in Indiana because according to a more rigorous definition of linkage to care, it is estimated that 45% of people living with HIV in Indiana are not linked with medical care.27 Respondents in this study could not articulate standard of care for managing HIV-positive patients beyond referral to specialty care outside the CHC. Partner counseling regarding testing, treatment retention practices, and access to additional HIVrelated services will be necessary components of medical homes for patients who have HIV. CHCs appeared to function well from a disease-reporting standpoint, because most reported diagnoses to the health department for these communicable conditions. Most CHCs also reported the encouragement of partners to obtain testing; however, this encouragement was likely no more than a testing referral, given the reported lack of partner services unless the partner was a patient of the CHC. As such, the functioning of CHCs in the public health system of care was unclear when it came to linking sexual partners of patients testing positive for HIV to testing and eventual treatment. Greater opportunities between local public health departments, HIV prevention organizations, and CHCs exist to coordinate partner services and to ensure a well-coordinated HIV prevention and treatment system of care. This study was an important baseline assessment of current HIV testing practices in a Midwestern state’s CHCs because it yielded a critical clinical practice deficit for public health program and policy focus. As CHCs begin to realize their role as medical homes in an era of routine HIV testing and linkage to care, additional resources and evaluation will be needed to ensure standard of care and therefore greater access to HIV testing. Future studies should examine CHC testing practices across several states with a focus on characteristics such as public health investment in HIV prevention, CHCs, and public health generally. j
SPH 116, Bloomington, IN 47405 (e-mail: bmeyerso@ indiana.edu). Reprints can be ordered at http://www.ajph. org by clicking the “Reprints” link. This article was accepted July 1, 2014.
About the Authors
9. Health Resources and Services Administration. Implementing Our Strategic Plan: Health Resources and Services Administration. [monograph]. 2011. Available at: http://www.hrsa.gov/about/strategicplanimplementation. pdf. Accessed July 8, 2013.
Beth E. Meyerson and Shalini M. Navale are with Indiana University School of Public Health-Bloomington. Anthony Gillespie and Anita Ohmit are with Indiana Minority Health Coalition, Inc, Indianapolis. Correspondence should be sent to Beth Meyerson, MDiv, PhD, Indiana University School of Public HealthBloomington Applied Health Science, 1025 E 7th St, Room
94 | Research and Practice | Peer Reviewed | Meyerson et al.
Contributors B. E. Meyerson, A. Gillespie, and A. Ohmit conceptualized the study. B. E. Meyerson directed all aspects of the study and the article preparation. S. M. Navale assisted in data collection, participated in the data analysis, and edited article iterations. A. Gillespie and A. Ohmit interpreted the study results and participated in editing the article.
Acknowledgments The study was funded by the Indiana Minority Health Initiative.
Human Participant Protection This study was deemed exempt by the Indiana University institutional review board.
References 1. Hawkins D, Groves D. The future role of community health centers in a changing health care landscape. J Ambul Care Manage. 2011;34(1):90---99. 2. The Advisory Board Company. Where each state stands on ACA’s Medicaid expansion: a roundup of what each state’s leadership has said about their Medicaid plans. June 14, 2013. Available at: http://www.advisory. com/Daily-Briefing/2012/11/09/MedicaidMap. Accessed May 31, 2013. 3. Jarrett V. We’re listening to businesses about the health care law [The White House Blog]. July 2, 2013. Available at: http://www.whitehouse.gov/blog/2013/ 07/02/we-re-listening-businesses-about-health-care-law. Accessed July 8, 2013. 4. Shin P, Markus A, Rosenbaum S, Sharac J. Adoption of health center performance measures and national benchmarks. J Ambul Care Manage. 2008;31(1):69---75. 5. US Preventive Services Task Force. Screening for HIV. April 2013. Available at: http://www. uspreventiveservicestaskforce.org/uspstf13/hiv/ hivfinalrs.htm. Accessed May 31, 2013. 6. Branson BM, Handsfield HH, Lampe MA, et al. Revised recommendations for HIV testing of adults, adolescents, and pregnant women in health-care settings. MMWR Recomm Rep. 2006;55(RR-14);1---17. 7. The White House Office of National AIDS Policy. National HIV/AIDS Strategy for the United States. July 2010. Available at: http://www.whitehouse.gov/sites/ default/files/uploads/NHAS.pdf. Accessed July 8, 2013. 8. National Association of Community Health Centers. A Model to Integrate Routine HIV Screening Services in Federally Qualified Health Centers [monograph]. Revised December 20, 2012. Available at: http://www.nachc. com/client//Clinical_HIV_Model_Implementing_ Routine_HIV_Screening_in_FQHCs%20_December% 2020122.docx. Accessed July 8, 2013.
