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. Author manuscript; available in PMC: 2023 Jan 1.
Published in final edited form as: Subst Abus. 2022;43(1):925–931. doi: 10.1080/08897077.2021.2010257

Cervical cancer screening, abnormal results, and follow-up in women with substance use-related diagnoses

McKenna C Eastment 1, Ayushi Gupta 1, Jocelyn James 1, Barbra A Richardson 2,3, Leeya Pinder 4, H Nina Kim 1,3, Anna Wald 1, Judith I Tsui 1
PMCID: PMC9632608  NIHMSID: NIHMS1842163  PMID: 35289732

Abstract

Background:

Substance use-related diagnoses are common and associated with poor health outcomes. The objective of this analysis was to compare rates of cervical cancer screening, screening abnormalities, and follow-up care in women with and without a substance use-related diagnosis seen for primary care between 1/1/2016 and 12/31/2019 in the University of Washington healthcare system.

Methods:

This study included women aged 21–65 years of age who had at least one outpatient visit between January 1, 2016 and December 31, 2019 within one of 45 primary care or women’s health clinics in the academic healthcare system. Exposure status was defined using ICD10 codes for substance-use related diagnoses or no substance-use related diagnoses. Only first cervical cancer screening was included. Generalized linear models with a binomial family and log link were used to estimate risk ratios.

Results:

3845 women had a substance use-related diagnosis and 89214 did not. Women with a substance use-related diagnosis were less likely to be screened for cervical cancer (44%, 1675/3845) compared to women without a substance use-related diagnosis (49%, 43338/89214; relative risk [RR] 0.90, 95% CI 0.86–0.93). Women with a substance use-related diagnosis were also more likely to have an abnormal screening result (18%, 304/1675) compared to women without a substance use-related diagnosis (10%, 4528/43338; RR 1.74, 95% CI 1.56–1.93). Follow-up for abnormal screens did not differ significantly between groups (24% vs 25%; RR 0.80, 95% CI 0.55–1.17).

Conclusion:

To combat disparities in cervical cancer screening for women with substance use-related diagnoses, public health efforts should expand access to screening where women with substance use-related diagnoses are seen, including acute care, inpatient hospitalizations, and addiction treatment settings.

Keywords: cervical cancer screening, substance use-related diagnosis, women, disparities

Introduction

Substance use and substance use disorders are very common in the United States, and yet they are often overlooked as a source of adverse health consequences1. Data from the 2019 National Survey on Drug Use and Health reported 13% of Americans aged 12 and older used an illicit substance in the past month2. Individuals with substance use-related diagnoses are at increased risk for morbidity and mortality3, and are less likely to be engaged in care4. Substance use, especially illicit drug use, is a highly stigmatized condition5, 6. Perceived stigma or bias related to substance use has been associated with avoidance of interactions with healthcare providers leading to decreased healthcare utilization4. As a result, persons who use drugs are less likely to engage in primary care and more likely to rely on acute care settings7. Consequently, they may be less likely to receive routine healthcare maintenance including preventative cancer screenings.

The United States has seen a decline in cervical cancer incidence and mortality with the widespread implementation of cervical cancer screening programs8. In 2018, the age-adjusted annual incidence of cervical cancer in the US was 7.5 cases per 100,0009. However, gaps in screening remain as most women diagnosed with cervical cancer had not been screened in the preceding three to five years, which is the recommended screening interval depending on age and screening modality10. Prior research suggests that women who smoke or use other substances are less likely to be screened for cervical cancer11, 12, despite the fact that smoking is itself a risk factor for cervical cancer13–17. Additionally, women who use substances may engage in behaviors that increase their risk for human papillomavirus (HPV)18, 19 and human immunodeficiency virus (HIV), which further increase a woman’s risk of cervical cancer20. Limited data from a few studies suggest that women with a substance use-related diagnosis have higher rates of abnormal cervical screening results but may not have higher rates of cervical cancer11, 12, 21, 22. Given care-seeking barriers for women with substance use-related diagnoses, understanding their cervical cancer screening rates and outcomes remains an important public health priority23. We aimed to compare rates of cervical cancer screening, screening abnormalities, and follow-up care in a large population of women with and without a substance use-related diagnosis seen for primary care in an academic healthcare system.

