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Sex Differences in Treatment Strategies Among Patients With Ulcerative Colitis

A Retrospective Cohort Analysis of Privately Insured Patients

Sceats, Lindsay A., M.D.1; Morris, Arden M., M.D., M.P.H.1; Bundorf, M. Kate, Ph.D., M.B.A, M.P.H.2; Park, K.T., M.D., M.S.3; Kin, Cindy, M.D., M.S.1

Diseases of the Colon & Rectum: May 2019 - Volume 62 - Issue 5 - p 586–594
doi: 10.1097/DCR.0000000000001342
Original Contribution: Inflammatory Bowel Disease
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BACKGROUND: Sex-based treatment disparities occur in many diseases. Women undergo fewer procedural interventions, and their care is less consistent with guideline-based therapy. There is limited research exploring sex-based differences in ulcerative colitis treatment. We hypothesized that women are less likely to be treated with strategies consistent with long-term disease remission, including surgery and maintenance medications.

OBJECTIVE: The aim of this study was to determine if patient sex is associated with choice of treatment strategy for ulcerative colitis.

DESIGN: This is a retrospective cohort analysis.

SETTING: Data were gathered from a large commercial insurance claims database from 2007 to 2015.

PATIENTS: We identified a cohort of 38,851 patients newly diagnosed with ulcerative colitis, aged 12 to 64 years with at least 1 year of follow-up.

MAIN OUTCOME MEASURES: The primary outcomes measured were the differences between male and female patients in 1) rates and types of index ulcerative colitis operations, 2) rates and types of ulcerative colitis medication prescriptions, and 3) rates of opioid prescriptions.

RESULTS: Men were more likely to undergo surgical treatment for ulcerative colitis (2.94% vs 1.97%, p < 0.001, OR 1.51, p < 0.001). The type of index operation performed did not vary by sex. Men were more likely to undergo treatment with maintenance medications, including biologic (12.4% vs 10.2%, p < 0.001, OR 1.22, p < 0.001), immunomodulatory (16.3% vs 14.9%, p < 0.001, OR 1.08, p = 0.006), and 5-aminosalicylate medications (67.0% vs 63.2%, p < 0.001, OR 1.18, p < 0.001). Women were more likely to undergo treatment with rescue therapies and symptomatic control with corticosteroids (55.5% vs 54.0%, p = 0.002, OR 1.07, p = 0.002) and opioids (50.2% vs 45.9%, p < 0.001, OR 1.17, p < 0.001).

LIMITATIONS: Claims data lack clinical characteristics acting as confounders.

CONCLUSIONS: Men with ulcerative colitis were more likely to undergo treatment consistent with long-term remission or cure, including maintenance medications and definitive surgery. Women were more likely to undergo treatment consistent with short-term symptom management. Further studies to explore underlying mechanisms of sex-related differences in ulcerative colitis treatment strategies and disease trajectories are warranted. See Video Abstract at

1 S-SPIRE Center, Department of Surgery, Stanford University, Stanford, California

2 Stanford University, Department of Health Research and Policy, Stanford, California

3 Inflammatory Bowel Disease Center, Department of Pediatrics (Gastroenterology), Stanford University, Stanford, California

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Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML and pdf versions of this article on the journal’s Web site (

Funding/Support: Women & Sex Differences in Medicine Seed Grant (Stanford University).

Financial Disclosures: None reported.

E-Poster presentation at the meeting of the American Society of Colon and Rectal Surgeons, May 19 to 23, 2018, Nashville, TN.

Correspondence: Cindy Kin, M.D., M.S., Stanford University, Department of Surgery, 300 Pasteur Dr, H3680K, Stanford, CA 94305. E-mail:

See “Editorial,” on page 517.

An increasing body of research suggests that women experience sex-based disparities in medical treatment across a variety of diseases. In many cases, treatment patterns for women deviate from guideline-indicated treatment, leading to poorer outcomes. This pattern has been demonstrated in diabetes mellitus,1,2 cardiovascular disease,3,4 stroke,5 and some cancers, including colorectal malignancies.6 Other studies have suggested that women are less frequently offered invasive procedural interventions,7–13 although they are more likely to seek preventative care.14,15

There is limited research exploring sex-based disparities in ulcerative colitis (UC) treatment, and data that do exist come primarily from single-site or small multi-institutional studies. These limited data suggest the possibility of treatment differences by sex, leading to differences in outcomes. A previous multicenter study showed that women with IBD received fewer immunomodulatory medications than men, and that men had significantly higher remission rates. After controlling for the type of medication prescribed, sex differences in remission rates vanished,16 suggesting that, when women are treated appropriately with guideline-based therapy, their outcomes are similar to men. In our prior work, we found that young male patients were more likely than older men or women of any age to undergo surgical treatment for UC.17 To date, there are very few population-level data examining the nature and magnitude of sex-related differences in UC treatment.