10. Chen M, Rhodes PH, Hall IH, Kilmarx PH, Branson BM, Valleroy LA. Prevalence of undiagnosed HIV infection among persons aged ‡ 13 years—National HIV
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Surveillance System, United States, 2005-2008. MMWR Morb Mortal Wkly Rep. 2012;61(suppl):57---64.
at: http://healthyamericans.org/report/114. Accessed October 14, 2014.
11. US Centers for Disease Control and Prevention. Late HIV testing—34 states, 1996-2005. MMWR Morb Mortal Wkly Rep. 2009;58(24):661---665.
26. Health Resources and Services Administration. HIV/AIDS care and treatment in health centers. June 16, 2011. Program Assistance Letter 2011-06. Available at: http://bphc.hrsa.gov/policiesregulations/policies/pdfs/ pal201106hiv/aids.pdf. Accessed August 21, 2013.
12. Gardner EM, McLees MP, Steiner JF, del Rio C, Burman WJ. The spectrum of engagement in HIV care and its relevance to test-and-treat strategies for prevention of HIV infection. Clin Infect Dis. 2011;52(6): 793---800. 13. Weis KE, Liese AD, Hussey J, Gibson JJ, Dufus WA. Associations of rural residence with timing of HIV diagnosis and stage of disease at diagnosis, South Carolina 2001-2005. J Rural Health. 2010;26:105---112.
27. Bertolli J, Shouse RL, Beer L, et al. Using HIV surveillance data to monitor missed opportunities for linkage and engagement in HIV medical care. Open AIDS J. 2012;6:131---141.
14. Ohl ME, Perencevich E. Frequency of human immunodeficiency virus (HIV) testing in urban vs. rural areas of the United States: results from a nationallyrepresentative sample. BMC Public Health. 2011;11:681. 15. Sutton M, Anthony MN, Vila C, Lellan-Lemal E, Weidle PJ. HIV testing and HIV/AIDS treatment services in rural counties in 10 southern states: service provider perspectives. J Rural Health. 2010;26: 240---247. 16. Zukoski AP, Thorburn S. Experiences of stigma and discrimination among adults living with HIV in a low HIV-prevalence context: a qualitative analysis. AIDS Patient Care STDS. 2009;23:267---276. 17. Meyerson B, Barnes P, Emetu RE, Bailey M, Ohmit A, Gillespie A. Institutional and structural barriers to HIV testing: elements for a theoretical framework. AIDS Patient Care STDS. 2014;28(1):22---27. 18. Arya M, Patuwo B, Lalani N, et al. Are primary care providers offering HIV testing to patients in a predominantly Hispanic community health center? An exploratory study. AIDS Patient Care STDS. 2012;26(5):256---258. 19. Cunningham CO, DeLuca J, Dyksterhouse R, Asgary R, Sacajiu G. Routine opt-out HIV testing in an urban community health center. AIDS Patient Care STDS. 2009;23(8):619---623. 20. Mimiaga MJ, Johnson CV, Reisner SL, VanDerwarker R, Mayer KH. Barriers to routine HIV testing among Massachusetts community health center personnel. Public Health Rep. 2011;126:643---652. 21. Johnson CV, Mimiaga MJ, Reisner SL, VanDerwarker R, Mayer KH. Barriers and facilitators to routine HIV testing: perceptions from Massachusetts Community Health Center personnel. AIDS Patient Care STDS. 2011; 25(11):647---655. 22. Myers JJ, Modica C, Dufour MS, Bernstein C, McNamara K. Routine rapid HIV screening in six community health centers serving populations at risk. J Gen Intern Med. 2009;24(12):1269---1274. 23. Weis KE, Liese AD, Hussey J, et al. A routine HIV screening program in a South Carolina community health center in an area of low HIV prevalence. AIDS Patient Care STDS. 2009;23(4):251---258. 24. Henry J. Kaiser Family Foundation, The Kaiser Commission on Medicaid and the Uninsured. Quality of Care in Community Health Centers and Factors Associated With Performance. June 2013. Available at: http:// kaiserfamilyfoundation.files.wordpress.com/2013/06/ 8447.pdf. Accessed July 30, 2013. 25. Trust for America’s Health. Investing in America’s health: a state by state look at public health funding & key health facts. Issue Report. May 2014. Available
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Routine HIV Testing in Indiana Community Health Centers Beth E. Meyerson, MDiv, PhD, Shalini M. Navale, MPH, PhD(c), Anthony Gillespie, and Anita Ohmit, MPH
