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J Womens Health (Larchmt). Dec 2008; 17(10): 1609–1614.
PMCID: PMC2716001
HIV Women's Health: A Study of Gynecological Healthcare Service Utilization in a U.S. Urban Clinic Population
Monique A. Tello, M.D., M.P.H.,corresponding author1 Hsin-Chieh Yeh, Ph.D.,1,2 Jean M. Keller, P.A.C.,3 Mary C. Beach, M.D., M.P.H.,1 Jean R. Anderson, M.D.,3 and Richard D. Moore, M.D., M.H.Sc.1
1Department of Medicine, Division of General Internal Medicine, Johns Hopkins Medical Institutions, Baltimore, Maryland.
2Department of Epidemiology, Johns Hopkins School of Public Health, Baltimore, Maryland.
3Department of Gynecology and Obstetrics, Johns Hopkins Medical Institutions, Baltimore, Maryland.
corresponding authorCorresponding author.
Address reprint requests to: Monique Aurora Tello, M.D., M.P.H., MGH Women's Health Associates, 55 Fruit Street, Yawkey 4B, Suite 4700, Boston, MA 02114. E-mail:mtello/at/partners.org
Background
Women infected with HIV have a high rate of many gynecological problems. Adherence to recommended gynecological care among women enrolled in our urban HIV clinics was hypothesized to be low.
Methods
We conducted an analysis of data from the Johns Hopkins HIV Clinical Cohort Database examining demographic and clinical predictors of clinic visit adherence by women in the HIV primary care and HIV gynecological clinics.
Results
Between January 2002 and April 2006, 1,086 women had 26,401 scheduled appointments to the two clinics, of which 21,959 were to HIV primary care and 4,442 were to HIV gynecological care. There were 12,097 (55%) completed primary care visits and 1,609 (36.2%) completed HIV gynecological visits (p < 0.001, accounting for clustering). By multivariate analysis, age <40 years (OR 0.81, 95% CI 0.70-0.94) and substance abuse (OR 0.67, 95% CI 0.61-0.73) were associated with a decreased likelihood of attending an HIV primary care appointment. African American race (OR 0.63, 95% CI 0.45-0.90), CD4 count <200 cells/mm3 (OR 0.73, 95% CI 0.56-0.95), and substance abuse (OR 0.57, 95% CI 0.45-0.71) were associated with a decreased likelihood of attending an HIV gynecological appointment.
Conclusions
This analysis determined that the rate of clinic visit adherence is significantly lower for HIV gynecological care than for HIV primary care in the same population of women. Factors associated with HIV gynecological clinic visit noncompliance included African American race/ethnicity, substance use, and more advanced immunosuppression. We have planned additional quantitative and qualitative studies to examine the associations with and barriers to HIV gynecological care, with the goal of creating appropriate interventions toward improving gynecological healthcare utilization among women enrolled in urban HIV clinics.
There are an estimated 1.2 million people living with HIV in the United States, and 300,000 of these are women.1 In Maryland, there are 14,346 people living with HIV, of whom 5,424 (38%) are women.2 Women infected with HIV are at increased risk for many gynecological problems, including vaginitis, genital herpes, genital condylomata, pelvic inflammatory disease (PID), and lower genital tract dysplasia and neoplasia.35 HIV-infected women have higher rates of cervical, vulvar, vaginal, and anal intraepithelial lesions than HIV-uninfected women,6 and invasive cervical cancer is an AIDS-defining illness. Based on our clinical experiences, however, we hypothesized that adherence to recommended gynecological care in our urban HIV clinic environment was poor.
Since the introduction of highly active antiretroviral therapy (HAART), HIV has become a chronic disease, and people infected with HIV require diverse preventive, acute, and long-term healthcare services.7 When available and recommended services are not used correctly, not only is quality of patient care compromised but also healthcare costs increase.7 Information on gynecological healthcare utilization patterns in the HIV-seropositive population can reveal underutilized and wasted resources and disparities in care. To better understand the extent of this problem, we analyzed data from an urban HIV clinic population where both primary and gynecological care is offered to HIV-infected adult women. This analysis was designed to determine the prevalence of scheduled visit compliance and to identify factors contributing to or associated with HIV gynecological scheduled clinic visit compliance.