Methods

Study setting, population and procedures

This study population consisted of women who had at least one outpatient visit between January 1, 2016 and December 31, 2019 within one of 45 primary care or women’s health clinics including gynecology clinics in the University of Washington (UW) Medicine academic healthcare system in the Seattle metropolitan area. They were identified using a clinical data repository of electronic health records and administrative data. Women between the ages of 21 and 65 were selected, as these were the recommended ages for cervical cancer screening during the study period24. Women who had a history of hysterectomy were excluded. This study was approved by the UW human subjects division.

Data source

Patient demographic characteristics and clinical information including pertinent visit encounters, exposure status, pathology reports, laboratory results, and procedure codes were extracted electronically as a deidentified dataset from the clinical data repository from two hospital systems and from 45 clinics.

Exposure and outcome measures

The primary exposure was having at least one or more substance use-related diagnosis. Women were assigned an exposure status if they met criteria to be included in the study population. Substance use-related diagnoses were defined using only International Classification of Diseases, 10th Edition (ICD10) codes for opioid-related disorders, cocaine-related disorders, other stimulant-related disorders, other psychoactive substance abuse, inhalant use/abuse, sedative/hypnotic/anxiolytic abuse, hallucinogen abuse, cannabis use, and alcohol abuse/misuse (Appendix 1), similar to other studies25–27. Nicotine-related disorders were not included in the exposed category for the primary analysis. Codes related to remission or cessation of substance use were not used as this analysis focused on active use. Overdose and toxic ingestion were also not included in these analyses because of a lack of detail for the specific substance used and intent of use in many of these ICD10 codes. The primary outcomes were receipt of cervical cancer screening identified through cytology reports (from Papanicolaou smears) and HPV test results, an abnormal cervical cancer screening result, and in cases of abnormal screening results, follow-up testing or procedures. An abnormal cervical cancer screening result was defined using cytology reports characterized using the Bethesda Criteria: high-risk HPV positive (types 16, 18, 31, 33, 35, 39, 45, 51, 56, 58, 59, 69), atypical squamous cells of undetermined significance (ASC-US), atypical squamous cells, cannot exclude HSIL (ASC-H), low-grade squamous intraepithelial lesion (LSIL), high-grade squamous intraepithelial lesion (HSIL) and squamous cell carcinoma. Follow-up was defined as any second Papanicolaou (pap) smear result, any second HPV result, or a procedure code indicating colposcopy, Loop Electrosurgical Excision Procedure (LEEP), cryotherapy, biopsy, ablation, or surgical removal (Appendix 2) within the study period.

Covariates included age, race (White, Black or African American, Asian, American Indian or Alaska Native, Native Hawaiian or Pacific Islander, Multiple races), ethnicity (Hispanic or Latino, not Hispanic or Latino), insurance status (self-pay or charity, Medicare/Medicaid, private, other, missing), number of outpatient visits, nicotine use, HIV status, hepatitis C status, and hysterectomy status. HIV status was classified using a published algorithm that includes laboratory results, medications, and ICD codes28. Hepatitis C status was defined as positive if reactive antibody test and/or detectable hepatitis C RNA was present at any point in the patient’s medical record, and otherwise was classified as negative. Hysterectomy was identified using both diagnosis codes (Z90.710) and procedure codes (Appendix 2).

Statistical analysis

For women with more than one cervical cancer screening encounter during the analysis, only the first screening event was included in these analyses. Patient demographic and clinical characteristics were summarized using descriptive statistics. Multiple imputation was used to fill in missing data on race and ethnicity. The primary analysis of the study was the unadjusted association between substance use-related diagnoses and the three outcomes (receipt of cervical cancer screening, an abnormal screening result, and follow-up for those with an abnormal screening result). Generalized linear models with a binomial family and log link were used to estimate risk ratios and 95% confidence intervals. Our chosen primary outcomes were the unadjusted analyses since our intent was simply to describe any existing disparities. However, adjusted analyses were also conducted to account for potential confounding; variables were selected a priori based on known and hypothesized associations with substance use and outcomes and included age, race, ethnicity, HIV status, nicotine use, and insurance status. Multiple sensitivity analyses were conducted. The first tested the association between polysubstance use (defined as having more than one ICD10 code for a substance use-related diagnosis) and our outcomes. The second examined the association between substance use dependence ICD10 codes (indicative of a moderate or severe use disorder) and our outcomes. The third excluded cannabis use and alcohol use in the substance use exposure group to understand the associations between illicit substances and study outcomes. The fourth sensitivity analysis included nicotine use in the exposure category of substance use-related diagnoses and examined associations with our study outcomes.