Community health centers (CHCs) have been important providers of primary and preventive care since the late 1960s for communities with uninsured or underinsured patients.1 The importance of CHCs is heightened for the millions who remain without insurance coverage because of the varied implementation of the Affordable Care Act, because almost half of US states have opted not to expand Medicaid,2 and because the federal government has delayed the implementation of the employer health insurance mandate until 2015.3 It has been argued that CHCs are uniquely positioned to provide community-based, nonstigmatized access to specialty services, such as HIV testing.1,4 Recent HIV testing recommendations by the US Preventive Services Task Force call for routine testing among adolescents and adults in clinical settings,5 echoing the 2006 Centers for Disease Control and Prevention recommendation.6 Such recommendations imply that testing services likely will be reimbursed—an important point for resource-constrained environments and a financial incentive to improve practitioner compliance around HIV testing. CHCs themselves have been the target of additional efforts to increase HIV testing to help fulfill the National HIV/AIDS Strategy to reduce new HIV infections.7---9 Understanding HIV testing in CHCs is important because it is now known that 20% of those living with HIV in the United States do not know their status,10 and 40% of those who learn it do so within a year of an AIDS diagnosis.11,12 Delayed HIV testing is particularly acute in rural populations,13,14 because barriers to testing such as stigma and fear of anonymity loss are more pronounced.15,16 Publicly funded HIV testing, while helpful to some communities, may not be sufficient to improve early HIV testing in all communities. A recent evaluation of HIV testing sites in a state with moderate HIV incidence found several important problems related to access: 20% of test attempts failed to result in a test, 48% of sites had reported confidentiality issues, and a little fewer than half of the sites received
Objectives. We assessed routine HIV testing in Indiana community health centers (CHCs). Methods. CHC medical directors reported HIV services, testing behaviors, barriers, and health center characteristics via survey from April to May 2013. Standard of care testing was measured by the extent to which CHCs complied with national guidelines for routine HIV testing in clinical settings. Results. Most (85.7%) CHCs reported HIV testing, primarily at patient request or if the patient was symptomatic. Routine HIV testing was provided for pregnant women by 60.7% of CHCs. Only 10.7% provided routine testing for adolescents to adults up to age 65 years. Routine testing was reported by 14.3% for gay and bisexual men, although 46.4% of CHCs reported asking patients about sexual orientation. Linkage to care services for HIV-positive patients, counseling for HIV treatment adherence, and partner testing generally was not provided. Conclusions. Most CHCs reported HIV testing, but such testing did not reflect the standard of care, because it depended on patient request or symptoms. One approach in future studies may be to allow respondents to compare current testing with standard of care and then reflect on barriers to and facilitators of adoption and implementation of routine HIV testing. (Am J Public Health. 2015;105:91–95. doi:10. 2105/AJPH.2014.302203)
a “no return” rating by test visitors (meaning that those evaluating the test site would not return for an HIV test if they needed one in the future).17 Given the delays in testing and the troubles experienced in some publicly funded testing sites, a tremendous need exists to understand whether and how routine HIV testing is offered in other public health settings such as CHCs. Despite the emerging federal interest in HIV testing in CHCs and the public health importance of understanding testing in these environments, not much is known about the level of services in CHCs, particularly in areas with moderate HIV incidence and in Midwestern settings. Studies evaluating routine HIV testing in CHCs have focused on patient acceptance of testing18,19 or on provider testing behavior.20---23 Implementation studies provided participating CHCs with training and HIV rapid test kits to facilitate participation and success. The most recent studies occurred in urban areas: one among patients in a Houston, Texas, CHC serving a predominantly Hispanic population21 and the other, the largest of extant studies, comparing the views of clinicians in 31 Boston, Massachusetts, health centers.23