The objective of this study was to determine the relationship between sex and medical and surgical treatment strategies for UC on a population level. We hypothesized that women are less likely than men to undergo treatment with strategies consistent with long-term disease remission, including immunomodulatory and/or biologic medications and definitive surgical resection.

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Study Design

We performed a retrospective cohort analysis of patients with newly diagnosed UC by using the 2007 to 2015 Truven MarketScan database. This database contains deidentified patient-level information from inpatient, outpatient, and pharmaceutical claims on 40 to 50 million privately insured patients per year. These claims originate from >150 large employer-sponsored health plans and include patients from all 50 states. The database includes demographic characteristics (ie, age, sex, geographic region), encounter data (ie, hospital admissions, outpatient visits, and associated procedures), pharmaceutical data (ie, medications, days supply, dose dispensed, strength, and administration method), and financial data (ie, total cost, copayment, deductibles). This study was exempt from full review by the Stanford University Institutional Review Board.

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We identified a cohort of patients aged 12 to 64 newly diagnosed with UC between 2008 and 2014 (Fig. 1). We defined a new diagnosis of UC as a patient with 1) ≥2 inpatient or outpatient encounters with a primary diagnosis of UC within 1 year (International Classification of Diseases, Ninth Revision (ICD-9) codes 556.xx and International Classification of Diseases, Tenth Revision (ICD-10) codes K51.xx), 2) ≥1 lower endoscopy within 6 months of the index UC encounter, and 3) no UC-related medication prescriptions within 12 months before the index UC encounter. We required at least 2 encounters on separate dates with a primary diagnosis of UC to exclude those whose single UC encounter may represent a spurious diagnosis. Because tissue or endoscopic evidence is necessary to definitively diagnose UC, we excluded patients without lower endoscopy within 6 months of the index UC encounter. We required patients to be continuously enrolled for at least 12 months before the index UC encounter and for at least 12 months afterward to ensure adequate lead-in and follow-up time. We also excluded patients with claims for UC medications within 1 year before diagnosis, because UC-related visits or lower endoscopies in these patients may indicate disease exacerbations rather than new diagnoses. We followed patients longitudinally during their enrollment period to assess time from diagnosis to treatment with UC medications and/or index UC operation.



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Variable Classification

We identified patients who underwent an index UC operation (total abdominal colectomy, total proctocolectomy with ileostomy, or total proctocolectomy with ileal pouch) using Current Procedural Terminology codes, ICD-9, and ICD-10 procedure codes (Appendix 1, Supplemental Digital Content, We measured UC medication use by identifying outpatient pharmaceutical claims or Healthcare Common Procedure Coding System/ J-codes for biologic medications (infliximab, adalimumab, certolizumab pegol, golimumab, natalizumab, vedolizumab, and ustekinumab), corticosteroids (prednisone, prednisolone, prednisolone sodium phosphate, methylprednisolone sodium succinate, hydrocortisone sodium succinate, hydrocortisone, methylprednisolone, budesonide, and hydrocortisone acetate), immunomodulatory medications (azathioprine, mercaptopurine, methotrexate, methotrexate sodium, cyclosporine, and tacrolimus), and 5-aminosalicylates (mesalamine, sulfasalazine, olsalazine sodium, and balsalazide sodium). We assessed opioid prescriptions by using outpatient pharmaceutical claims with therapeutic class 60 (opiate-containing medications) (Appendix 2, Supplemental Digital Content,

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The primary outcomes of interest were UC-related medical and surgical treatments, based on pharmaceutical claims and inpatient claims for index UC operations. For surgical treatment, we assessed the type of operation performed and time between diagnosis and surgery. For medical treatment, we assessed types of prescriptions filled and time between diagnosis and medication initiation. Each medication class was assessed individually, irrespective of the other medications used by the patient. For time-to-event analyses, the first medication prescription for each event class was considered the event of interest.