The Johns Hopkins University AIDS Service provides comprehensive primary and subspecialty medical care, including gynecological care (the Johns Hopkins HIV Women's Health Program), that is located in a single clinic facility. The majority of patients who are seen there for HIV primary care are also referred to the Johns Hopkins HIV Women's Health Program for all preventive and acute gynecological care. The HIV primary care examination rooms are not equipped for pelvic examinations or for collecting gynecological specimens. Once a patient is referred to the HIV Women's Health Program, that patient's subsequent gynecological care is maintained and scheduled through the HIV Women's Health Program. With one exception, the HIV primary care and gynecological providers are different providers. The waiting room and registrar are shared.
All continuity care patients who enroll in the HIV primary care clinic are offered the opportunity to join a prospective, observational clinical cohort. The refusal rate is <1.5%. At baseline, a comprehensive evaluation of medical and social histories, physical examination, and laboratory studies is recorded. These data are prospectively updated from the clinic-based medical record by trained data monitors every 6 months, with new medical diagnoses, hospitalizations, procedures, pharmaceutical prescriptions and filling, and laboratory and radiographic results. Maintenance of the cohort and use of its contents for analysis of patient outcomes are approved by the Institutional Review Board of the Johns Hopkins University School of Medicine.
This study is based on a subset of data collected on women who had at least one visit to the HIV clinic during January 2002 to April 2006. Clinic appointments to the HIV primary care and HIV gynecological clinics were recorded as completed, missed, or cancelled. A cancelled visit (either by the provider or the patient) was not designated as a missed visit. The percents of missed visits for each of the two clinics were calculated. We also compared clinic visit adherence for the two clinics and conducted multivariate analyses using logistic regression. A generalized estimating equations (GEE) approach was used to account for clustering of multiple clinic visits by the same patients. The multivariate analyses examined the association between clinic visit adherence for the two clinics with race (African American or Caucasian), age <40 years, CD4 count <200 cells/mm3, HIV-1 RNA level >400 c/mL (copies per milliliter of blood), receiving HAART prior to the scheduled appointment, having a history of an AIDS-defining opportunistic illness (OI) prior to scheduled appointment, having a history of hospitalization prior to scheduled appointment, heavy alcohol use (defined as self-reported >7 drinks per week, on average, at baseline), and illicit or injection substance use (any self-reported history of cocaine or heroin use at baseline). Age 40 was chosen as a break point for several reasons: 95% of endometrial cancers are diagnosed in women aged ≥40, so women > age 40 with irregular bleeding generally receive more aggressive evaluation8; most gynecological malignancies are diagnosed in women >40 years, even in women with HIV9; it is also the age when yearly mammography should begin.10
Table 1 shows the demographic characteristics of the 1,086 total female patients who had at least one visit between January 2002 and April 2006. The mean age was 36.6 years, with 84% of patients self-identified as African American. There was a high prevalence of illicit substance abuse at baseline in this population, with 58% of patients reporting some history of cocaine or heroin use by injection or other administration. These women had 26,401 appointments to the two clinics, of which 21,959 were to primary care and 4,442 were to gynecology. There were 12,097 (55.1%) completed HIV primary care clinic visits, and there were 1,609 (32.2%) completed HIV gynecological clinic visits. By logistic regression accounting for clustering, patients were half as likely to appear for their HIV gynecological clinic appointments as for their HIV primary care visit appointments (OR 0.48, 95% CI 0.44-0.52). By multivariate analyses, age <40 years (OR 0.81, 95% CI 0.70-0.94) and any illicit substance abuse at baseline (OR 0.67, 95% CI 0.61-0.73) were associated with a decreased likelihood of attending an HIV primary care appointment (Table 2). African American race (OR 0.63, 95% CI 0.45-0.90), CD4 count <200 cells/mm3 (OR 0.73, 95% CI 0.56-0.95) and any illicit substance abuse at baseline (OR 0.57, 95% CI 0.45-0.71) were associated with a decreased likelihood of appearing for a scheduled HIV gynecological appointment (Table 3).
