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. 2022 Jul 14;17(7):e0266747. doi: 10.1371/journal.pone.0266747

Annual HIV screening rates for HIV-negative men who have sex with men in primary care

Courtney B Spensley 1, Melissa Plegue 1,2, Robinson Seda 3, Diane M Harper 1,4,5,*
Editor: Dawn K Smith6
PMCID: PMC9282649  PMID: 35834582

Abstract

Background

Men who have sex with men (MSM) account for most new HIV diagnoses in the US. Annual HIV testing is recommended for sexually active MSM if HIV status is negative or unknown. Our primary study aim was to determine annual HIV screening rates in primary care across multiple years for HIV-negative MSM to estimate compliance with guidelines. A secondary exploratory endpoint was to document rates for non-MSM in primary care.

Methods

We conducted a three-year retrospective cohort study, analyzing data from electronic medical records of HIV-negative men aged 18 to 45 years in primary care at a large academic health system using inferential and logistic regression modeling.

Results

Of 17,841 men, 730 (4.1%) indicated that they had a male partner during the study period. MSM were screened at higher rates annually than non-MSM (about 38% vs. 9%, p<0.001). Younger patients (p-value<0.001) and patients with an internal medicine primary care provider (p-value<0.001) were more likely to have an HIV test ordered in both groups. For all categories of race and self-reported illegal drug use, MSM patients had higher odds of HIV test orders than non-MSM patients. Race and drug use did not have a significant effect on HIV orders in the MSM group. Among non-MSM, Black patients had higher odds of being tested than both White and Asian patients regardless of drug use.

Conclusions

While MSM are screened for HIV at higher rates than non-MSM, overall screening rates remain lower than desired, particularly for older patients and patients with a family medicine or pediatric PCP. Targeted interventions to improve HIV screening rates for MSM in primary care are discussed.

Introduction

The incidence of HIV infection in the United States has decreased over the past decade, but the number of new infections among men who have sex with men (MSM) has plateaued around 26,000 per year [1]. In 2018, MSM accounted for 69% of all new HIV diagnoses [2]. The lifetime risk of HIV diagnosis among MSM is 88 times the risk of non-MSM.[3].

Due to the higher risk of HIV infection among MSM, frequent screening is paramount to prevention and timely treatment. Since 2006, the Centers for Disease Control (CDC) has recommended that sexually active MSM be screened for HIV at least once annually if HIV status is negative or unknown. More frequent screening is recommended for MSM with higher risk sexual behaviors [4]. As often as every 3 to 6 months, screening may be more effective in averting lifetime costs associated with HIV infection than annual screening [5].

Despite these recommendations, HIV screening remains suboptimal. The percentage of undiagnosed infections among all MSM is estimated at 15% and is much higher among young MSM [6]. Those with undiagnosed infection and those diagnosed but not receiving care are responsible for most new HIV transmissions [7]. Although 77% of MSM surveyed for National HIV Behavioral Surveillance self-reported being screened in the past year [8], a recent systematic review found that self-reported 12-month screening rates for MSM vary widely, from 40% to 71% [9]. MSM are tested in clinical settings, but these also vary widely and include primary care and specialty clinics, emergency departments, urgent care, hospitals, sexually transmitted infection (STI) clinics, and drug treatment programs, among others. The proportion of tests done by primary care providers (PCPs) is therefore unclear. In addition, among non-MSM there is always a portion who are bi-sexual, have not realized their sexual orientation, or describe their sexual orientation in other terms and would benefit from the annual HIV screening guidelines.

Previous studies have found that HIV-negative MSM with a PCP are more likely to be tested for HIV than other men [10, 11] and a majority of MSM report that their PCP is aware of their sexual orientation [12]. This suggests that PCPs are ideally positioned to improve HIV screening for MSM.

Our primary study objective was to determine medical-record verified annual HIV screening rates in primary care across multiple years for HIV-negative MSM to estimate compliance with guidelines. A secondary exploratory endpoint was to document rates for non-MSM in primary care.

Materials and methods

We performed a retrospective chart review of HIV-negative men with PCPs at Michigan Medicine. Primary care specialties were defined as family medicine, internal medicine, medicine-pediatrics, or pediatrics. Michigan Medicine primary care includes 16 clinic locations, serving three counties in Southeast Michigan. Patients included in this study were all males with no prior HIV diagnosis between 18 and 45 years who had at least one primary care encounter between March 2016 and March 2019. We chose 2016 as the index year because the question of the sexual partners’ gender became coded data elements with the clinic contact. Eligible patients were grouped based on reported sexual partners at the most recent disclosure. Individuals who reported having a male sexual partner or both a male and female partner were included in the MSM group. The non-MSM group included individuals who reported only a female partner or no partner. Patients who did not answer the question were excluded from the study. The study proposal was submitted to the Institutional Review Boards of the University of Michigan Medical School and was exempted from ongoing IRB review (HUM00155091). Individual consent was waived for this study.