Stata version 17 was used for analyses29.

Results

A total of 94,416 women aged 21–65 years of age seen at least once in a primary care or women’s health clinic were identified; 4818 (5%) were excluded because of a history of hysterectomy (5.2% among women with a substance use-related diagnosis v. 2.3% among those without a substance use-related diagnosis), leaving 93,059 women in the analysis. Of this group, 3,845 (4%) women had a substance use-related diagnosis recorded by ICD10 and 89214 (96%) did not. Polysubstance use was common: including alcohol, 80% (3096/3845) of the subsample had evidence of polysubstance use. Restricting to non-alcohol and nicotine substances, still 80% (1969/2473) met criteria for polysubstance use. The majority of women (55%) were between 21–39 years of age. Overall, 69% of women were White and 8% Hispanic or Latina (Table 1). Black women were over-represented among the group of women with a substance use-related diagnosis, compared to those who did not have a substance use-related diagnosis (15% vs 8%). Overall, private insurance was most common (46%). However, in women with a substance use-related diagnosis self-pay or charity (40%) and Medicare/Medicaid (34%) coverage were most common. Women with a substance use-related diagnosis had on average twice the number of outpatient visits in the system compared to women without a substance use-related diagnosis (12 versus 6). Nicotine use was captured more often in women with a substance use-related diagnosis than in women without a substance use-related diagnosis (34% versus 1%). A higher proportion of women with a substance use-related diagnosis had HIV (9%) and hepatitis C infections (17%) than women without a substance use-related diagnosis (1% for both infections).

Table 1.

Demographics and clinical characteristics of 93059 women with and without a substance use-related diagnosis who are eligible for cervical cancer screening

Variable All women
N=93059
N(%) or Mean (SD)		 With substance use-related diagnoses
N=3845
N (%) or Mean (SD)		 Without substance use-related diagnosis
N=89214
N (%) or Mean (SD)
Age (years)
 21–39 51000 (55%) 1772 (46%) 49228 (55%)
 40–49 17384 (19%) 755 (20%) 16629 (19%)
 50–59 16117 (17%) 913 (24%) 15204 (17%)
 60–65 8558 (9%) 405 (11%) 8153 (9%)
Race
 White 54988 (69%) 2730 (74%) 52258 (69%)
 Black or African American 6873 (9%) 564 (15%) 6309 (8%)
 Asian 14206 (18%) 141 (4%) 14065 (19%)
 American Indian or Alaska Native 966 (1%) 145 (4%) 821 (1%)
 Native Hawaiian or Pacific Islander 777 (1%) 27 (1%) 750 (1%)
 Multiple races 1419 (2%) 104 (3%) 1315 (2%)
Ethnicity
 Hispanic or Latino 6062 (8%) 230 (6%) 5832 (8%)
 Not Hispanic or Latino 71937 (92%) 3456 (94%) 68481 (92%)
Insurance status
 Self-pay or charity 35020 (38%) 1556 (40%) 33464 (38%)
 Medicare/Medicaid 10739 (12%) 1301 (34%) 9438 (11%)
 Private 43216 (46%) 706 (18%) 42510 (48%)
 Other 3268 (4%) 179 (5%) 3089 (3%)
 Missing 816 (1%) 103 (3%) 713 (1%)
Number of outpatient visits 6 (7.6) 12 (15.5) 6 (6.9)
History of substance use 1
 Opioid use 1207 (1%) 1207 (31%)
 Cocaine use 408 (0.4%) 408 (11%)
 Other stimulant use 614 (0.7%) 645 (17%)
 Cannabis use 1120 (1%) 1211 (31%)
 Alcohol abuse/dependence 1511 (2%) 1568 (41%)
 Other use2 417 (0.5%) 417 (11%)
Nicotine use 2601 (3%) 1303 (34%) 1298 (1%)
HIV status
 Positive 1332 (1%) 328 (9%) 1004 (1%)
 Negative 91727 (99%) 3517 (91%) 88210 (99%)
Hepatitis C status
 Positive 1754 (2%) 644 (17%) 1110 (1%)
 Negative 91305 (98%) 3201 (83%) 88104 (99%)
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1

These categories are not mutually exclusive and were determined using ICD10 codes listed in Appendix 1.