Table 1.
Table 1.
Demographic Characteristics of 1,086 Female Patients
Table 2.
Table 2.
Demographic and Clinical Predictors of HIV Primary Care Clinic Visit Adherence
Table 3.
Table 3.
Demographic and Clinical Predictors of HIV Gynecological Clinic Visit Adherence
No previous study has compared adherence by women to HIV primary care and gynecological visits simultaneously using actual clinic records data. Although there is a relatively low rate of scheduled primary care clinic visit adherence in our population of HIV-infected women, the rate of gynecological clinic visit adherence is significantly lower than the rate of primary care visit adherence in the same population of women. It is important to note that this study was done in a facility where the gynecological specialty services are located in the same clinic facility, which is intended to facilitate comprehensive care. However, these results demonstrate that there remain what would appear to be substantial barriers to gynecological care in HIV-infected women. The high rate of missed gynecology appointments indicates a potentially serious healthcare diagnosis and management problem, especially given the high rates of gynecology-associated illness known to occur in this population.
Gynecological healthcare is an important component of ongoing HIV care in women. A study of 262 HIV-infected women found that 46.9% had at least one incident gynecological condition with serial assessment, including such conditions as vulvovaginal candidiasis, oncogenic human papillomavirus (HPV), abnormal Pap smears, genital warts, and amenorrhea.11 In a study of 65 women admitted to an inpatient AIDS service, 83% had coexisting gynecological disease, although only 9% were admitted with a primary gynecological problem.3 The prevalence of cervical dysplasia in HIV-infected women varies from 11% to 60%,1214 rates approximately 10-fold higher than that observed among HIV-uninfected women.15 Studies have shown that Pap smear sensitivity and specificity are comparable in HIV-infected and uninfected women,12 although mild cytological atypia, such as atypical cells of undetermined significance (ASCUS) and inflammation, are more likely to be associated with dysplasia in HIV-infected women than in HIV-uninfected women and should prompt follow-up, generally including colposcopic examination.4,16 There is a clearly increased prevalence of squamous intraepithelial lesions (SIL) among HIV-infected women, and diagnosis of SIL in the HIV-infected woman always warrants colposcopic examination.4,5,12 Confirmation of a high-grade cervical lesion mandates excisional treatment to prevent progression to invasive cervical cancer, an AIDS-defining illness. Furthermore, unlike other AIDS-associated infections, effective combination antiretroviral therapy and immune reconstitution are not clearly associated with reduction or regression of HPV-related lesions, including lower genital tract dysplasia, although study findings are mixed.17,18
Few studies have examined adherence with gynecological visits among HIV-positive women. The prospective Swiss HIV Cohort Study (SHCS) examined factors associated with frequency of gynecological follow-up, including cervical cancer screening, in a cohort of 2,186 HIV-positive women using self-reported data; they found that only 45% of those women reported seeing a gynecologist within the previous 6 months, although 82% of the women reported having a Pap smear. Predictors for fewer gynecological examinations and Pap smears were older age, nonwhite ethnicity, current IVDU, lower education, lower CD4 counts, underweight, obesity, and current smoking.19 Another study showed that 70% of a sample of U.S. urban HIV-positive women reported having had a gynecological examination in the previous year.20 These results, which are based on self-reported data, suggest that adherence with recommended gynecological care among HIV-positive women is inadequate.