Data were obtained from a computerized search of the Michigan Medicine electronic medical records (EMR) and included patient age, race, sexual partner gender, HIV test order dates, self-reported alcohol consumption, and self-reported illegal drug use, in addition to provider specialty. All HIV test orders were included for analysis, regardless of whether a result was available. For patients who did not have an HIV test ordered, we additionally searched encounter notes for the terms "HIV" and "STI" in conjunction with "counsel," "screen," and "test." The presence of these terms could indicate a pertinent discussion about testing for HIV. Annual rates of HIV screening were calculated in three 12-month time periods by counting at least one HIV test order for a unique person in that 12 -month time period divided by the identified MSM population in that same time frame. Additionally, rates of HIV discussion among MSM were similarly counted through medical note documentation for those without an HIV test order. The same procedure was completed separately for non-MSM. Chi-square tests, stratified by time period, compared HIV testing and discussion rates between MSM and non-MSM patients. A Cochran-Mantel-Haenszel (CMH) test was used to compare the difference in HIV testing and discussion rates between groups across the three time periods.

Associations with having an HIV test ordered were evaluated using a clustered logistic regression model under a Generalized Estimating Equations (GEE) framework to account for repeated measures on the same patient across time periods. Models were adjusted for age, race, substance use (alcohol and illegal drugs), provider specialty, and time period. The main covariate of interest was group (MSM vs non-MSM). Interactions between group and other variables were investigated using F-tests to evaluate their inclusion by jointly testing the significance of all parameters involved in the interaction term. To aid in the interpretation of significant interactions, marginal effects and probabilities at set levels of covariates were estimated. All statistics were performed using Stata 15.1 software.

Results

In total, 17,841 men met the criteria for inclusion over all three years. About 40% had data in all three time periods, 30% had data in two time periods, and the remaining 30% had data in only a single time period. Records identified 730 (4.1%) patients as having a male partner at some point during the study period. Compared with the non-MSM group, MSM patients were younger, were more often Hispanic, and more likely to use alcohol and illegal drugs (Table 1).

Table 1. Characteristics of MSM and non-MSM.

MSM Non-MSM p-value
(n = 730) (n = 17,111)
Age, mean(SD) 30.9 (6.8) 34.7 (6.9) <0.001
Age Group, n(%) <0.001
    18–25 180 (24.7) 2,095 (12.2)
    26–30 203 (27.8) 2,847 (16.6)
    31–35 153 (21.0) 3,719 (21.7)
    36–40 117 (16.0) 4,109 (24.0)
    41–45 77 (10.6) 4,341 (25.4)
Race, n(%) 0.67
    White 563 (78.2) 12,857 (76.3)
    Black 64 (8.9) 1,591 (9.4)
    Asian 65 (9.0) 1,624 (9.6)
    Other 28 (3.9) 773 (4.6)
Hispanic, n(%) 37 (5.1) 760 (4.6) 0.49
Female Partner ever n(%) 172 (23.6) 16,618 (97.1) <0.001
Alcohol Use, n(%) 527 (80.2) 12,101 (76.2) 0.018
Illegal Drugs, n(%) 112 (17.8) 1,726 (11.3) <0.001
IV Drugs, n(%) 1 (0.2) 12 (0.07) 0.49
Department, n(%) 0.07
Family Medicine 347 (47.5) 8,501 (49.7)
Internal Medicine 341 (46.7) 7,354 (43.0)
Internal Medicine-Pediatrics 34 (4.7) 1,111 (6.5)
Pediatrics 8 (1.1) 145 (0.9)
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Primary outcome: HIV test ordering. The HIV test ordering rates for MSM ranged between 35–43% per year, significantly higher than the 9% for non-MSM in each year (Table 2). The CMH test for homogeneity of odds ratios across the three years was not significant (p-value = 0.19), suggesting this difference in HIV test ordering rates between groups was consistent across the three time periods. For encounters that did not have an HIV test ordered, MSM encounter notes were significantly more likely to contain HIV terms than non-MSM notes, suggesting a screening discussion occurred (MSM 20% vs non-MSM 10% in each year, p-values<0.001), but, likewise, this was also not significantly different across the three years. In addition, the combined discussion of any HIV and/or STI terms in the encounter notes was not different between MSM and non-MSM over all three years CMH homogeneity test (p-value = 0.12).

Table 2. Yearly HIV test order rates and noted HIV discussion by MSM vs. non-MSM.

HIV TESTS ORDERED % (95% CI) HIV TERMS IN NOTE WITHOUT HIV TEST ORDER, % (95% CI)
MSM Non-MSM p-value MSM Non-MSM p-value
YEAR 1 N = 478 N = 11,235 N = 309 N = 10,275
3/1/16-2/28/17 35.3 (31.2, 39.8) 8.5 (8.0, 9.1) <0.001 21.4 (17.1, 26.3) 10.9 (10.3, 11.5) <0.001
YEAR 2 N = 533 N = 11,887 N = 335 N = 10,870
3/1/17-2/28/18 37.1 (33.1, 41.3) 8.6 (8.1, 9.1) <0.001 19.7 (15.8, 24.3) 10.4 (9.9, 11.0) <0.001
YEAR 3 N = 550 N = 12,394 N = 316 N = 11,277
3/1/18-2/28/19 42.5 (38.5, 46.7) 9.0 (8.5, 9.5) <0.001 20.6 (16.5, 25.4) 10.9 (10.4, 11.5) <0.001
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CMH across years for MSM was not significant for HIV tests ordered or for HIV terms in encounter notes indicating there was no difference in rates among years.