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Notably, the Boston CHCs were rated as high performing in a recent national review of performance and may not reflect the performance of CHCs in other communities.24 Studies of HIV testing in CHCs have not yet included moderate HIV incidence states or focused on rural and urban areas. These communities tend to have lower levels of HIV prevention and public health investment, which heightens the need for strong HIV testing services in CHCs. The objective of this study was to identify the extent to which CHCs in Indiana implement routine HIV testing. Indiana is a Midwestern, moderate HIV incidence state with low public health investment. In 2014, Indiana ranked 50th in per capita funding from the Health Resources and Services Administration (federal funding source for HIV treatment and also for CHCs) and from the Centers for Disease Control and Prevention (the primary federal funding source for HIV prevention). Indiana ranked 37th for state per capita public health investment.25
METHODS The study applied community participatory research principles. The research goal, methods,
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and analysis plan were developed by a community-based research team composed of the Indiana University School of Public Health-Bloomington; the Rural Center for AIDS/STD Prevention; the Indiana Minority Health Coalition; minority health coalitions from Lake, Marion, St. Joseph, and Vigo counties; the American Indian Center of Indiana; the Indiana HIV Prevention Community Planning Group; the Midwest AIDS Training and Education Center; the Indiana Primary Health Care Association; and the Indiana State Department of Health Division of HIV/STD and Viral Hepatitis and the Office of Primary Care. Clarification of CHC categorization and inclusion was determined in conference with the Office of Primary Care of the Indiana State Department of Health and the Indiana Primary Health Care Association. We measured HIV testing in CHCs by a 42-question online survey of Indiana CHC medical directors from April to May 2013. Participants were recruited by e-mail invitation to clinic leadership from the state of Indiana’s Office of Primary Care. This office sent 2 reminder e-mails during the study period to encourage survey completion, and the final e-mail offered a telephone interview by a research staff member. The survey gathered both quantitative and qualitative data about current HIV services, testing expectations, clinician behaviors and beliefs, barriers to and facilitators of services, and characteristics of the health center. We measured clinic expectations for HIV testing for adults aged 65 years or younger, pregnant women, and gay or bisexual men. The phrase “testing expectations” was used in the survey as a proxy for clinic policy guiding HIV testing because it was thought that many CHCs would not have a written policy about HIV testing but might operate with some type of expressed expectation. We measured standard of care testing by the extent to which CHCs complied with current 2012 US Preventive Services Task Force guidelines for routine HIV testing in clinical settings for adolescents to adults aged 65 years and for pregnant women.8 Although quite recent, this guidance essentially reflected the 2006 Centers for Disease Control and Prevention recommendations for routine testing in clinical settings.9 We described quantitative data and then evaluated for associations with key
infrastructure and demographic indicators such as Federally Qualified Health Center designation, Rural Health Center designation, Ryan White Comprehensive AIDS Resources Emergency Act funding, clinic categorization (multisite, hospital, county, unaffiliated), and census designation (rural or urban). We gathered qualitative data to provide explanation to quantitative responses. These were coded textually for emerging themes, verified by a second and independent coder, and quantitated to assist statistical comparison with reported testing behaviors and clinic indicators.
