In 2017, more than 2 million cases of chlamydia, gonorrhea, and syphilis were reported in the United States.1 The number of reported cases of acute HCV infection increased approximately 3.7-fold during a 7-year period, rising annually since 2010 to an estimated 44,300 cases in 2017.2 In addition, the number of HIV diagnoses reported annually in the United States remained steady in recent years, prompting a new initiative to reduce incident infections in the United States.3
Having an STI is an established risk factor for HIV infection4 and an indication for preventive services such as HIV preexposure prophylaxis (PrEP).5 The Centers for Disease Control and Prevention (CDC) recommends that all individuals between the ages of 13 and 64 years be tested for HIV at least once as part of routine health care6 and those who are at higher risk of HIV, including those with an STI, be tested at least annually.7 National surveys, however, demonstrate that these recommendations have not been fully implemented. An analysis of 2016 and 2017 population-based survey data found that overall, only 38.9% of the US population had ever been tested for HIV infection, including 46.9% in the 50 local jurisdictions where most new HIV diagnoses occurred and 35.5% in 7 states with disproportionate occurrence of HIV in rural areas.8 The concomitant rise in STI diagnoses and consistently low rates of HIV testing in the United States underscore missed opportunities for HIV screening.
Although the current CDC guidelines do not provide a specific recommendation for HIV screening of those diagnosed as having HCV infection,6,7 the National Institutes of Health Consensus Statement on HCV does recommend HIV testing for HCV-infected persons at risk of HIV infection.9 The shared risk factors for HIV and HCV transmission, and the synergistic effect of HIV on the adverse health outcomes and mortality risk of HCV-infected persons10 may warrant HIV testing among HCV-infected persons.11 HIV testing of HCV-infected persons can lead to the timely identification of HIV/HCV coinfected persons, inform medical care, and mitigate disease progression and mortality.
Integration of HIV screening into prevention and treatment of HCV infection and STIs is a critical example of how HIV testing can be normalized in clinical practice. HIV testing is necessary for HIV prevention and control, with an HIV test result providing the gateway to HIV treatment for persons with HIV infection or preventive services, such as PrEP, for persons without HIV infection.11–15 In addition, as the US opioid crisis continues, preventing the transmission of infectious diseases like hepatitis C and HIV through screening remains essential.16,17
In February 2019, the US government unveiled Ending the HIV Epidemic: A Plan for America , which is a national plan for reducing the number of new HIV infections by 90% by 2030.3 One of the four key strategies in the plan aims to bolster HIV screening, particularly among those who are at high risk of acquiring HIV, such as those who are diagnosed as having an HCV infection or STI, and to use the HIV test result to facilitate linkage to treatment or prevention services.3 Although prevalence and frequency of HIV testing have been examined in the United States,8 HIV testing rates between persons who have had an STI or HCV infection and those who have not have not been well examined among a nationally representative sample in the United States. The main aim of this article is to estimate HIV testing rates and changes in these rates over time for persons aged 20 to 59 years who reported a selected STI or HCV infection and those who did not, using data from the National Health and Nutrition Examination Survey (NHANES; 2005–2016).
METHODS
Data Source and Participant Selection
The NHANES is an ongoing survey of the civilian, noninstitutionalized population of the United States.18 A representative sample of households and noninstitutional quarters are included via multistage probability sampling. The NHANES collects information on a variety of topics including demographic information, sexual behaviors, history of STIs, and HIV testing. Participants completed a household interview, followed by a physical examination and interview at a mobile examination center (MEC). Sensitive questions on topics such as sexual behavior were administered privately at the MEC. Informed consent or assent was obtained from all participants or their guardians for both the interview and physical examination components, and the survey was approved by the CDC Research Ethics Review Board. We analyzed NHANES data collected from 2005 to 2016, representing six, 2-year cycles of data collection. Data were pooled from the 2005–2016 NHANES to increase sample size and reliability of estimates.18 Overall interview response rates ranged from 80.5% in 2005 to 2006 to 61.3% in 2015 to 2016.19 The average examination response rate for the pooled sample was 71.1% from 2005 to 2016. The NHANES only collected data on sexual behaviors and history of STIs from survey participants aged 20 to 59 years during some cycles between 2005–2006 and 2015–2016; thus, data regarding history of diagnosis of a selected STI were unavailable for respondents outside this age range. Therefore, the analytic sample (n = 22,101) was restricted to respondents who were 20 to 59 years of age and who had completed the questions on sexual behaviors and STI history at the MEC (n = 38,835 were excluded based on these parameters). After making this age restriction, some additional participants were excluded because they either did not complete the MEC examination and thus were not asked the questions about HIV testing and STI history, or they provided noninformative answers (e.g., “do not know”) to at least one of the questions about HIV testing or STI history (13.6%; resulting in a sample of 19,102).