The logistic regression model did not find a significant effect of time-period on the likelihood of ordering an HIV test (Table 3). However, when adjusting for group, age, PCP department, race, alcohol and illegal drug use, all were associated with HIV test ordering. Older individuals were significantly less likely to have an HIV test ordered (aOR (95% CI) = 0.937 (0.93, 0.94)), and individuals with a history of alcohol use were more likely to have a test ordered (aOR (95% CI) = 1.18 (1.06, 1.30)). Patients of pediatricians were less likely to have an HIV test ordered compared with patients of family medicine physicians (aOR(95% CI) = 0.22 (0.12, 0.40)) and internal medicine patients were more likely than family medicine patients (aOR (95% CI) = 1.19 (1.10, 1.30)).

Table 3. GEE model results on HIV test order.

Odds Ratio 95% CI p-value
Age 0.94 [0.93, 0.94] 0.000
Department (Ref = Family Medicine)
    Internal Medicine 1.19 [1.10, 1.30] 0.000
    Internal Medicine, Pediatrics 1.06 [0.89, 1.25] 0.504
    Pedicatrics 0.22 [0.12, 0.40] 0.000
Alcohol Use (Ref = none) 1.18 [1.06, 1.30] 0.001
Drug Use (Ref = none) 1.85 [1.63, 2.10] 0.000
Race (Ref = White)
    Black 3.10 [2.72, 3.54] 0.000
    Asian 0.97 [0.81, 1.16] 0.715
    Other Race 1.34 [1.08, 1.66] 0.007
Group (Ref = Non-MSM)
    MSM 6.72 [5.74, 7.88] 0.000
Time (Ref = Year 1) 1.00
    Year 2 1.00 [0.92, 1.09] 0.971
    Year 3 1.01 [0.93, 1.10] 0.791
Group*Drug Use Interaction Term
MSM*Drug Use 0.62 [0.45, 0.85] 0.003
Group*Race Interaction Terms
MSM*Black 0.45 [0.29, 0.69] 0.000
MSM*Asian 1.29 [0.81, 2.07] 0.282
MSM*Other Race 0.85 [0.45, 1.63] 0.629
Drug Use*Race Interaction Terms
Drug Use*Black 0.70 [0.55, 0.90] 0.006
Drug Use*Asian 0.74 [0.39, 1.42] 0.368
Drug Use*Other Race 1.40 [0.86, 2.29] 0.177
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Significant group interactions were found with race (interaction F-test p-value = 0.01) and illegal drug use (interaction F-test p-value = 0.006). Within MSM patients, there were no significant differences in the likelihood of test orders based on levels of drug use or race. However, in the non-MSM group, there were both significant race and drug use effects. Fig 1 illustrates interaction results through the predicted probability of HIV tests being ordered under different levels of group, race, and self-reported illegal drug use.

Fig 1. Predicted probability of HIV test ordering by MSM v non-MSM, race, and Illegal drug use status.

Fig 1

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The probabilities of HIV test ordering estimated from regression GEE modeling were adjusted for patient age, group (MSM vs non-MSM), race, PCP department, time, alcohol use and illegal drug use. Interactions of group*race, group*illegal drug use and race*illegal drug use were included, the group*race*drug use interaction was not significant.

The MSM group had a higher probability of HIV testing being ordered, compared with non- MSM, regardless of race or illegal drug use. Within the non-MSM group, race differences were found between Black patients and both White and Asian, with Black patients having a higher probability of test ordered regardless of drug use. In all non-MSM racial groups, except Asians, there were significantly higher rates of HIV test ordering among drug users than those who self-reported no illegal drug use.

Discussion

We are the first to document medically verified HIV test ordering from a large electronic health record of patients receiving primary care that was not a short-term quality improvement project [13]. Our results of an HIV test order rate are between 35–43% for MSM, considerably lower than the CDC or USPSTF goal [1, 2, 8, 14, 15]. Others have shown that men who self-disclose MSM status are more likely to have HIV testing ordered than not [16–18]. On the other hand, among the non-MSM, we document a much higher frequency of HIV testing in our study at 9% compared with 2% in other populations of non-MSM [13].

In addition, by analyzing data over three years, we find that the HIV testing rate for MSM is consistently low, thus establishing a reliable baseline annual testing rate. These results hold even after adjusting for self-report alcohol or illegal drug use, prominent risk factors for HIV outside of sexual orientation. We are also the first to show that among those MSM without an HIV test order entered into the health system, only 20% receive HIV counseling as documented in the text of the note, severely lower than is necessary to raise awareness and identify those who could benefit [4]. These baseline testing and counseling rates are essential for future quality improvement interventions to meet CDC or USPSTF screening goals.

Our results suggest that current systems are inadequate. We hypothesize that multi-level interventions with the health system, primary care physicians, and men themselves could be necessary to increase the HIV test ordering rate. The CDC estimates that 15% of men are unaware that they have HIV, in part, because they have never been tested [19]. The portion of MSM who do not have a PCP is unknown, as many seek care through STI clinics or Emergency Departments [20]. Even with a PCP, many MSM may not disclose their sexual orientation, often due to negative experiences or perceived quality of communication [21], despite recommendations to do so [22]. Studies about physician-related barriers to care reveal that some take a complete sexual history only when relevant to the chief complaint [23]. Even if the PCP is aware of the patients’ sexual orientation, MSM-specific screening guidelines may not be known [24].