To determine whether sex differences are influenced by women’s concerns over reproduction, we conducted secondary sensitivity analyses of women past usual reproductive age (defined as ≥45 years) and men ≥45 years to assess for differences in treatment strategies by age. The age of 45 years was chosen given the Centers for Disease Control and Prevention definition of usual reproductive age.18 Given previously described risks of methotrexate on sperm counts and birth defects, we also conducted a subgroup analysis of methotrexate use in men <45 years. Finally, we conducted a post hoc analysis comparing differences in health care utilization by men and women to determine whether treatment differences could be influenced by the rate at which care was accessed. We assessed mean number of annual outpatient visits, mean number of emergency department visits, and mean number of hospitalizations (both for UC and for any cause). We additionally assessed specialty providers accessed for care, including internal medicine physicians, gastroenterologists, surgeons, and psychiatrists.

The primary independent variable of interest was sex. Covariates adjusted for in multivariate analysis included age group, geographic region, insurance plan type, and grouped Charlson comorbidity index score (calculated using inpatient and outpatient claims from the 12-month lead-in period). These were chosen both for their clinical significance as well as their statistical significance in bivariate analysis.

We used χ2 tests to compare binary differences by sex in medical and surgical treatment, as well as frequency and type of health care utilization. We used total time at risk of undergoing surgery to calculate incidence rates of UC surgery. We used multivariate logistic regression to estimate the association between sex, surgical treatment, and treatment with UC medications while controlling for covariates. Multivariate regression was also used to determine adjusted ORs of seeing specialty medical providers. We used Kaplan-Meier time-to-event analyses to compare time-to-surgery and time-to-medication from index UC diagnosis between men and women. We used χ2 tests and Student t tests to compare categorical and continuous demographic variables (Stata v14.2; College Station, TX).

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After applying inclusion criteria (Fig. 2), we identified 38,851 patients with a new diagnosis of UC, 52% of whom were female (Table 1). Women were slightly older (mean age 43 vs 42.1 years, p < 0.001) and slightly more likely to have comorbidities (grouped Charlson comorbidity index 0.64 vs 0.61, p < 0.001) than men. Most patients had exclusive provider organization/preferred provider organization insurance. The smaller proportion of the cohort diagnosed in the study’s later years reflects the lower number of overall covered lives contained in the database during these years; the overall proportion of patients diagnosed with UC each year was constant. Patients were followed for different amounts of time after UC diagnosis relative to the availability of claims data and their continued enrollment in a participating insurance plan. The mean duration of follow-up after UC diagnosis was 3.30 years (range 1–8 years), which did not differ by sex.





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Surgical Treatment of UC

Men were 50% more likely to undergo surgical treatment for UC than women (2.94% vs 1.97%, p < 0.001) (Table 2). There was no difference by sex in the type of operation performed. Use of laparoscopic versus open surgery did not significantly differ by sex (men 55.4% vs women 44.7%, p = 0.17). Men had a higher incidence rate of surgery than women (5.2 vs 3.5 UC surgeries per 1000 person-years; data not shown). The effect of sex persisted after adjusting for covariates, including age group, geographic region, insurance plan type, and grouped Charlson comorbidity index score (OR, 1.51; 95% CI, 1.32–1.73; p < 0.001) (Appendix 3, Supplement Digital Content, In Kaplan-Meier time-to-event analysis, men progressed to surgery more quickly than women (Fig. 3A).





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Medical Treatment of UC

Maintenance Medications

Men were significantly more likely than women to be prescribed medications used for maintenance therapy including biologic (12.43% vs 10.19%, p < 0.001), immunomodulatory (16.30% vs 14.86%, p < 0.001), and 5-aminosalicylate medications (66.96% vs 63.21%, p < 0.001) (Table 3). Men were significantly more likely than women to be treated with biologic (OR, 1.22; 95% CI, 1.14–1.30; p < 0.001), immunomodulatory (OR, 1.08; 95% CI, 1.02–1.14; p = 0.006), and 5-aminosalicylate medications (OR, 1.18; 95% CI, 1.13–1.23; p<0.001) in multivariate analysis (Appendix 4, Supplement Digital Content, Men started biologic, immunomodulatory, and 5-aminosalicylate medications significantly earlier than women (Figs. 3B–D).



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Rescue and Palliative Medications

Women were significantly more likely to be prescribed corticosteroids (55.53% vs 53.99%, p = 0.002) as well as opioids (50.23% vs 45.86%, p < 0.001) (Table 3). After adjusting for covariates, male sex remained protective against treatment with corticosteroids (OR, 0.93; 95% CI, 0.90–0.98; p = 0.002) and opioids (OR, 0.85; 95% CI, 0.82–0.89; p<0.001) (Appendix 4, Supplement Digital Content, Mean number of opioid prescriptions for women was significantly higher than for men (3.73 prescriptions vs 2.73, p < 0.001).