RESULTS Indiana has a total of 40 CHCs operating 134 clinic sites. CHCs were classified into 4 types: (1) multisite CHCs (of which there are 18 CHCs with 93 sites), (2) county government---associated networks (of which there are 3 CHCs with 11 sites), (3) hospital-associated networks (of which there are 10 CHCs with 22 sites), and (4) unaffiliated CHCs (of which there are 9 CHCs or clinics). Completed surveys were returned by 28 CHCs for a response rate of 70%, with representation from each classification: multisite (61.1%), county government (100%), hospital (63.6%), and unaffiliated (77.8%; Table 1). Of the CHCs in the sample, 28.6% had a Federally Qualified Health Center designation, and 32.1% had a Rural Health Center designation. More than half of the CHCs (67.9%) primarily served metropolitan areas, 14.3% served micropolitan areas, and 17.9% served rural communities.
HIV Testing Expectations and Practice Most CHCs reported HIV testing (85.7%), but routine HIV testing was not the norm
among CHCs in this sample. As noted in Table 2, HIV testing at standard of care was reported for pregnant women most often (60.7%). Only 10.7% of CHCs tested at standard of care for adolescents to adults aged 65 years, and 14.3% tested at standard of care for gay or bisexual men. CHCs in metropolitan areas were more likely to report standard of care testing for pregnant women and the only CHCs to report standard of care testing for gay or bisexual men. CHCs that provided standard of care testing for pregnant women did not necessarily report standard of care testing for gay and bisexual men or for other adults aged 65 years or younger. Participants were asked to identify the clinic expectations for HIV testing—when, under what conditions, and for what populations testing would be offered. Three populations were presented to respondents, with several options related to the conditions for testing (only at patient request, only if patient is symptomatic, patient circumstance such as trimester timing) and related to timing (e.g., annual, every 3 years). Table 3 reports clinic expectations for HIV testing for each of 3 populations: adolescents to adults aged 65 years or younger, pregnant women, and gay or bisexual men. As reported, HIV testing was generally offered only at patient request or when patients were symptomatic. This was reported for more than half of the CHCs for adults aged 65 years or younger and for about 40% of CHCs for gay and bisexual male patients. More than half (57.1%) reported offering testing to pregnant women at first trimester. Notably, several CHCs reported lack of knowledge about HIV testing expectations and practices for gay or bisexual men (35.7%) and for pregnant women (28.6%).
TABLE 1—Indiana Community Health Center (CHC) Characteristics (n = 28): April–May 2013 CHC Type
Metropolitan
Rural or Micropolitan b
Sample, No. (% of Classification) 3 (100)
County affiliated
1
2
Hospital affiliated
3
4b
6 (63.6)
Multisite
9a
2b
11 (61.1)
Unaffiliated
6a
1
10 (77.8)
Total
19
9
28
a
Federally Qualified Health Center designations for 5 multisite CHCs and 3 unaffiliated CHCs. Rural Health Center designations for 2 county government–affiliated CHCs, 5 hospital-affiliated CHCs, and 2 multisite CHCs.
b
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TABLE 2—Standard of Care HIV Testing by Population and Selected Community Health Center Characteristics (n = 28): Indiana, April–May 2013 Adults Aged £ 65 Years, No. (% Category)
Characteristic
Pregnant Women, No. (% Category)
Gay or Bisexual Men, No. (% Category)
Results, Partner Services, and Linkage to Care
Federally qualified health center Yes (8 clinics)
1 (12.5)
6 (75.0)
2 (25.0)
No (20 clinics) Rural Health Center
2 (10.0)
11 (55.0)
2 (10.0)
Yes (9 clinics)
1 (11.1)
4 (44.4)
...
No (19 clinics)
2 (10.5)
13 (68.4)
4 (21.0)
Yes (19 clinics)
2 (10.5)
13 (68.4)
4 (21.1)
No (9 clinics)
1 (11.1)
4 (44.4)
...
1 (33.3) ...
2 (66.7) 2 (28.6)
... ...