We showed that among non-MSM, HIV testing was greater among persons of color independent of self-reported alcohol and illegal drug use. These findings correlate to the successful increased public health campaigns to target Black and Hispanic men who are infected with HIV at disproportionately higher rates than White men. Despite this effort which has resulted in higher rates of HIV screening among Black and Hispanic men [11, 13, 25], no improved health outcomes have been documented from this increased testing [16]. Nevertheless, our work supports the need for universal screening to all races, potentially prompted by a best policy advisory from the EMR or national quality metrics [13, 26].

Limitations

While the medically verifiable HIV test order is a strength of this work, the self-report characteristics of sexual practice, sexual orientation, alcohol use, and illegal drug use cannot be verified and may cause misclassification of risk factors and outcome populations [27]. As we stated in the methods section, patients with missing data for a sexual partner were not included in our analysis.

Moreover, we cannot verify the veracity of what was said in the clinic visit and what the PCP documented. While all patients who identified as MSM in our study had a male sexual partner by self-disclosure at some point during the study period, it is unclear whether the PCPS were aware of this designation before the office visit. Furthermore, while a proportion of encounter notes suggest discussion of HIV for MSM who did not have a test order, we cannot verify how accurately EHR documentation reflects actual patient-provider discussions.

Methodologically, our results are not weighted by population proportions across other demographic characteristics. Therefore, we cannot generalize results to a wider population than our clinic panels.

In addition, we are not able to evaluate the barriers physicians may have encountered in offering this testing. Barriers to HIV testing, such as lack of provider comfort with discussing sexual behavior and knowledge about HIV screening and treatment, are well documented and highlight problems with screening patients based on individual risk assessment [28] reinforcing the need for universal testing.

Conclusion

While MSM are screened for HIV at higher rates than non-MSM, overall screening rates remain lower than desired, particularly for older patients and patients with a family medicine or pediatric PCP. Targeted interventions are needed to improve HIV screening rates for MSM in primary care.

Acknowledgments

We thank the Data Office for Clinical & Translational Research at the University of Michigan Medical School and especially Chiu-Mei, Jeff Cowall, and Rino Srivastava for the coding required to extract EMR data from this project.

Abbreviations

MSM

men who have sex with men (MSM)

PCP

primary care provider (PCP)

EMR

electronic medical records (EMR)

HIV

human immunodeficiency virus (HIV)

STI

sexually transmitted infection (STI)

CDC

Centers for Disease Control (CDC)

CMH

Cochran-Mantel-Haenszel (CMH) test

GEE

Generalized Estimating Equations (GEE) framework

Data Availability

Data files are available from Michigan's Deep Blue database (https://doi.org/10.7302/00fw-qr09).

Funding Statement

NCATS funding through UL1TR002240 The University of Michigan Rogel Cancer Center P30CA046592.

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Decision Letter 0

Elisa Panada

9 Dec 2021

PONE-D-21-22682Annual HIV screening rates for HIV-negative men who have sex with men in primary carePLOS ONE

Dear Dr. Harper,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The manuscript has been evaluated by two reviewers, and their comments are available below. The reviewers have raised a number of concerns that need attention. They request additional information on methodological aspects of the study, revisions to the statistical analyses and inclusion/exclusion criteria for patients. Could you please revise the manuscript to carefully address the concerns raised?

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PLOS ONE

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Reviewers' comments:

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1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: No

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

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Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Increasing rates of routine HIV screening in primary care practices is critical to ending the HIV epidemic. As such, the manuscript addresses an important issue. However, there are several points that I feel require clarification.

(1) Please provide a justification for limiting the sample to ages 18 to 45. The CDC recommendations are not limited to men in these age groups, so I see no reason not to include men of all ages. In fact, I would expect disparities in rates of testing by age to be even greater if older men had been included in the sample.

(2) Please also provide some discussion about how reliably data on sexual orientation are actually reported in the EHR. The authors do not mention any missing data on this variable, but I can't believe that there were no cases with sexual orientation excluded. Depending on the size of the sample, it may be necessary to run the analyses with three groups (MSM, non-MSM, and missing).

(3) Please reference the tables/figures in the narrative portion of the text to help guide the reader.

(4) I do not understand why the authors chose to examine the data across years. Is there any reason to expect an increase in HIV screening over the three-year period? I see no justification for that and it does not make sense to me. The question is about an individual's receipt of an HIV screening test, so I would have expected the analysis to focus at the individual level to see if any screening had occurred, controlling for the number of days/years the individual was included in the sample. Those with data across all three calendar years would have more opportunity to have a screening test than those who were in the sample for only one year. The finding of significant differences by year but no significance by the CMH test was confusing at first, because the authors provided no justification for expecting changes in screening patterns by year. The approach to analysis that I have suggested seems to me more in line with the stated objectives of the study.

(5) On a related note, in line 190, the authors note that the lack of an increasing in screening is "a disquieting finding." The low level of testing overall is certainly disquieting, but since the authors have not indicated a reason to expect an increase in annual rates of screening, this finding in and of itself is not especially "disquieting."

(6) Lines 165-166 appear to be missing something - the sentence is incomplete.

(7) The Limitations section should be expanded to include more discussion of the reliability of the methods used. Do the authors have any means to determine how regularly clinicians include in their notes discussions with patients about matters such as HIV testing, especially if the patient refused to be tested?