Respondents were asked if their blood had ever been tested for HIV (excluding tests done as part of blood donation) at the MEC using the computer-assisted personal interviewing instrument. Respondents who self-reported ever having had sex were also asked if, in the past 12 months, they had been told by a doctor or other health care professional that they had chlamydia or gonorrhea, and if they had ever been told they had genital herpes. The questions about genital herpes, chlamydia, and gonorrhea were self-administered at the MEC using an audio computer-assisted self-interviewing instrument, so the responses to these questions were based on respondents' knowledge of their infection status. During the survey cycles between 2005 and 2012, the question about hepatitis C was asked on a follow-up telephone survey of respondents who tested HCV RNA positive at the MEC (Those who responded “no” to the following question: “Was the test result in our letter the first time you were told you had hepatitis C?” were coded as having been told they had hepatitis C.) During the survey cycles between 2013 and 2016, the hepatitis C question was asked of all respondents during the household interview using the computer-assisted personal interviewing instrument regardless of anti-HCV or HCV RNA positivity.20 Respondents who answered “yes” to having been told that they had any of the selected STIs (i.e., gonorrhea, chlamydia, and genital herpes) or HCV infection were classified as “reporting a previous diagnosis of selected STI or HCV infection.” The periods were not directly comparable given the change in how data on HCV infection were collected starting the 2013 to 2014 cycle. Therefore, we conducted a sensitivity analysis in which we considered respondents who answered “yes” to having been diagnosed as having any of the selected STIs (i.e., gonorrhea, chlamydia, and genital herpes), separately from those reporting being diagnosed as having STIs and an HCV infection.
Definition of Key Study Variables
Demographic and health-related covariates that have also been shown to be associated with risk of HIV infection3 were included in the analysis. These included the following: age; gender; race/ethnicity (coded as non-Hispanic white, non-Hispanic black, Hispanic, and other non-Hispanic race); education (high school graduate or less and some college or more); family annual income (at or below federal poverty level and above federal poverty level); marital status (married, living with partner, unmarried/single); health insurance status (yes/no); whether the respondent had a health care–related visit to a doctor or other health care professional in the past 12 months (yes/no); have a routine place to go for health care (yes/no); condom use (never, sometimes, always for both male and female respondents); ever pregnant including currently pregnant, live births, miscarriages, stillbirths, tubal pregnancies, and abortions (women only, yes/no); self-reported heterosexual or homosexual/bisexual identity; (yes/no); and gender of sex partners in the past 12 months (men only, women only, both men and women, and no partners).
Statistical Analysis
SAS-Callable SUDAAN software (Release 10.0; Research Triangle Institute, Durham, NC) was used to generate prevalence estimates. All analyses accounted for the complex NHANES survey design and data examination weights. Respondents with missing values, including responses of refused or do not know, were excluded in the estimation of reported proportions. Estimates of weighted proportions and their 95% confidence intervals were used to compare characteristics, and to assess differences in proportions reporting ever being tested for HIV based on demographic and health-related characteristics of US adults with or without a self-reported selected STI or HCV infection. Estimated proportion reporting ever being tested for HIV was also stratified by lifetime history of pregnancy and health care utilization in the past 12 months, as these factors were thought to potentially be associated with both HIV testing and self-reported diagnosis of other STIs or HCV infection. In addition, a Satterthwaite-adjusted Wald χ2 statistic was used to compare the association between HIV testing history between 2 cycles (2005–2006 and 2015–2016) both for those who reported having ever been told they had a selected STI or HCV infection and for those who did not. Because of the change in the way HCV infection was assessed, we conducted a sensitivity analysis in which the comparison of the proportion reporting ever being tested for HIV for 2005–2006 and 2015–2016 cycles were also estimated only for the group reporting a selected STI but not HCV infection. Statistical significance was determined at P < 0.05. Estimates with a relative standard error between 30% and 49% were included but flagged as potentially unstable; however, estimates with relative standard error greater than or equal to 50% were suppressed.