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Medical and Surgical Treatment of UC in Patients Past Usual Reproductive Age

Sex differences in surgical treatment persisted among women past the usual reproductive age. Compared with men ≥45 years old, women ≥45 years old were less likely to undergo surgical treatment for UC (1.82% vs 2.44%, p = 0.002). The positive effect of male sex persisted in this older age group in multivariate analysis (OR, 1.29; 95% CI, 1.04–1.58; p = 0.02) (Appendix 5, Supplement Digital Content, Women ≥45 years old progressed more slowly to surgery compared with their male peers in time-to-event analysis (Fig. 4).



Sex differences in maintenance medical treatment also persisted in an age-stratified analysis. Women past usual reproductive age underwent treatment with biologic medications less frequently than their male peers (6.19% vs 8.12%, p < 0.001) and were less likely to be treated with 5-aminosalicylates (57.40% vs 62.12%, p < 0.001). The positive effect of male sex persisted in multivariate analysis (biologics: OR, 1.35; 95% CI, 1.20–1.52; p < 0.001; 5-aminosalicylates: OR, 1.24; 95% CI, 1.17–1.32; p < 0.001) (Appendix 6, Supplemental Digital Content, Young men <45 years old used methotrexate at a rate equivalent to their female counterparts (2.13% vs 2.06%, p = 0.72).

Finally, differences in rescue medication treatment persisted in the age-stratified cohort. Women remained more likely to undergo treatment with corticosteroids than their male peers (51.34% vs 49.46%, p = 0.01). Male sex remained protective against corticosteroid treatment in multivariate analysis (OR, 0.92; 95% CI, 0.87–0.98; p = 0.02).

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Health Care Utilization

In a post hoc analysis, we assessed sex differences in health care utilization. Women with UC were more likely to access the health care system for any reason compared with men. Women were more likely to visit the emergency department during their enrollment (50.2% vs 46.8%, p < 0.001; OR, 1.15; 95% CI, 1.10–1.20; p < 0.001) or to be hospitalized for any reason during their enrollment (33.2% vs 26.8%, p < 0.001; OR, 1.38; 95% CI, 1.31–1.44; p < 0.001). Women had a higher mean number of annual outpatient visits (12.2 vs 9.1 visits, p < 0.001). However, when we assessed health care utilization specific to UC, this pattern changed. Men had slightly higher mean annual UC-related outpatient visits (3.0 vs 2.7, p < 0.001), whereas women were very slightly more likely to visit the emergency department for UC (9.1% vs 8.6%, p = 0.12; OR, 1.08; 95% CI, 1.01–1.16; p = 0.04). Men and women were equally likely to be hospitalized for UC (15.4% vs 15.1%, p = 0.49; OR, 1.04; 95% CI, 0.98–1.10; p = 0.20).

Men and women sought care from specialist providers at different rates. Both men and women were very likely to seek care from internal medicine physicians and gastroenterologists. Women were very slightly more likely to see an internal medicine physician compared with men (88.7% vs 87.4%, p < 0.001; OR, 1.13; 95% CI, 1.06–1.20; p < 0.001). There were no differences in rates of gastroenterologist consultation after adjusting for covariates (80.6% vs 79.6%, p = 0.02; OR, 1.05; 95% CI, 0.99–1.11; p = 0.06). Although they underwent less surgical therapy for UC, women were more likely to seek consultation with a colorectal or general surgeon (27.3% vs 23.5%, p < 0.001; OR, 1.22; 95% CI, 1.16–1.28; p < 0.001). Women were also more likely to seek care from a psychiatrist than men (9.9% vs 6.1%, p < 0.001; OR, 1.39; 95% CI, 1.28–1.50; p < 0.001).

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We found persistent differences in treatment patterns between men and women with UC. Men were more likely than women to undergo treatment aligned with longer-term disease maintenance or surgical cure. Men were more likely to undergo treatment to proactively manage disease, whereas women were more likely to undergo treatment to reactively manage symptoms, specifically, corticosteroids and narcotic pain medication.