Most CHCs (90.9%) reported encouraging patients to refer partners for testing and treatment, but 89.3% indicated that they do not provide on-site counseling, risk reduction, or testing for partners; however, 50.0% reported that they would do so if partners were patients of the health center. HIV treatment generally was not provided by CHCs, because 72.7% of the participants reported referring patients elsewhere for HIV treatment “all of the time.” Participants did not indicate how they evaluated or ensured patient access to HIV treatment or adherence to antiretroviral medications once patients were referred elsewhere for treatment.
Metro
Classification County (3 clinics) Hospital (7 clinics) Multisite (11 clinics)
1 (9.1)
8 (72.7)
3 (27.3)
Unaffiliated clinic (7 clinics)
2 (28.6)
4 (57.1)
1 (14.3)
Total at standard of care (28 clinics)
3 (10.7)
17 (60.7)
4 (14.3)
This is significant because 46.4% of CHCs reported asking patients about sexual orientation. Reported testing expectations and clinic classification, Federally Qualified Health Center or Rural Health Center status, and census designation were not found to be associated at the P < .05 level. When asked their perception of how well staff followed CHC HIV testing expectations, 37.9% indicated that clinicians followed expectations very well, 51.8% indicated well or most of the time, and 10.3% reported that compliance varied by clinician. Fewer than half
(46.7%) of the participants indicated that HIV screening recommendations were the most difficult to follow as compared with hepatitis C, sexually transmitted diseases (gonorrhea, chlamydia, syphilis), and cervical cancer. Most participants (73%) believed that no barriers to HIV testing existed for their CHCs, yet 20.9% reported barriers to HIV testing. Community discomfort with HIV, lack of HIV treatment options in the community, and cost including lack of reimbursement for testing were most commonly cited. Published protocols, guidelines, and policies facilitated staff adherence to
TABLE 3—Reported Expectations for HIV Testing in Indiana Community Health Centers by Population (n = 28): April–May 2013 Expectation
Adults Aged £ 65 Years, No. Clinics (%)
Gay or Bisexual Men, No. Clinics (%)
Pregnant Women, No. Clinics (%)
Only at patient request
17 (60.7)
12 (42.9)
2 (7.1)
Only if patient is symptomatic
14 (50.0)
11 (39.3)
2 (7.1)
3 (10.7)
4 (14.3)
...
... ...
... ...
... ...
Annual Every 3 y Every 5 y First trimester
...
...
16 (57.1)
Second trimester
...
...
1 (3.6)
Third trimester
...
...
2 (7.1)
Delivery
...
...
1 (3.6)
3 (10.7)
10 (35.7)
8 (28.6)
Do not know
clinic screening expectations for 50% of CHCs, and 15.4% of the respondents perceived that management guidance or clinician knowledge of protocols facilitated testing.
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Training Offered to or Expected of and Obtained by Clinic Staff CHCs were asked to indicate whether any of 4 nationally emphasized training topics were available and required of clinicians in 201226: offering and providing HIV testing, HIV screening guidelines, delivering prevention counseling to HIV-positive patients to reduce transmission, and retaining HIV-positive patients in care. A smaller sample of CHCs (n = 22) responded to related questions. More than half (60.0%, 12) of the CHCs reported that training about HIV screening guidelines and training focused on offering and providing HIV testing were available to clinicians in 2012, but neither was required of clinicians. Training about the HIV screening guidelines was available and required at only 3 (13.6%) CHCs, and only 2 (9.1%) required training about offering and providing HIV testing in 2012. Those CHCs where training was not available for one module tended also to report that training was not available for the other modules (Fisher P = .008). Associations were not significant between available or required training and clinic characteristics such as Federally Qualified Health Center status, metropolitan or nonmetropolitan, and clinic affiliation. However, associations with testing below standard of care for adults
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aged 65 years or younger and the lack of available training about HIV prevention counseling and retention of patients in care was significant at P £ .05. A significant association also was found between not testing at standard of care for gay and bisexual men and having training about HIV screening guidelines made available but not requiring it of clinicians in 2012.