RESULTS
Overall, 44.4% of the US population aged 20 to 59 years reported ever having been tested for HIV. From 2005 to 2016, an average of 5.2% of the population reported having been told by a doctor or other health care professional that they had a selected STI or HCV infection. This percentage varied only slightly across cycles of NHANES (Appendix Table 1). The proportion reporting an HIV test was higher for the group that self-reported a selected STI or HCV infection (68.1%) compared with the group that did not (42.9%) (Appendix Table 2). Furthermore, the percentage of US adults aged 20 to 59 years who ever tested for HIV remained relatively stable over time for the group that reported any selected STI or HCV infection (P = 0.59), the group reporting any selected STI, without considering HCV infection (P = 0.83), and the group that reported no selected STI or HCV infection (P = 0.63) (Fig. 1 A and Appendix Table 2). Also, the percentage reporting HIV testing did not vary by type of STI reported (Fig. 1 B); however, disease-specific estimates for some individual cycles were unstable, and the confidence intervals for these estimates by year and infection type were wide (Appendix Table 2).
Figure 1: Factors associated with having ever been tested for HIV among US Adults aged 20 to 59 years who did and did not report ever being diagnosed as having a selected STI or HCV, 2005 to 2016. This figure shows select factors associated with the proportion of adults aged 20 to 59 years who completed the medical examination and self-administered risk behavior survey of the NHANES, with nonmissing data for diagnoses with selected STIs or HCV and ever testing for HIV (unweighted n = 19,102) from 2005 to 2016. Selected STIs include self-report of a diagnosis of gonorrhea or chlamydia in the past 12 months or ever being diagnosed as having herpes. From 2005 to 2012, the question about hepatitis C is “Was the test result in our letter the first time you were told you had hepatitis C?” This was asked on a follow-up survey 6 months after examination of NHANES respondents who tested anti-HCV positive or anti-HCV indeterminate but HCV RNA positive. In 2013 to 2016, the question about hepatitis C was “Has a doctor or other health professional ever told you that you have hepatitis C? (Hepatitis is a form of liver disease. Hepatitis C is an infection of the liver from the HCV).” A, The proportion reporting an HIV test for each of the 6 cycles of NHANES included in this analysis, stratified by whether or not the participant reported being diagnosed as having a selected STI or HCV. Proportions are based on the data for 19102 respondents aged 20 to 59 years who completed the NHANES medical examination between the 2005–2006 and 2015–2016 cycles with nonmissing values for selected STI and HCV variables as well as the variable for ever testing for HIV. B,The proportion reporting ever having been tested for HIV, by which selected STI or HCV they reported. Proportions are based on the data for 19102 respondents aged 20 to 59 years who completed the NHANES medical examination between the 2005–2006 and 2015–2016 cycles with nonmissing values for selected STI and HCV variables as well as the variable for ever testing for HIV. *Past 12 months. **Ever. C, The proportion of the NHANES sample (both men and women) by whether the participant reported seeing a doctor or other health care provider in the past 12 months as well as history of a selected STI or HCV. Proportions are based on the data for 19092 respondents aged 20 to 59 years who completed the NHANES medical examination between the 2005–2006 and 2015–2016 cycles with nonmissing values for selected STI and HCV variables as well as the variables for ever testing for HIV and whether or not they had seen a health care provider in the past 12months. D, Data for femaleNHANES participants and the proportion reporting ever having been tested forHIV by both history of ever being pregnant as well as history of a selected STI or HCV. Proportions are based on the data for 9699 female respondents aged 20 to 59 years who completed the NHANES medical examination between the 2005–2006 and 2015–2016 cycles with nonmissing values for selected STI and HCV variables as well as the variables for ever testing for HIV and ever or currently being pregnant.
