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Rates of Primary and Secondary Syphilis Among White and Black Non-Hispanic Men Who Have Sex With Men, United States, 2014

Grey, Jeremy A. PhD*; Bernstein, Kyle T. PhD, ScM; Sullivan, Patrick S. DVM, PhD*; Kidd, Sarah E. MD, MPH; Gift, Thomas L. PhD; Hall, Eric W. MPH*; Hankin-Wei, Abigail MD; Weinstock, Hillard S. MD, MPH; Rosenberg, Eli S. PhD*

JAIDS Journal of Acquired Immune Deficiency Syndromes: November 1, 2017 - Volume 76 - Issue 3 - p e65–e73
doi: 10.1097/QAI.0000000000001508
Epidemiology
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Background: Men who have sex with men (MSM) in the United States experience an approximately 100-fold greater rate of primary and secondary (P&S) syphilis diagnoses compared with men who have sex with women only. As in the general population, racial/ethnic disparities in P&S syphilis diagnosis rates may exist among MSM, but MSM-specific P&S syphilis rates by race/ethnicity are unavailable. We enhanced a published modeling approach to estimate area-level MSM populations by race/ethnicity and provide the first estimates of P&S syphilis among black and white non-Hispanic MSM.

Methods: We used data from the American Community Survey (ACS), published findings from the National Health and Nutrition Examination Survey (NHANES), and national syphilis surveillance data to estimate state-level rates of P&S syphilis diagnoses among MSM, overall and for black and white non-Hispanic MSM. We also used variability around ACS and NHANES estimates to calculate 95% confidence intervals for each rate.

Results: Among 11,359 cases of P&S syphilis among MSM with known race/ethnicity in 2014, 72.5% were among white (40.3%) or black (32.2%) MSM. The national rate of P&S syphilis diagnosis was 168.4/100,000 for white MSM and 583.9/100,000 for black MSM. Regional rates for black MSM ranged from 602.0/100,000 (South) to 521.5/100,000 (Midwest) and were consistently higher than those for white MSM.

Conclusions: Although white MSM accounted for more P&S syphilis diagnoses than black MSM in 2014, when evaluating diagnoses based on rate per 100,000, black MSM had consistently and markedly higher rates than white MSM, with the highest impacted states located in the US South.

Supplemental Digital Content is Available in the Text.

*Department of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA;

Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, GA; and

Department of Emergency Medicine, Emory University School of Medicine, Atlanta, GA.

Correspondence to: Jeremy A. Grey, PhD, 1600 Clifton Road, MS E63, Atlanta, GA 30329-4027 (e-mail: yej7@cdc.gov).

This effort was supported by Cooperative Agreement Number 5U38PS004646 by the National Center for HIV, Viral Hepatitis, STD and TB Prevention (NCHHSTP), Centers for Disease Control and Prevention, as part of the NCHHSTP Epidemiologic and Economic Modeling Cooperative Agreement.

The authors have conflicts of interest to disclose.

The findings and conclusions in this manuscript are those of the authors and do not necessarily represent views of the Centers for Disease Control and Prevention.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.jaids.com).

Received March 21, 2017

Accepted July 07, 2017

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INTRODUCTION

Syphilis is a sexually transmitted bacterial infection with broad implications for individual health, public health, and preventive medicine. Clinically, syphilis is classified into several stages; the primary and secondary (P&S) stages of syphilis suggest more recent infection and are often used in surveillance to represent acute infections.1 Left untreated during these earlier stages, clinical manifestations of syphilis include cardiovascular and neurological morbidity as well as pregnancy complications, such as stillbirth, low birth weight, prematurity, and congenital anomalies.1 Syphilis has also been shown to increase the risk of transmission and acquisition of HIV.3

Rates of reported P&S syphilis declined to historic lows in the 1990s, leading to optimism about the potential for syphilis elimination in the United States, a goal highlighted in the 1999 National Plan for the Elimination of Syphilis.4 However, since 2001, the national rate of syphilis began rising, and rates of P&S syphilis have increased almost every year, nearly quadrupling between 2001 and 2015 (from 2.1 to 7.5 cases per 100,000 in 2015).1 The increases in syphilis rates have occurred predominantly among men across all categories of age and race/ethnicity, with the largest increases noted among men who have sex with men (MSM).1,4 Thus, further understanding of the racial, sexual, and geographic disparities in syphilis transmission should guide programs and policies aimed at reducing transmission of syphilis and addressing disparities in diagnosis rates.1,5