2

Includes inhalant abuse, sedative/hypnotic/anxiolytic abuse, hallucinogen abuse

Among women with a substance use-related diagnosis, 44% (1675/3845) received cervical cancer screening at least once in the study period, whereas among women without a substance use-related diagnosis, 49% (43,338/89,214) received screening, corresponding to a relative risk [RR] of 0.90 (95% confidence interval [CI] 0.86–0.93). The results were similar after adjustment for age, race, ethnicity, HIV status, nicotine use, and insurance status (adjusted RR [aRR] 0.96, 95% CI 0.92–1.00).

Women with a substance use-related diagnosis were more likely to have an abnormal cervical cancer screening result compared to women without a substance use-related diagnosis (18%, 304/1675, in women with a substance use-related diagnosis compared to 10%, 4528/43338, in women without a substance use-related diagnosis). The two most common positive screens were high-risk HPV DNA positivity and atypical squamous cells of undetermined significance (ASC-US) (Figure 1). Only one woman in the cohort had cervical cancer. Women with a substance use-related diagnosis had a higher relative risk of an abnormal screening result compared to women without a substance use-related diagnosis (RR 1.74 95% CI 1.56–1.93). This association was similar after adjustment for age, race, ethnicity, HIV status, nicotine use, and insurance (aRR 1.38 95% CI 1.22–1.56).

Figure 1.

Figure 1.

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Proportions of ‘positive cervical cancer screening’ by type of result in women with and without a substance use-related diagnosis. Women can be included in two categories if they have both abnormal pathology in addition to being high risk HPV DNA positive. Solid lines represent binomial 95% confidence intervals

Documented follow-up within the healthcare system after an abnormal screening result was similar in women with and without a substance use-related diagnosis (24% vs 25%, respectively) in both unadjusted (RR 0.91 95% CI 0.72–1.16) and adjusted analyses (aRR 0.91 95% CI 0.70–1.18).

Sensitivity analyses

The first sensitivity analysis examined the association between polysubstance use and receipt of cervical cancer screening, positive screen, and follow-up. The findings were similar to our primary analyses. Women with polysubstance use were less likely to be screened for cervical cancer compared to women without a substance use-related diagnosis in unadjusted analyses (RR 0.93 95% CI 0.89–0.98). These results were not statistically significant in our adjusted analyses (aRR 0.99 95% CI 0.94–1.04). In women who were screened for cervical cancer, those with polysubstance use were more likely to have a positive screen compared to women without a substance-use related diagnosis in both unadjusted (RR 1.80 95% CI 1.56–2.06) and adjusted analyses (aRR 1.34 95% CI 1.14–1.58). Among those with a positive cervical cancer screen, there was no difference in follow-up between women with polysubstance use and women without a substance use-related diagnosis.

The second sensitivity analysis examined the association between substance dependence and the cervical cancer care cascade. The results were similar to our primary analysis. Women with substance dependence were less likely to be screened for cervical cancer (RR 0.89 95% CI 0.86–0.92) and more likely to have a positive screen compared to women without substance-use related diagnoses (RR 1.75 95% CI 1.57–1.94). The results were similar in adjusted analyses and remained statistically significant. There was no difference in follow-up for a positive screening result in women with substance dependence and women without substance use-related diagnoses.

In our third sensitivity analysis, we redefined substance use as illicit substances and thus excluded cannabis use and alcohol use. With this modified definition, our findings were similar to our primary analyses, but demonstrated more substantial disparities. Women with a substance use-related diagnosis were less likely to be screened for cervical cancer compared to women without a substance use-related diagnosis in both unadjusted (RR 0.75 95% CI 0.71–0.80) and adjusted analyses (aRR 0.80 95% CI 0.75–0.85). In women who were screened for cervical cancer, women with a substance use-related diagnosis were more likely to have an abnormal screening result compared to women without a substance use-related diagnosis in both unadjusted (RR 1.73 95% CI 1.48–2.02) and adjusted analyses (aRR 1.20 95% CI 1.01–1.43). There were no differences in follow-up for women with an abnormal screening result for women with a substance use-related diagnosis compared to women without a substance use-related diagnosis (RR 0.80 95% CI 0.55–1.17; aRR 0.73 95% CI 0.48–1.11).