A higher proportion of participants (both male and female) who reported a health care visit in the past 12 months and reported a selected STI or HCV infection reported having ever had an HIV test (68.8%), compared with those who reported a health care visit in the past 12 months but did not report a selected STI or HCV infection (45%) (Fig. 1 C). The group that reported neither a selected STI or HCV infection nor a visit to a health care provider in the past 12 months had the lowest percentage reporting ever being tested for HIV (34.7%; Fig. 1 C). There were a higher proportion of women who were currently or had ever been pregnant and self-reported a selected STI or HCV infection (67.1%), compared with those who were ever pregnant but did not report a selected STI or HCV infection (50.8%). A much lower proportion of women who had never been pregnant and did not self-report one of the selected infections had ever been tested for HIV (33.6%) (Fig. 1 D).
Characteristics of NHANES participants with self-reported, selected STIs or HCV infection indicate that this group is likely also at increased risk of HIV (Appendix Table 3). Among the combined 6 cycles of NHANES from 2005 to 2016, self-reported STIs or HCV infections were reported more often by women compared with men (7.0% vs. 3.4%) and non-Hispanic blacks compared with non-Hispanic whites or Hispanics (7.8% vs. 5.4%, or 3.5%). Self-reported STIs or HCV infections were also more likely to have been reported by those who had a health care visit in the past 12 months (5.8%) compared with those who did not, and ever injected drugs (17.2%) compared with those who did not inject drugs. Men who had sex with men only were more likely to report a selected STI or HCV infection than men who had sex with women only (9.8% vs. 3.4%), and men and women who self-identified as homosexual or bisexual were more likely to report a selected STI or HCV infection than those who self-identified as heterosexual (9.4% vs. 5.5%).
DISCUSSION
Findings from this analysis underscore potential missed opportunities for HIV testing in the United States. Overall, only 44.4% of the US population aged 20 to 59 years reported ever having been tested for HIV. Although the proportion reporting an HIV test was higher for the group that self-reported a selected STI or HCV infection (68.1%) compared with the group that did not (42.9%), gaps in HIV screening persist, even for those at higher risk of HIV. The factors associated with reporting a selected STI in this study highlight that more needs to be done to ensure HIV screening is conducted when testing for STIs and HCV infection. Moreover, although a higher proportion of women who had ever been pregnant and reported having had a selected STI or HCV infection had reported ever being tested for HIV, only about half of all women who had ever been pregnant and did not report a selected STI or HCV infection reported HIV testing. A lower proportion of women who had never been pregnant and did not self-report a selected STI were tested, with only 33.6% of this group reporting ever being tested for HIV. The findings on HIV testing among pregnant women indicate some progress toward the adoption of universal prenatal HIV screening in the United States, as well as the integration of HIV screening into screening and treatment services for other STIs or HCV infection; however, the overall results also indicate the missed opportunities to incorporate HIV screening into routine clinical care, even when there is no indication of HIV risk. To end the HIV epidemic in the United States, persons both with and without known indications for screening, such as pregnancy or STI or HCV infection diagnoses, will need to be tested at least once.