The epidemiology of P&S syphilis throughout the United States highlights the heterogeneity of the epidemic. Although P&S syphilis increases have been seen across many states and regions, state-level variation in case numbers is an important dimension of the syphilis epidemic. For example, there was nearly a 150% increase in diagnoses of P&S syphilis in California from 2006 (5.1/100,000) to 2015 (12.6/100,000), which exceeded the national rate increase during the same period (3.3–7.5/100,000, a 127% increase).1,6 Surveillance reports have shown that syphilis rates across the US population also show marked disparities by race/ethnicity, with diagnosis rates 5 times higher among black non-Hispanic men (39.0/100,000) compared with white non-Hispanic men (7.6/100,000) in 2015.1

Nationally, MSM experience an approximately 100-fold greater rate of P&S syphilis diagnoses compared with men who have sex with women only,7 although MSM rates of P&S syphilis among racial/ethnic groups have not been possible. We recently developed a modeling approach for estimating numbers of MSM in US counties and states, as described by Grey et al.8 This approach was used to update national estimates7 and provide the first state-specific estimates of P&S syphilis burden among MSM in 2015.9 Here, we extend this methodology to estimate area-level MSM populations by racial/ethnic groups. We synthesize this information to provide the first estimates of P&S syphilis by race/ethnicity—specifically black and white non-Hispanic men—among MSM in the United States. This delineation of P&S syphilis rates by racial/ethnic groups of MSM by state is a critical step in understanding the social determinants of syphilis and other sexually transmitted disease risk disparities in the United States.7

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METHODS

MSM Population Denominators

We estimated race/ethnicity-specific numbers of adult MSM in each state using an updated version of our previously published method.8 In brief, the previous method adjusted published estimates of the percentage of adult men who are MSM, both nationally7 and by its urban–rural classification10 (also called “urbanicity”)11 according to each US county's concentration of households headed by a male with a male partner. The number of total households and male–male households in counties was obtained from the American Community Survey (ACS).12 A county's weighted percentage of MSM among adult men (age 18 and older) was based on the ratio of the county's percentage of male–male households among all households to the percentage of male–male households among all counties at the same level of urbanicity. Thus, counties with greater than expected density of male–male households were estimated to have more MSM, whereas counties with less density of male–male households were estimated to have fewer MSM. The percentages from NHANES that were reported by Oster et al11 were multiplied by this ratio to obtain an adjusted percentage of MSM among adult men. Thus, the final estimates of MSM population size were determined by multiplying the adjusted percentage by the number of adult men in the county according to the current population estimates from the US Census Bureau. The number of MSM in states and metropolitan statistical areas was then calculated by summing county-level MSM population estimates.

For the analysis presented here, we modified the previously published model by incorporating the estimates by Oster et al11 of the percentage of MSM among adult men within the 4 US regions. Consequently, the new estimates take into account the county's density of male–male households relative to all counties at the same level of urbanicity and within the same region. This modification was made to reduce errors due to regional differences in same-sex cohabitation or reporting of male–male households to the US Census Bureau. In addition, we updated the previous estimates to represent 2014 by incorporating data from the ACS 2010–2014 summary files.12

After determining each county's estimated number of MSM according to the new method, we estimated the number of MSM within each racial/ethnic category according to the racial/ethnic distribution of adult men residing in that county. Here, we assume that the racial/ethnic distribution of the adult MSM population in a given county reflects the communities in which they reside.7

In addition to revising the method for estimating overall MSM populations at the county level, we estimated confidence intervals (CIs) around our state-level point estimates of MSM population size, which we did not include in our previous work.8 These CIs took into account variability in the data sources by sampling from distributions around each estimate. For the data from the ACS summary files, we used margin of error files provided by the US Census Bureau for the 90% CIs for each variable. We also used published 95% CIs for the estimates published by Purcell et al7 and Oster et al.11 Thus, using randomly drawn parameters from the distributions around these key model parameters, we performed our estimation method 100,000 times.

The values we report are the medians across the 100,000 results. The 95% CIs represent the values at the 2.5th and 97.5th percentiles around the race/ethnicity-specific national and area-specific estimates of MSM populations' sizes. These CIs for the number of MSM were carried forward as denominators to yield CIs for MSM P&S syphilis rates by area and race/ethnicity.