In our fourth sensitivity analysis, nicotine-related disorders were included in the exposure category and associations with our outcomes were assessed. The results did not differ significantly with the primary analyses. Those with substance use-related diagnoses including nicotine use were less likely to be screened for cervical cancer (RR 0.89 95% CI 0.87–.92), more likely to screen positive among those who were screened (RR 1.71 95% CI 1.56–1.88), and just as likely to follow-up if they had a positive result (RR 0.98 95% CI 0.81–1.17) compared to women without substance use-related diagnoses.

Discussion

Our study found that women with a substance use-related diagnosis were somewhat less likely to have cervical cancer screening completed and yet substantially more likely to have an abnormal screening result compared to women without a substance use-related diagnosis. We did not observe any difference in the relative risk of having follow-up for an abnormal screening result between the two groups. While adjustment was performed for potential confounders, our primary analysis of unadjusted risk ratios better highlights the disparities in women with a substance use-related diagnosis.

Similar to our study, a large study of Medicaid enrollees in Maryland demonstrated lower cervical cancer screening rates in women with substance use disorders compared to women without substance use disorders11, although the authors did not find any differences in genital cancers between the two groups. In our study, only one woman had cervical cancer, but we did find a much higher risk of an abnormal cervical cancer screening result in women with a substance use-related diagnosis. Other smaller studies have found low screening rates in women in drug treatment programs21, and on opioid replacement therapy30. The finding of lower screening rates in women with substance use disorders could be related to stigma and avoidance of healthcare providers outside of emergency needs4, 7, or lower uptake of screening because of higher rates of intimate partner violence, sexual trauma and/or competing priorities31. It is important to note that many people with substance use disorders may not regularly attend primary care visits and the disparities presented here could be underestimates. This analysis captured only women who were already engaged in care and it does not account for the population of women without documented outpatient clinic visits. However, while women with substance use-related diagnoses had twice the number of outpatient visits as women without substance use-related diagnoses and twice the number of opportunities for screening, the screening rates were still lower. Given the evidence of disparities in cervical cancer screening among women with a substance use-related diagnosis, public health efforts should explore alternative care models, such as HPV testing using self-swabbing and screening in alternative settings such as addiction treatment programs or during inpatient hospitalizations. Screening programs also need to implement trauma-informed care for this marginalized and vulnerable population of women32.

Women with substance use-related diagnoses had higher risk of abnormal screens compared to women without a substance use-related diagnosis though cervical cancer did not differ between groups. This has been seen in the literature previously and may be related to behaviors that increase risk of HPV and HIV11, 12, 21, 22. Public health messaging that emphasizes these increased risks of cervical dysplasia may help address these findings.

Our study did not find differences in follow-up rates for abnormal screening results in women with and without substance use-related diagnoses. However, we used a very liberal definition of follow-up and did not restrict this follow-up to recommended time intervals. Despite this liberal definition, follow-up rates were low in both groups of women and may be explained by women seeking care outside of this system. In addition, follow-up for women who had an abnormal screen may have been missed if their positive screen was near the end of the study period, though we expect that this would be the same for both populations of women. This is the first study to our knowledge documenting cervical cancer screening follow-up in this population.