Increasing access to health care is an important pathway to HIV screening and diagnosis, a key strategy outlined in Ending the HIV Epidemic: A Plan for America .3 However, even among those who had seen a health care provider in the past 12 months, only 45% of those who did not self-report a selected STI or HCV reported ever being tested for HIV. Integration of routine screening into health care through existing strategies, such as electronic medical record (EMR) prompts,21,22 computerized templates, or automated reminders, may improve HIV testing rates.23 The CDC also recommends that as part of the clinical encounter, health care providers routinely obtain sexual histories from their patients and address risk reduction accordingly.7 Risk assessment of patients is an underutilized component of clinical care in the United States, and barriers such as a lack of comfort or confidence in obtaining patients' sexual history,24 the lack of risk assessment on many EMRs,22 and competing clinical priorities25 persist and can impede the ability to assess for risk and test for many infectious diseases. Normalization of HIV testing, incorporation of alerts and risk assessment in EMRs, and education of patients and providers may help promote HIV screening in clinical settings. Addressing the contextual factors that contribute to stigma and poor outcomes in the HIV care continuum could empower patients to ask for and accept an HIV test as part of their clinical care and thereby increase HIV screening in clinical settings.26
In 2015 to 2016, an estimated 90.1% of those who were told they had HCV infection had also been tested for HIV. As the opioid crisis persists in the United States, preventing the transmission of infectious diseases remains key.16,17 Injection drug use increases the risk of blood-borne infections, including HIV and HCV infection. For example, in 2015, 181 individuals in Scott County, Indiana, were diagnosed as having HIV due to injection drug use, most of whom were coinfected with HCV.27,28 Integration of HIV and hepatitis C testing services within both clinical and nonclinical care settings, including partnering with community-based organizations and public health departments, can help improve the ability to detect both HIV and HCV infections and increase access to prevention services and treatment of infectious diseases and substance use disorders.29
Limitations
This study has several limitations. First, this study analyzed cross-sectional data, so we are unable to make causal inferences. Second, the percentage of US adults with a history of STIs who had ever been tested for HIV was likely influenced by the STIs for which information was available, as NHANES does not collect data on every STI, and respondents were only asked to report chlamydia and gonorrhea diagnoses in the past year, and on ever being told that they had genital herpes. Third, having an STI was self-reported and therefore subject to recall and social desirability biases. Fourth, we might have underestimated the percentage ever tested for HIV because the HIV testing measure excluded tests other than blood tests, such as oral fluid tests. Fifth, from 2005 to 2012, our measure of ever receiving an HCV infection diagnosis only includes persons currently infected with HCV (RNA positive) who report being diagnosed and cannot be directly compared with estimates for the 2013–2014 cycles onward because of changes in the questionnaire. In addition, to produce more stable estimates, HCV was examined with STIs. Also, in 2005 to 2012, only respondents who tested HCV RNA positive (i.e., currently infected) were asked if this was the first time they were informed that they had been infected with HCV; thus, those who had been infected and resolved their infection (HCV antibody positive but HCV RNA negative) were not asked if they were aware of their prior HCV infection, further underestimating the proportion ever diagnosed as having HCV infection. Regardless of the cycle and methods for ascertaining whether a respondent had ever been diagnosed as having HCV infection, the number reporting this diagnosis was low, and including or excluding those with HCV who reported that the NHANES result was not the first time they learned of their diagnosis (2005–2012) or reported having been told of an HCV diagnosis (2013–2016) did not affect the overall proportion that reported being tested for HIV among those with other infections. Sixth, because of insufficient sample size, rates of HIV testing with and without prior STI/HCV diagnosis among those who were ever pregnant could not be assessed across each of the NHANES cycles. Seventh, hepatitis B infection was not included because awareness/diagnosis was not measured before 2013. Eighth, data on syphilis infection were not collected in the NHANES cycles reported and thus were not included in this article. Finally, the NHANES only collects data on sexual behaviors and history of STIs from survey participants aged 20 to 59 years; thus, data regarding history of diagnosis of a selected STI were unavailable for respondents outside this age range.
CONCLUSIONS
Self-reported HIV testing remains suboptimal in the United States, even among those reporting a history of receiving a diagnosis of STIs or HCV infection. Integrated screening for multiple pathogens including HIV, other STIs, and HCV infection might improve HIV testing uptake. Further research is needed to examine the feasibility of and determine the best approaches to incorporating integrated screening for multiple pathogens in clinical and nonclinical settings. To end the HIV epidemic in the United States, innovative HIV screening approaches will need to be implemented, and existing screening strategies must be scaled up. Ensuring that HIV tests are offered routinely to those receiving services for other infections with overlapping risk factors can help reduce missed opportunities for diagnosing HIV infections as early as possible and serves to promote timely linkage to PrEP or antiretroviral treatment.
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APPENDIX TABLE 1: Proportion of men and women aged 20 – 59 who have been told by a doctor or other health care professional that had a selected STI or HCV: NHANES 2005 – 2016
APPENDIX TABLE 2: Proportion of men and women aged 20 – 59 who have ever tested for HIV among those who have been told by a doctor or other health care professional that had a selected STI or HCV: NHANES 2005 – 2016
APPENDIX TABLE 3: Sociodemographic and health–related characteristics of men and women aged 20 – 59 who have ever been told by a doctor or other health care professional that had a selected STI or HCV: NHANES 2005 – 2016