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P&S Syphilis Cases

To calculate rates, we used state-level diagnoses of P&S syphilis (“cases”) reported to the CDC by jurisdictions as part of the National Notifiable Diseases Surveillance System. Case reports include information on sex, race/ethnicity, and sex of partners—“male,” “female,” or “both male and female.” The completeness of surveillance reporting for these data varies by state, however. In 2014, the percentage of unknown race/ethnicity ranged from 0% in 14 states (Alaska, Delaware, Indiana, Iowa, Kentucky, Michigan, North Carolina, Oklahoma, South Carolina, South Dakota, Utah, Vermont, Virginia, and West Virginia) to 31.3% (Maine).13 The percentage of unknown sex of partners in the 49 states that reported those data ranged from 1.2% (South Carolina) to 80.9% (Delaware).13

Because diagnosis data among MSM are limited to cases for which all relevant data are reported, previous CDC reports have suppressed MSM-specific data for states in which data about sex of partners were reported on fewer than 70% of P&S syphilis cases.13 For our 1-year cross-sectional analysis, we expand this criterion to retain states with data on sex of partners from at least 50% but fewer than 70% of cases, but we report them separately. We fully suppressed data from states with less than 50% reporting of sex of partners for cases. Furthermore, states and state-by-race/ethnicity strata with fewer than 5 cases were suppressed to protect privacy. Those with 5 or more cases but less than 12 were reported, but rates were excluded because of instability.14 Suppressed states, those with low reporting of sex of sex partners, and cases with missing race/ethnicity information contributed to regional and overall estimates. Because of low case counts in the majority of states for other races and ethnicities, we limited presented P&S syphilis rates to 3 groups: (1) MSM of all race/ethnicities, (2) black non-Hispanic MSM, and (3) white non-Hispanic MSM.

For rates, we divided the P&S syphilis case counts by the overall estimated number of MSM as well as the estimated number of MSM among each racial/ethnic category. Rates were calculated this way for each of the 100,000 iterations of the estimation method to determine the 95% CIs around each value. Thus, variation in the rates represents variability in the denominator estimates; the case counts do not vary.

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RESULTS

The estimated number of non-Hispanic black and white MSM and the total number of MSM in 2014 are summarized by US region, division, and state in Table 1. (Estimates for all races/ethnicities according to the enhanced methodology are provided in Supplemental Digital Content Table 1, http://links.lww.com/QAI/B74. Ratios of the upper and lower confidence bounds, which provide a standard way to examine variability in the estimates across race/ethnicity, are provided in Supplemental Digital Content Table 2, http://links.lww.com/QAI/B74.) We estimated 4.64 million MSM in 2014 (95% CI: 4,165,934 to 5,174,979). On examining non-Hispanic black and white MSM, regional differences were apparent. The South had the largest absolute populations of both black (351,185; 95% CI: 266,440 to 448,993) and white (984,093; 95% CI: 746,228 to 1,260,888) MSM, and the South had a larger percentage of all black MSM in the United States (56.2%; 95% CI: 45.9 to 65.9) compared with white MSM (36.2%; 95% CI: 27.8 to 45.5). California had the largest population of white MSM (311,012; 95% CI: 214,325 to 432,827) in the country but only the fourth-largest population of black MSM (44,226; 95% CI: 30,266 to 62,032). Three states had larger populations of black MSM than California, all of them in the South: Texas (63,590; 95% CI: 47,043 to 83,610), Florida (62,477; 95% CI: 47,143 to 80,519), and Georgia (46,540; 95% CI: 34,691 to 60,840).

TABLE 1-a

TABLE 1-a

TABLE 1-b

TABLE 1-b

We present the number and rates of reported P&S syphilis cases among adult MSM in 2014, by state and race/ethnicity, in Table 2 (states with sex partner information reported for at least 70% of cases) and Table 3 (states with at least 50% but less than 70% of sex partner information reported; rates are underestimated rates and should be examined with caution). In 2014, 11,711 cases of P&S syphilis were reported among adult MSM in the United States, yielding a rate of 252.3 cases per 100,000 MSM. California had the highest reported number of cases among MSM at 2244 (19% of cases), whereas Idaho, Maine, Montana, North Dakota, South Dakota, and Vermont each reported fewer than 12 cases among MSM. The top 5 highest rates were in South Carolina (545.7/100,000), Mississippi (539.3/100,000), Louisiana (527.2/100,00), Nevada (493.6/100,000), and Georgia (443.8/100,000, with 50%–70% known partner sex). At the Census region level, rates ranged from 200.8/100,000 in the Midwest to 271.1/100,000 in the West, with the largest number of cases (4625) in the South.