There are study limitations to note. The use of ICD10 codes for capturing substance use-related diagnoses are based on older terms of “abuse” and “dependence”, and do not map on to the current terminology of mild, moderate or severe substance use disorder as recommended by the 5th edition of Diagnostic and Statistical Manual of Mental Disorder (DSM-V)33. Particularly in the case of opioids, this could lead to misclassification of a substance use disorder for individuals who had physical dependence to prescribed opioids27, 34, 35. Thus, having a substance-related diagnosis may not equate with having a substance use disorder. Research suggests that substance use disorders are underdiagnosed which could have led to under-ascertainment of our exposure. In theory, these misclassifications of the exposure in both directions should bias to the null, which gives greater weight to our findings26, 36. Next, characterization of substance use included the whole spectrum of substances, from cannabis and alcohol to heroin, and did not differentiate frequency, patterns, routes, or severity of use. A sensitivity analysis was conducted that showed similar, even stronger, associations for all the primary outcomes when only examining illicit substances and excluding cannabis and alcohol use. Also, a sensitivity analysis that redefined our exposure variable to individuals with a diagnosis code for “dependence”, which could indicate a moderate to severe use disorder, showed similar results, as did the analysis that examined individuals with polysubstance use defined as having more than one substance use-related diagnosis code.

Given how we defined our study population and the time period, another limitation is that some women were included in the study because they had an outpatient visit prior to Dec 31, 2019 but were not able to accrue follow-up. While this could lead to an under-ascertainment of receipt of pap smear and follow-up, we would not expect the under-ascertainment to be different between the exposed and unexposed women. Lastly, we limited our cohort to women with at least one outpatient primary care visit and only captured outpatient clinic screening results, which may have led to under-ascertainment of our outcomes as well as restriction to women who were at least partially engaged in care. Within our cohort overall, we found lower cervical cancer screening rates than what has been reported by the Centers for Disease Control24, which could indicate incomplete capture of results.

Despite these limitations, this study had a number of strengths. These include a very large sample size including multiple clinics across a large academic health system, accurate assessment of endpoints with the use of pathology reports, and the ability to capture many other important demographic and clinical characteristics to better understand the population of women being examined.

Conclusions

In this study, women with substance use-related diagnoses were less likely than women without substance use-related diagnoses to receive cervical cancer screening and more likely to have an abnormal result when screened. To combat disparities in cervical cancer screening for women with substance use-related diagnoses, public health efforts should expand access to screening where women with substance use-related diagnosis are seen, including acute care, inpatient hospitalizations, and addiction treatment settings.

Supplementary Material

Supp 1

Table 2.

Association between substance use-related diagnosis and cervical cancer screening, positive cervical cancer screening result, and follow-up for positive cervical cancer screening results in those with documented substance use-related diagnosis compared to those without

With substance use-related diagnosis
N (%)		 Without substance use-related diagnosis
N (%)		 Unadjusted RR (95% CI) p-value Adjusted RR1 (95% CI) p-value
Cervical cancer screening completed 1675/3845 (44%) 43338/89214 (49%) 0.90 (0.86–0.93) <0.001 0.96 (0.92–1.00) 0.04
Positive screen among those screened 2 304 (18%) 4528 (10%) 1.74 (1.56–1.93) <0.001 1.38 (1.22–1.56) <0.001
Follow-up among those with a positive screening result 3 72 (24%) 1110 (25%) 0.91 (0.72–1.16) 0.5 0.91 (0.70–1.18) 0.5
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Abbreviations: RR=Risk ratio, CI=Confidence Interval

1

Adjusted for age, race, ethnicity, HIV status, nicotine use, and insurance

2

Positive screen includes high-risk HPV DNA positive, atypical squamous cells of undetermined significance (ASCUS) low-grade squamous intraepithelial lesion (LSIL), atypical squamous cells, cannot rule out HSIL (ASC-H), high-grade squamous intraepithelial lesion (HSIL), malignant neoplasm of cervix uteri

3

This includes any follow-up procedure (pathology report or HPV test or procedure code) following a positive screen

Acknowledgments:

We would like to acknowledge Emily Ford, MD, for her assistance with the dataset formatting.

Financial Support:

MCE received support from NIH NCI K08CA228761. Research reported in this manuscript was supported by the University of Washington / Fred Hutch Center for AIDS Research, an NIH-funded program under award number AI027757 which is supported by the following NIH Institutes and Centers: NIAID, NCI, NIMH, NIDA, NICHD, NHLBI, NIA, NIGMS, NIDDK. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of Interest:

The authors have no conflicts of interest to report. Anna Wald received research funding from NIH, Sanofi and GSK and is a consultant for Aicuris, X-Vax, Gilead, and Crozet; she also serves on a DSMB for Merck.

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