Most studies of gynecological healthcare utilization in the HIV-seropositive population have focused on compliance with recommended cervical cancer screening, Pap smear evaluation, and follow-up of abnormal Pap smear results. One large study of 43,000 HIV-positive women found that a significant percentage of women who had abnormal Pap smears did not receive a repeat Pap test or colposcopy.13 A study of adherence to colposcopy among 462 women with or at risk for HIV infection found that adherence rates were 65% and comparable to the national average but “nevertheless unacceptably low for a group at such high risk for SIL.”21 A 2006 Quality Improvement Program Review of HIV primary care services conducted by the Baltimore City Health Department Ryan White Title I Office showed that only 50% of HIV-positive women in Baltimore City had received a Pap smear in the previous year.22 Our finding of an association between a CD4 count <200 cells/mm3 and greater nonadherence to scheduled clinic visits is particularly troubling, as the incidence and the severity of gynecological pathology may be greater in women with advanced immunosuppression.
Our study found that African American race increased the risk of missed gynecological visits but not missed HIV primary care visits. Our study population is 84% African American, which may differ from other study populations. One study showed that urban HIV-positive African American women were less likely to have had an outpatient visit in the previous 6 months or to have been on OI prophylaxis.20 Several studies have also identified race/ethnicity as a factor associated with cervical cancer screening disparities in the HIV-uninfected population. In 1996, the National Institutes of Health (NIH) issued a consensus statement on cervical cancer, which stated that in the United States, ethnic and racial minority women, elderly women, medically uninsured women, and low-income women were not screened or were not screened at regular intervals for cervical cancer.23 In a 2005 study conducted by the National Breast and Cervical Cancer Early Detection Program (NBCCEDP) on recommended follow-up for ASCUS or low-grade SIL (LSIL) of over 10,000 women, only 44% of women received appropriate follow-up, and African American women were least likely to receive appropriate follow-up.24 Studies focusing on minority racial/ethnic populations indicate that lack of health insurance, lower level of education, lack of continuity of care, and lower use of public services were associated with lack of adherence to annual Pap smears.2527 Unfortunately, we did not have data to assess income, employment, or education. All of our patients were either insured or were eligible to receive primary and gynecological care paid by the Ryan White CARE Act support, which does not require an enrollment wait time or other special procedure in our region, so insurance was not likely a barrier in this study.
We also found that substance use was associated with a decreased rate of both gynecological appointment and primary care visit adherence. One study showed that U.S. urban HIV-positive intravenous drug users were less likely to report having a regular doctor or any outpatient visit in the previous 6 months.20 Although there is scant literature on the association of substance abuse with primary care or gynecological appointment adherence, several studies examining the HIV-infected population in general have linked such factors as substance abuse to HIV medication nonadherence.2831 One study of 150 HIV-infected people found that drug use was associated with a 4-fold greater risk of medication adherence failure.32 Unfortunately substance use and abuse in women is closely linked to HIV: the CDC reported that 1 in 5 new HIV diagnoses in women were related to injection drug use in 2005.1 Women who sell or trade sex for drugs are at risk for HIV infection through sexual transmission. A study of HIV-positive African American women with histories of childhood sexual abuse found that substance use was a significant health problem, as well as a barrier to healthcare.33 Crack cocaine use has been negatively associated with colposcopy adherence among women with or at risk for HIV infection.21
Our results indicating a generally low rate of appointment adherence are consistent with results of other studies of barriers to healthcare utilization in HIV-infected women. For example, HIV-infected women are less likely to be on combination antiretroviral therapy and are more likely than men to have hospitalizations and emergency room visits.34 Other studies have suggested that healthcare systems are not structured to meet women's healthcare needs: clinics tend to have inconvenient and inflexible hours, long waits, and a lack of staff from the same ethnic or racial groups as most patients.35 Authors have suggested that cultural values and beliefs, as well as such competing needs as for food, clothing, and shelter, may adversely affect Pap smear screening among women from racial and ethnic minority groups.27 Subsistence issues, such as lack of transportation and fear of the consequences of missing work, also have been identified as barriers to HIV-infected women