(8) Please provide details within the text regarding which characteristics the study's sample "matches the distribution in the state of Michigan." Is that only in regards to the percentage of men identified as MSM (4.1%) or is that across other demographic characteristics? If it is only in terms of the percentage, then the authors' claims of generalizability cannot be substantiated. It could be that the percentage is similar but that the study sample includes a higher percentage of white MSM than found in the state as a whole.

Reviewer #2: Thank you for allowing me to review your manuscript. Your research is clearly communicated and has meaningful implications to improve clinical practice. Please see a few comments/thoughts I had while reviewing.

on page 6, line 81, you mention non-MSM and state bi-sexual men. I understand those who may not be aware of their sexual identity, but was curious why you did not include bi-sexual men as MSM? Are you suggesting here that the bi-sexual men may not have engaged in a sexual encounter with another man or are you just directly placing bisexual men in a "non MSM" category?

Another question I had was the distribution of race/age based on practice setting. This is clearly not a focus of your work, but as you noted, STI clinics and ER's are frequently used sites; however, because you are the first to describe this data, did you see any associations with race/ethnicity and practice setting? Again, a question I had while reading that may have implications for clinical intervention implementation. And as a total side note, it would be interesting to see if the age/race/ethnicity/gender of the provider showed any significant outcomes.

it took me a few seconds to understand table 1, which made me wonder if it would make for a more clear presentation to have the M and SD in the column header. That is the format I think most readers are accustomed to seeing.

Finally, please consider changing your conclusions section to a Discussion, followed by your important conclusion statement. You have many important points to address and separating the discussion from your suggested conclusions may better frame the entirety of your discussion as well as making the clinical implications stand out to readers.

Thank you again for allowing me to review this manuscript. I enjoyed reading it and can clearly see the importance of this study.

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2022 Jul 14;17(7):e0266747. doi: 10.1371/journal.pone.0266747.r002

Author response to Decision Letter 0

17 Jan 2022

January 17, 2022

Elisa Panada

Associate Editor

PLoS ONE

Re: PONE-#-21-22682: Annual HIV screening rates for HIV-negative men who have sex with men in primary care https://www.editorialmanager.com/pone/default1.aspx

Dear Dr Panada,

We are happy to provide the revisions to our manuscript as requested by the reviewers.

Reviewer # 1 Response to reviewer Page

Please provide a justification for limiting the sample to ages 18 to 45. The CDC recommendations are not limited to men in these age groups, so I see no reason not to include men of all ages. In fact, I would expect disparities in rates of testing by age to be even greater if older men had been included in the sample. We thank you for this question. We agree that older men are equally important for HIV screening and would probably be even less screened than younger men, but we restricted our age range due to limited resources for data acquisition and analyst time.

-

Please also provide some discussion about how reliably data on sexual orientation are actually reported in the EHR. The authors do not mention any missing data on this variable, but I can't believe that there were no cases with sexual orientation excluded. Depending on the size of the sample, it may be necessary to run the analyses with three groups (MSM, non-MSM, and missing). Sexual orientation was determined based on the person’s response to an intake question asking them to disclose if they have a sexual partner. Data were extracted from the EHR only for patients who met the inclusion criteria of having a record of a sexual partner: male, female, none, or both. We cannot attest to the accuracy/reliability of self-disclosed sexual activity.

We acknowledge this limitation in lines 219-xxx: “Patients with missing data for sexual partner were not included in our analysis.”

methods

Please reference the tables/figures in the narrative portion of the text to help guide the reader. The table/figure references are included in the narrative portion in bolded green font.

I do not understand why the authors chose to examine the data across years. Is there any reason to expect an increase in HIV screening over the three-year period? I see no justification for that and it does not make sense to me The data were split into one year segments because the CDC recommendation is for eligible MSM to be screened at least once annually if his HIV status was negative or unknown. We used men with fixed encounter dates within 12 months to define the eligible population for screening in that year. We were able to extract the sexual orientation data for three distinct years. There was not a hypothesized change in screening rates over time; instead, we wanted to establish baseline annual screening rates, which we felt would be more accurate over a several-year period rather than a single year.

We presented the annual HIV screening rates for both MSM and non-MSM and found no difference year over year. This baseline is essential for future quality improvement projects to increase screening rates. We have added this in the discussion.

Lines 189-190: “In addition, by analyzing data over three years, we find that HIV testing rate for MSM are consistently low, thus establishing a reliable baseline annual testing rate.”

Lines 195-xxx: “These baseline annual testing and counseling rates are important to establish for future quality improvement interventions to meet CDC or USPSTF screening goals.”

The question is about an individual's receipt of an HIV screening test, so I would have expected the analysis to focus at the individual level to see if any screening had occurred, controlling for the number of days/years the individual was included in the sample. Those with data across all three calendar years would have more opportunity to have a screening test than those who were in the sample for only one year. Thank you. To clarify, analysis was performed at the person-year level. Individuals were included in each year period based on whether or not they had a record of any encounter during the time frame. If an individual did not have an encounter in a given year, they were not included in the denominator for screening rates, nor did they contribute to models for that year. Screening is meant to be done annually, and so individuals were included in each year as long as they had at least one encounter, regardless of prior screening status.