TABLE 2-a

TABLE 2-a

TABLE 2-b

TABLE 2-b

TABLE 3

TABLE 3

Of the 11,359 cases of P&S syphilis among MSM reported in 2014 for whom race/ethnicity were known (11,359/11,711, or 97.0% of all MSM cases), 8240 (72.5%) were among non-Hispanic white or black MSM. White MSM represented 40.3% of all reported MSM cases with known race/ethnicity (4580/11,359) and black MSM represented 32.2% (3660/11,359). Among all states with sufficient data, rates for black MSM exceeded those for white MSM, with overall national rates of 583.9/100,000 among black MSM and 168.4/100,000 among white MSM. The rates among black MSM were consistently high across regions, from a high of 602.0/100,000 in the South to a low of 521.5/100,000 in the Midwest, with substantial variation between states. The highest rate was in South Carolina (1398.1/100,000), with additional rates above 1000.0/100,000 in Georgia, Mississippi, Nevada, and Pennsylvania. Among white MSM, the variation in rates was lower, from a low of 140.5/100,000 in the Midwest to a high of 168.3/100,000 in the Northeast. The highest rate was 359.0/100,000 in Nevada, and Arizona, California, Louisiana, Rhode Island, and South Carolina also had rates above 250.0/100,000.

Figures 1 and 2 display maps of the distribution of P&S syphilis rates among all MSM and among only white MSM and only black MSM, respectively, using decile cut-points. The maps underscore our finding that isolating state rates of P&S syphilis among MSM by race category significantly reduce the variation in rates by geographic location. When mapping P&S syphilis cases among all MSM, regardless of race/ethnicity, the highest rates are concentrated in a distinct band across the US South. By contrast, when rates among black and white MSM are disaggregated and viewed on separate maps, the most notable feature is the lower rates of syphilis among white MSM (35 of 41 states with sufficient data for white MSM are in the lower 5 deciles), and the uniformly higher rates of syphilis among black MSM (29 of 30 states with sufficient data for black MSM are in the top 5 deciles), across most of the United States.

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

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DISCUSSION

We present an enhancement to our previous methodology, enabling estimation of the sizes of race-specific populations of MSM by state across the United States, and providing a clearer picture of the variation in distribution of the MSM population across the United States by race and ethnicity. Using these revised estimates of the MSM population distribution in the United States, we were then able to use syphilis case surveillance data to present the first-ever state-by-state estimates of P&S syphilis rates among non-Hispanic black and white MSM. Compared with heterosexual males, MSM in the United States are disproportionately burdened by syphilis.9 Our analysis further shows that among the MSM population, there are additional racial/ethnic disparities. Across all the states examined, irrespective of the relative size of the MSM population, black MSM had significantly higher risks of P&S syphilis compared with white MSM.

The most recent report of MSM-specific syphilis rates used data from 2008.7 Between 2008 and 2014, our data show a 63.8% increase in P&S syphilis among MSM overall (154–252.3/100,000), a 65.4% increase among non-Hispanic black MSM (353–583.9/100,000), and a 115.9% increase among white MSM (78–168.4/100,000).7 Although percentage increases in P&S syphilis rates were higher among white MSM, absolute rate increases were higher among black MSM. Thus, these data reinforce the need to have population-specific interventions among MSM.

Although a critical finding from our data is the systematically higher rates of syphilis among black MSM, our state-by-state findings highlight areas where rates among black MSM are particularly elevated; for example, the P&S syphilis rate in Georgia, Mississippi, and South Carolina each represent a 2-fold or greater rate than the national P&S syphilis rate among black MSM, and are nearly 10-fold the syphilis rate for MSM overall. When comparing these rates with the overall national syphilis surveillance rate of 7.5 cases per 100,000 US adults, these disparities and the vulnerability of the black MSM population in the South are further underscored.1 In the West, South, and Northeast, the P&S syphilis epidemics for white MSM are more uniform and less concentrated in the South. These racially specific and different geographic patterns can inform national, state, and regional approaches to sexually transmitted disease control.

The P&S syphilis racial/ethnic disparities can help inform local program planning and development of syphilis education and prevention interventions. The data presented here underscore the need to develop a more lucid local epidemiology of P&S syphilis, including greater attention to collecting and reporting comprehensive data regarding sexual history and sex of sex partners. Local and state health departments may need to explore whether prevention approaches for MSM may differ by racial/ethnic group. Of importance, the methodology presented will allow for continual updates as new surveillance and census data become available, allowing the public health understanding of US syphilis rates and subpopulation disparities to evolve as new data become available.