receiving healthcare.36 One study of HIV-positive African American women found that barriers to healthcare included confidentiality issues, difficulty getting an appointment, long clinic wait times, and obligation to care for others. These authors call for HIV care interventions that link the cultural beliefs and values of the population with the health skills and attitudes being promoted in the clinic.33 Child care issues have been postulated to be a potential barrier to keeping medical appointments. Some physicians caring for HIV-infected women have advocated “a multidisciplinary approach to treatment and prevention that would address women's life circumstances along with their medical needs.”35, pg 652 Many of these factors may explain the generally low rate of appointment adherence we found but do not necessarily explain the discordantly low rate of gynecological appointment adherence, as many of these issues should have affected both HIV primary care and gynecological care, which are located in the same clinic facility. Both clinics use the same clinic operating hours, waiting room, and clinical space (although different sets of rooms), registrars, and medical assistants for vital signs. Wait times for appointment after referral, as well as wait times to be seen on the day of appointment, are similar. However, HIV primary care and HIV gynecological care appointments are rarely scheduled on the same day for each patient. In a national study of self-reported factors associated with cervical cancer screening among HIV-positive women, women who reported having a gynecologist and a primary care provider at the same clinical site were almost twice as likely to report having had a Pap smear in the previous 12 months.13 The authors concluded that providing gynecological care at the same site as primary HIV care might improve delivery of gynecological care. We did not find this to be the case at our clinic site.
This was an analysis of data from our prospective, observational clinical cohort. Therefore, we did not have additional variables of interest, such as income, employment, housing status, education, or psychosocial and behavioral factors. One study of HIV-infected U.S. adults found that 26% of patients perceived discrimination by healthcare providers and that this could discourage medication adherence and follow-up.37 Psychosocial measures, including depression, HIV stigma, low coping self-efficacy, low adherence self-efficacy, poor-perceived patient-provider relationship, low-perceived respect, and low-perceived utility of treatment also have been cited as contributing to medication nonadherence among HIV-infected clinic patients.38,39 As mentioned, belief factors, such as embarrassment, fear of discomfort during the gynecological examination, and fear of pathology, may be barriers to gynecological care, as may logistical concerns, such as child care issues. Several studies focusing on the Hispanic population have identified fatalistic attitude toward cancer, as well as embarrassment, fear, and pain during the pelvic examination, as potential barriers to having a Pap smear.40,41 Another study focusing on female college students also identified embarrassment and pain as potential barriers to undergoing a pelvic examination or a Pap smear, although the majority of women in the study had undergone Pap smears in the past year.42 We did not have access to these variables in our study.
We recognize the limitations of an analysis of data as a means to explore these behavioral and emotional issues, so we have developed subsequent quantitative and qualitative phases for study of this problem. In order to further examine and determine the barriers to HIV gynecological clinic visit adherence, we have developed and will be administering a targeted questionnaire to women who receive both HIV primary care and HIV gynecological care at our clinic. We will also conduct a qualitative study using focus groups comprising women who receive both HIV primary care and gynecological care at our clinic, which will attempt to further elucidate the major barriers to gynecological care for these women.
Our study of an urban HIV-positive population database shows a low rate of HIV primary care clinic visit compliance and a dramatically low rate of HIV gynecological clinic visit compliance. More information is needed to examine the barriers to HIV gynecological clinic visit adherence in this population, and we have quantitative and qualitative studies in place to clarify potential logistical, behavioral, and emotional variables that may ultimately help to improve care. Given the incidence and prevalence of gynecological pathology in HIV-infected women and the importance of early screening for detection of pathology, it will be critical to create appropriate interventions that target barriers to receiving gynecological healthcare among women enrolled in urban HIV clinics.
Acknowledgments
This study was supported by the Lawrence S. Linn award granted through the Society of General Internal Medicine in April 2007 (NIH ROI DA11602; K24DA00432).
Disclosure Statement
No competing financial interests exist.
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