The finding of significant differences by year but no significance by the CMH test was confusing at first, because the authors provided no justification for expecting changes in screening patterns by year. The approach to analysis that I have suggested seems to me more in line with the stated objectives of the study. We have stated the purpose of CMH testing in the Methods section in lines 112-114. However, we agree with the reviewer that the interpretation of the CMH test result was not clearly stated. We have revised the results section with the following, which more appropriately points out that the test finds consistent differences between the MSM and non-MSM ordering rates across the three time periods rather than suggesting we were looking for changes in rates across time.

Lines 137-xxx: “The CMH test for homogeneity of odds ratios across the three years was not significant (p-value=0.19), suggesting this difference in HIV test ordering rates between groups was consistent across the three time periods.”

On a related note, in line 190, the authors note that the lack of an increasing in screening is "a disquieting finding." The low level of testing overall is certainly disquieting, but since the authors have not indicated a reason to expect an increase in annual rates of screening, this finding in and of itself is not especially "disquieting." We thank the reviewer and share his/her level of dissatisfaction with the wording. It is correct that we did not have reason to expect any change in rates of annual screening, as our intent was to establish baseline screening annual rates prior to initiating quality improvement interventions at our clinics. We are changing the wording to reflect that the rates did not increase over 3 years, but instead were consistent.

Lines 189-190: “In addition, by analyzing data over three years, we find that HIV testing rate for MSM are consistently low, thus establishing a reliable baseline annual testing rate.”

Lines xxx-xxx (previously 165-166) appear to be missing something - the sentence is incomplete We used a green font to highlight the table and figures. It is apparent that the green color was not visible in the reviewer’s copy of the manuscript. The sentence is complete: “Figure 1 illustrates interaction results through the predicted probability of HIV test being ordered under different levels of group, race, and self-reported illegal drug use.”

The Limitations section should be expanded to include more discussion of the reliability of the methods used.

Do the authors have any means to determine how regularly clinicians include in their notes discussions with patients about matters such as HIV testing, especially if the patient refused to be tested? This is a retrospective review of medical records, and, as has been well-established, not all information is recorded in a clinic visit that a research visit would require. We include in our methods section our process for determining how clinicians include discussion with patients about HIV testing in their notes.

Lines 104-106: “For patients who did not have an HIV test ordered, we additionally searched encounter notes for the terms “HIV” and “STI” in conjunction with “counsel”, “screen” and “test”. The presence of these terms could indicate a pertinent discussion about testing for HIV.”

Additionally, we acknowledge the limitations of documentation reliability in the limitations section beginning on line 220 and have added additional clarification as follows.

Lines 223-xxx: “Furthermore, while a proportion of encounter notes suggest discussion of HIV for MSM who did not have a test order, we cannot verify how accurately EHR documentation reflects actual patient-provider discussions.”

Please provide details within the text regarding which characteristics the study's sample "matches the distribution in the state of Michigan." Is that only in regards to the percentage of men identified as MSM (4.1 %) or is that across other demographic characteristics? If it is only in terms of the percentage, then the authors' claims of generalizability cannot be substantiated. It could be that the percentage is similar but that the study sample includes a higher percentage of white MSM than found in the state as a whole. Our results are not weighted by population proportions which would have been the more accurate way to describe generalizability of our results to others in Michigan. Therefore, we have moved this paragraph to a limitation agreeing that we cannot state these are generalizable to a wider population other than our clinic panels.

Lines 224-225: “Methodologically, while a strength of our work is that our population distribution of MSM and non-MSM matches the population distribution in the state of Michigan (MDHHS 2021), our results are not weighted by population proportions across other demographic characteristics. Therefore, we cannot generalize results to a wider population than our clinic panels.”

Reviewer # 2

on page 6, line 81, you mention non-MSM and state bi-sexual men. I understand those who may not be aware of their sexual identity, but was curious why you did not include bi-sexual men as MSM? Are you suggesting here that the bisexual men may not have engaged in a sexual encounter with another man or are you just directly placing bisexual men in a "non MSM" category? To clarify, individuals were identified as MSM in our study if they had ever indicated having a male partner, regardless of whether or not they ever had a female partner. So, in that respect we did include bi-sexual men in our MSM group. We have clarified this in the methods section.

Lines 98-xxx: “Eligible patients were grouped based on reported sexual partners. Individuals who reported having a male sexual partner or both a male and female partner were included in the MSM group. The non-MSM group included individuals who reported only a female partner and those with neither male nor female partners.”

Another question I had was the distribution of race/age based on practice setting. This is clearly not a focus of your work, but as you noted, STI clinics and ER's are frequently used sites; however, because you are the first to describe this data, did you see any associations with race/ethnicity and practice setting? Again, a question I had while reading that may have implications for clinical intervention implementation. And as a total side note, it would be interesting to see if the age/race/ethnicity/gender of the provider showed any significant outcomes We did collect data on the practice setting and on the age/race/ethnicity/gender of both the providers and patients. We agree that this would be interesting for future analysis but is beyond the scope of this initial study.

it took me a few seconds to understand table 1, which made me wonder if it would make for a more clear presentation to have the M and SD in the column header. That is the format I think most readers are accustomed to seeing. Yes, we understand that if all of the data were means and standard deviations, then the labeling would be most appropriate in the header. However, the bottom half of the table presents data in number and percent, therefore, we must keep the labeling as it is.