DISCUSSION This study was a baseline study of CHC provision of routine HIV testing in a Midwestern, moderate HIV incidence state with low levels of public health investment. Most CHCs reported providing HIV testing, but such testing did not reflect the standard of care, because it depended on patient request or symptoms. Even though most CHCs reported no barriers to HIV testing, several indicated that the HIV guidelines were most difficult to follow. At the same time, a bit of confusion emerged, because respondents reported that most clinicians followed the guidelines well and that such guidelines were the basis of testing practice. Additional evaluation will help to make sense of this particular observation. It may be entirely possible that expectations for HIV testing (patient request or symptoms) were seen as appropriate because of the funding environment: public health funding for HIV testing is lacking in Indiana CHCs. Therefore, barriers to this reported testing approach under the current funding scenario were not perceived. This theory is further reinforced by the observation that resource constraints were not identified as barriers to HIV testing by most CHCs. Still, offering testing only at patient request or if symptomatic reflects a critical obliviousness to potential testing barriers faced by patients who are in need of HIV testing. One approach in future studies may be to allow respondents to compare their current testing with standard of care and then reflect on barriers to and facilitators of adoption and implementation of routine HIV testing to standard of care. As CHCs evolve more fully into their role as medical homes for all patients, including those with HIV, they will need to focus on services such as retention of patients in HIV medical care and especially antiretroviral treatment
adherence. This is important in Indiana because according to a more rigorous definition of linkage to care, it is estimated that 45% of people living with HIV in Indiana are not linked with medical care.27 Respondents in this study could not articulate standard of care for managing HIV-positive patients beyond referral to specialty care outside the CHC. Partner counseling regarding testing, treatment retention practices, and access to additional HIVrelated services will be necessary components of medical homes for patients who have HIV. CHCs appeared to function well from a disease-reporting standpoint, because most reported diagnoses to the health department for these communicable conditions. Most CHCs also reported the encouragement of partners to obtain testing; however, this encouragement was likely no more than a testing referral, given the reported lack of partner services unless the partner was a patient of the CHC. As such, the functioning of CHCs in the public health system of care was unclear when it came to linking sexual partners of patients testing positive for HIV to testing and eventual treatment. Greater opportunities between local public health departments, HIV prevention organizations, and CHCs exist to coordinate partner services and to ensure a well-coordinated HIV prevention and treatment system of care. This study was an important baseline assessment of current HIV testing practices in a Midwestern state’s CHCs because it yielded a critical clinical practice deficit for public health program and policy focus. As CHCs begin to realize their role as medical homes in an era of routine HIV testing and linkage to care, additional resources and evaluation will be needed to ensure standard of care and therefore greater access to HIV testing. Future studies should examine CHC testing practices across several states with a focus on characteristics such as public health investment in HIV prevention, CHCs, and public health generally. j
SPH 116, Bloomington, IN 47405 (e-mail: bmeyerso@ indiana.edu). Reprints can be ordered at http://www.ajph. org by clicking the “Reprints” link. This article was accepted July 1, 2014.
About the Authors
9. Health Resources and Services Administration. Implementing Our Strategic Plan: Health Resources and Services Administration. [monograph]. 2011. Available at: http://www.hrsa.gov/about/strategicplanimplementation. pdf. Accessed July 8, 2013.
Beth E. Meyerson and Shalini M. Navale are with Indiana University School of Public Health-Bloomington. Anthony Gillespie and Anita Ohmit are with Indiana Minority Health Coalition, Inc, Indianapolis. Correspondence should be sent to Beth Meyerson, MDiv, PhD, Indiana University School of Public HealthBloomington Applied Health Science, 1025 E 7th St, Room
94 | Research and Practice | Peer Reviewed | Meyerson et al.
Contributors B. E. Meyerson, A. Gillespie, and A. Ohmit conceptualized the study. B. E. Meyerson directed all aspects of the study and the article preparation. S. M. Navale assisted in data collection, participated in the data analysis, and edited article iterations. A. Gillespie and A. Ohmit interpreted the study results and participated in editing the article.
Acknowledgments The study was funded by the Indiana Minority Health Initiative.
Human Participant Protection This study was deemed exempt by the Indiana University institutional review board.
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