The findings presented here illustrate the importance of surveillance methodologies for accurately estimating population denominators, such as developing accurate estimates of state- and county-level MSM populations by race across the United States. In deepening our understanding of disease risk and transmission in the United States, these denominator estimates can be as important as accurate case surveillance. For example, in Nevada, only 40 cases of P&S syphilis were reported among black MSM in 2014 compared with 359 cases among white MSM. Yet, the race-specific rates of P&S syphilis were estimated to be 1058.5/100,000 and 252.0/100,000 for black and white MSM, respectively. In this example, the burden of disease is considerably higher for black MSM compared with white MSM. Also, the rate ratio for black MSM compared with white MSM was 4.2, whereas the case ratio was 9, suggesting the magnitude of racial/ethnic disparities may also differ when rates are compared rather than absolute case counts.

The results of our model rely on the accuracy of the ACS data,12 the published NHANES estimates,7,11 and the surveillance data that were available. Consequently, there are several ways in which our findings and estimates are limited by those data. First, because of small cell sizes and resultant instability of rate estimates, we were unable to establish P&S syphilis rate estimates for racial and ethnic groups other than non-Hispanic white and black MSM. In some areas, this limitation may result from very small population sizes of some MSM groups, whereas in other populations the model was limited by suppression of data in states where a significant proportion of P&S syphilis surveillance is lacking information about sexual behavior. As a result, important subpopulation disparities in P&S syphilis may be missed in this analysis, such as Hispanic or Asian MSM. However, the methodology presented can be applied to state- and county-level data by state and local health departments where sufficiently stable rate estimates can be calculated. Finally, in states where sex of sexual partner or race/ethnicity was not collected for all cases of P&S syphilis, rates are likely underestimated. Although it is unlikely that the missing data would be skewed sufficiently to alter our finding of significant racial disparities in P&S syphilis infection rates, the implications of this missing data highlight the importance of accurate and complete disease surveillance reporting from state and local health departments.

Beyond the data and parameters used in our estimation method, we assumed that the racial distribution of MSM follows racial distribution of adult men in the county, as reported by census data. Although there is no reason to expect that this assumption is erroneous in a manner that would alter the P&S syphilis rate disparities in a systematic fashion, absent a large-scale population-based study, it is impossible to know if there may be some areas of the country where this assumption leads to a racial distribution that is not fully representative of the population in question. However, given the very marked and consistent racial disparity in P&S syphilis rates observed in this study, it is unlikely that this association could be fully or largely explained by an error in this assumption.

We estimated race/ethnicity-specific rates of reported P&S syphilis among MSM in the United States, by state of residence. Although white MSM account for the more cases than black MSM, when evaluating diagnoses based on rate per 100,000, black MSM had consistently and markedly higher rates (eg, 583.9/100,000 nationally) than white MSM (eg, 168.4/100,000 nationally), with the highest impacted states located in the US South. This first-ever publication of state-level rates of P&S syphilis among MSM help state and local public health departments to better understand the populations' disparities and public health needs within the communities they serve, as well as underscoring the importance of ensuring complete and accurate surveillance collection data to drive data-based public health planning.

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ACKNOWLEDGMENTS

The authors thank the Applied Public Health Advisory Group, a collaborative set of state and local public health professionals convened for this project, for their guidance and expertise. They specifically thank Taylor Wimbly for her assistance with formatting tables and Thomas Bertrand, Mary Ann Chiasson, Gregory Felzien, Jane Kelly, and Katie Moore for reviewing this paper and providing feedback.

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REFERENCES

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9. de Voux A, Kidd S, Grey JA, et al. State-specific rates of primary and secondary syphilis among men who have sex with men—United States, 2015. MMWR Morb Mortal Weekly Rep. 2017;66:349–354.
10. Ingram DD, Franco SJ. 2013 NCHS urban–rural classification scheme for counties. Vital Health Stat. 2014;2:1–73.
11. Oster AM, Sternberg M, Lansky A, et al. Population size estimates for men who have sex with men and persons who inject drugs. J Urban Health. 2015;92:733–743.
12. US Census Bureau. American Community Survey 5-Year Summary File, 2010–2014. US Census Bureau; 2015. Available at: https://http://www.census.gov/programs-surveys/acs/technical-documentation/summary-file-documentation.2014.html.
13. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2014. Atlanta, GA: Centers for Disease Control and Prevention; 2015.
14. AIDSVu. Data methods—state/county. 2016. Available at: https://aidsvu.org/data-methods-statecounty/. Accessed January 22, 2017.
Keywords:

syphilis; primary and secondary syphilis; men who have sex with men; population estimation; health disparities

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