Finally, please consider changing your conclusions section to a Discussion, followed by your important conclusion statement. You have many important points to address and separating the discussion from your suggested conclusions may better frame the entirety of your discussion as well as making the clinical implications stand out to readers. Thank you. We agree with this reviewer’s suggestion and have changed our conclusions section to discussion and added our conclusion statement beginning on line 231.

Thank you again for allowing me to review this manuscript. I enjoyed reading it and can clearly see the importance of this study. Thank you for your kind words.

Attachment

Submitted filename: response to reviewers_MP0107_cbs edits-dmh edits.docx

Click here for additional data file. (24.4KB, docx)

Decision Letter 1

Dawn K Smith

28 Feb 2022

PONE-D-21-22682R1Annual HIV screening rates for HIV-negative men who have sex with men in primary carePLOS ONE

Dear Dr. Harper,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

ACADEMIC EDITOR:

Thank you for the responsive edits to some of the reviewer comments. However, I am requesting that you please address additional comments from Reviewer 1. With these clarifications, the paper will be reconsidered to see if it is acceptable for publication. I believe it will contribute to the important need for clinicians to do more regular HIV testing particularly for MSM and others at high ongoing risk for HIV acquisition (e.g., PWID)

Please submit your revised manuscript by Apr 14 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Dawn K. Smith

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: No

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: No

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The authors have addressed some of the questions I raised in my initial review, but a re-reading raised additional questions and some responses to earlier questions by myself and the other reviewer have not been adequately addressed.

(1) The authors have clarified the source of information regarding sexual orientation. However, there remains some confusion. Over what timeframe was the question regarding sexual partner asked? Over the past year? Lifetime? The way I have seen this question asked in a clinical setting is in regard to sexual preference (male, female, or both). Maybe that is what the authors intended to say (i.e., preference rather than "having a sexual partner" which implies that the question refers to whether or not the patient has a current sexual partner)? In any case, current sexual partner is not necessarily indicative of sexual orientation, and that should be mentioned in the Limitations section. In the Materials and Methods section, the authors state that the non-MSM group includes "those with neither male nor female partner." I'm assuming that the authors mean that the person indicated that they were not sexually active but the wording is awkward since it could be taken to mean that the patient reported sexual activity with a non-human partner. The discussion is also confusing because, in their response to reviewer comments and Discussion, the authors now state that "Patients with missing data for sexual partner were not included in our analysis." If the authors mean that a person is missing data on sexual activity, then it would be better to simply say that in the methods section. In any case, the authors should state the number of cases excluded due to missing data.

(2) How was the search of the encounter notes performed? Given the large number of encounters included in the study, I'm assuming this process was automated. The authors should provide more details regarding the methods of the search. The description is also unclear because the authors specifically reference "rates of HIV discussion among MSM." Table 2 suggests that the search was performed for all patients included in the study (i.e., including for non-MSM), but the description suggests otherwise. If the same procedure was followed for both groups (which I'm sure it was), then that should be stated clearly. Similarly, when describing the calculation of the annual testing rates, the authors only mention the calculation for MSM. For the sake of completeness, please indicate that the same procedure was completed separately for non-MSM.

(3) Table 1 as reformatted remains confusing as the table headers do not align with the columns and the p-value column appears to be missing. I disagree with the authors' statement to the second reviewer that "we must keep the labeling as it is." There are ways to improve the presentation of the data and that should be done. Tables and Figures should stand on their own, so all necessary clarifications should be made.

(4) In the first paragraph of the Results section, please take out the statement, "... consistent with state-specific data for generalizability." Per my earlier comments and the authors' acknowledgement, this statement is confusing and not valid in any case. Please also remove the reference to generalizability from the discussion section (i.e., the paragraph that starts, "Methodologically, while a strength...") or at least limit it the context of the clinical sites.

(5) In the Discussion section, the authors state, "Our results also indicate that multi-level interventions with the health system, primary care physicians, and men themselves could be necessary to increase the HIV test ordering rate." The study does not address the specific barriers to testing, so this statement (even if true) is not specifically substantiated by the study. The authors may justify this statement on the basis of other research, but not on the basis of the study as reported.

(6) Please provide the tables describing the logistic regression models. The discussion is difficult to follow without data to reference.

Reviewer #2: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2022 Jul 14;17(7):e0266747. doi: 10.1371/journal.pone.0266747.r004

Author response to Decision Letter 1

19 Mar 2022

March 10, 2022

Dawn K Smith

Academic Editor, PLOS ONE

Re: PONE-#-21-22682R1: Annual HIV screening rates for HIV-negative men who have sex with men in primary care

Dear Editor Smith,

Thank you for the opportunity to respond a second time to Reviewer #1. We apologize for any miscommunication between our responses and the understanding of our comments.

Reviewer Comment Response Page

The authors have clarified the source of information regarding sexual orientation. However, there remains some confusion. Over what timeframe was the question regarding sexual partner asked? Over the past year? Lifetime? The question that is asked of each person is “What is the sex of your partner?” and the boxes to check are one for female, one for male, and a comment box. This sexuality question is meant to be reviewed at every visit but is often answered only at the first visit. A person can check none, one, or both boxes each time the question is updated.

We have changed the sentence to say:

Eligible patients were grouped based on reported sexual partners at the most recent disclosure.

5

The way I have seen this question asked in a clinical setting is in regard to sexual preference (male, female, or both). Maybe preference rather than "having a sexual partner" question refers to whether or not the patient has a current sexual partner)? In any case, a current sexual partner is not necessarily indicative of sexual orientation, and that should be mentioned in the Limitations section.

We do not intend for the response to the question of who one has sex with to indicate sexual orientation. We define MSM literally to be men who have sex with men, not an orientation.

In the Materials and Methods section, the authors state that the non-MSM group includes "those with neither male nor female partner." I’m assuming that the authors mean that the person indicated that they were not sexually active but the wording is awkward since it could be taken to mean that the patient-reported sexual activity with a non-human partner.

Thank you for drawing this inappropriate attribution to our wording to our attention.

We have changed the sentence to read:

The non-MSM group included individuals who reported only a female partner or no partner. 5

The discussion is also confusing because, in their response to reviewer comments and Discussion, the authors now state that "Patients with missing data for a sexual partner were not included in our analysis." If the authors mean that a person is missing data on sexual activity, then it would be better to simply say that in the methods section. We have added this sentence to the methods section:

Patients who did not answer the question were excluded from the study. 5

The authors should state the number of cases excluded due to missing data. that is what the authors intended to say We apologize that this is still a confusing point in the manuscript and have attempted to clarify the text to make it more clear. We extracted data from the EHR on all eligible men who indicated being sexually active. If they were not sexually active, they would not have completed partner information and therefore not be included in the extraction. We included all men who were extracted and grouped them into either those who had some indication of a male partner vs. those who had only female or no known partner, but sexually active with humans.

How was the search of the encounter notes performed? Given the large number of encounters included in the study,

I'm assuming this process was automated. The authors should provide more details regarding the methods of the search.

We appreciate the reviewer’s concern for accuracy. We state in the methods that the terms HIV counsel…, HIV screen… HIV test… as well as STI counsel… STI screen… and STI test were programmed in the automated search. We feel that this is clear and that providing more coding detail would be confusing to the reader with no additional value. 6

The description is also unclear because the authors specifically reference "rates of HIV discussion among MSM."

Table 2 suggests that the search was performed for all patients included in the study (i.e., including for non-MSM), but the description suggests otherwise. If the same procedure was followed for both groups (which I'm sure it was), then that should be stated clearly.

As noted below, we have clarified that the same procedure was used for MSM and non-MSM by stating:

The same procedure was completed separately for non-MSM. 6

Similarly, when describing the calculation of the annual testing rates, the authors only mention the calculation for MSM. For the sake of completeness, please indicate that the same procedure was completed separately for non-MSM. Thank you. We have added this sentence:

The same procedure was completed separately for non-MSM. 6

Table 1 as reformatted remains confusing as the table headers do not align with the columns and the p-value column appears to be missing. I disagree with the authors' statement to the second reviewer that "we must keep the labeling as it is." There are ways to improve the presentation of the data and that should be done. Tables and Figures should stand on their own, so all necessary clarifications should be made We profusely apologize for Table 1. We agree that the table as presented to you was massively mis-formatted. We have corrected this issue. 7

In the first paragraph of the Results section, please take out the statement, "... consistent with state-specific data for generalizability." Per my earlier comments and the authors' acknowledgment, this statement is confusing and not valid in any case. Please also remove the reference to generalizability from the discussion section (i.e., the paragraph that starts,

"Methodologically, while a strength...") or at least limit it the context of the clinical sites We apologize. We have now removed this statement and its references from the results section and from the discussion section. 6

In the Discussion section, the authors state, "Our results also indicate that multi-level interventions with the health system, primary care physicians, and men themselves could be necessary to increase the HIV test ordering rate."

The study does not address the specific barriers to testing, so this statement (even if true) is not specifically substantiated by the study. The authors may justify this statement on the basis of other research, but not on the basis of the study as reported. We thank you for noting this obscurity. We have changed the first two sentences of this paragraph to :

Our results suggest that current systems are inadequate. We hypothesize that multi-level interventions with the health system, primary care physicians, and men themselves could be necessary to increase the HIV test ordering rate. 10

Please provide the tables describing the logistic regression models. The discussion is difficult to follow without data to

reference. We have provided Table 3 which provides the details of the logistic regression model.

We are grateful for your attention to detail and sincerely feel we have made all the changes and clarifications asked.

Sincerely,

Diane M Harper MD MPH MS

Professor

University of Michigan

Attachment

Submitted filename: response to reviewers.docx

Click here for additional data file. (18.3KB, docx)

Decision Letter 2

Dawn K Smith

28 Mar 2022

Annual HIV screening rates for HIV-negative men who have sex with men in primary care

PONE-D-21-22682R2

Dear Dr. Harper,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Kind regards,

Dawn K. Smith

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Thank you for clearly addressing the major comments from reviewers. The paper is much improved.

Reviewers' comments:

Acceptance letter

Dawn K Smith

6 Jul 2022

PONE-D-21-22682R2

Annual HIV screening rates for HIV-negative men who have sex with men in primary care

Dear Dr. Harper:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Dawn K. Smith

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    Attachment

    Submitted filename: response to reviewers_MP0107_cbs edits-dmh edits.docx

    Click here for additional data file. (24.4KB, docx)
    Attachment

    Submitted filename: response to reviewers.docx

    Click here for additional data file. (18.3KB, docx)

    Data Availability Statement

    Data files are available from Michigan's Deep Blue database (https://doi.org/10.7302/00fw-qr09).

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