It is particularly interesting that women undergo less surgical therapy for UC than men, even though they are more likely to undergo surgical consultation. The underlying reasons behind this discrepancy beg further investigation. Are female patients counseled by surgeons to defer or avoid surgery, or is it a patient-driven decision? Several factors may influence patient and provider choices regarding surgery. Prior studies have described a 20% to 30% increased risk of female infertility after restorative proctocolectomy and ileal pouch.19,20 It is possible that risk aversion toward postoperative infertility may drive female patients and providers away from proctocolectomy. However, a subgroup analysis of women ≥45 years showed that low rates of surgery persisted for women after usual reproductive age. Women may have increased concerns about postoperative body image related to stomas and scarring compared with men. A Dutch study showed that women undergoing open restorative proctocolectomy have a lower postoperative body image score than men.21

Sex-specific differences in UC medications are harder to explain, given that nearly all UC medications are considered safe even during pregnancy. In this study, the largest differences by sex included 1) biologic medications, 2) 5-aminosalicylates, and 3) opioids. Women were slower to start biologic medications than men, potentially indicating delay in initiation or reluctance in treatment. There is no evidence that biologic medications are teratogenic, so women are encouraged to continue biologic medications while pregnant or breast-feeding.22 For other medications considered in our analysis, 5-aminosalicylates have been shown to affect fertility in men but not women,23 yet men were more likely to take these drugs than women. Methotrexate has been associated with birth defects, pregnancy loss, and azoospermia,24 yet our analysis suggests that men and women <45 years take methotrexate at equivalent rates.

The difference in rates of opioid prescription is especially concerning, because this could serve as an indicator of poorly treated disease requiring more pain control. Differences in opioid prescription rates disappear for patients ≥45 years, suggesting that sex differences in opioid prescription exist primarily in younger patients. Prior studies have investigated sex differences in pain reporting and seeking pain relief, as well as the psychogenic attributions providers may make regarding pain in female but not male patients.25 It is possible that female patients’ reports of pain could result in an attempt by providers to deal with the symptom instead of prompting a more in-depth exploration of potentially inadequate disease control.26

The current study has limitations related to its retrospective nature and use of a commercial claims database. Databases built on billing codes rely on the accuracy of coding by physicians to obtain the correct diagnoses and procedures. For this reason, we required stringent enrollment criteria including ≥2 encounters with a primary diagnosis of UC, lower endoscopy, and lengthy pre- and postdiagnosis periods to ensure that those captured would represent a patient with newly diagnosed UC as accurately as possible. Despite this, the mean duration of follow-up is 3.3 years, with a maximum follow-up of 8 years. A longer duration of follow-up would provide additional information regarding long-term treatment choices and the consequences of the treatment differences noted here. In addition, the database used for this analysis contains no clinical or laboratory data to address questions of disease severity (such as frequency of bowel movements, bleeding, and nutritional status) that may influence patient and provider decisions regarding treatment strategy. The ability to statistically adjust for or match on clinical and laboratory markers of disease severity (including endoscopy reports, number of bloody bowel movements, hemoglobin, albumin, C-reactive protein, and fecal calprotectin) would strengthen our conclusion that sex alone is driving the treatment differences noted here. Thus, it is possible, albeit unlikely, that men described in this analysis may have more severe UC and thus undergo more medical and surgical treatment. This data set also does not reliably capture whether a surgery was completed on an elective or emergent basis; accordingly, we have refrained from commenting about sex differences in the urgency of surgical treatment.

The magnitude of treatment differences by sex noted here are small, and, if present for a single medication or treatment option, would likely bear little clinical significance despite strong statistical significance. However, the remarkable consistency across a variety of treatment classes in this large population study suggests a small but important sex-based treatment bias. Similar patterns exist for female patients with other diseases, including receiving less care consistent with guideline-indicated therapy and decreased likelihood of undergoing procedural interventions,7–13 which further strengthens this conclusion. It is critical for providers caring for patients with UC to recognize that sex-based treatment preferences exist, and to appropriately explore these preferences in their own patients. It is also important to remain vigilant to the possibility of misattribution of symptoms (for example, to gynecological issues). Providers and patients should engage in shared decision making to achieve satisfactory clinical outcomes using treatment methods acceptable to patients.

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In summary, our study is the largest population-level study describing treatment differences by sex for patients with UC. We found that men are more likely than women to receive treatment consistent with long-term disease remission or cure. Further work is necessary to understand the implications of sex-driven treatment differences on UC outcomes and to identify the underlying reasons for these treatment differences. Understanding patient- and provider-level drivers of these differences requires a qualitative or mixed-methods approach. Exploring the decision-making process of male and female patients with UC choosing between different treatment options may provide additional insight. Interviewing providers who care for patients with UC may reveal different methods of counseling used for male versus female patients.

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Data for this project were accessed using the Stanford Center for Population Health Sciences Data Core. The PHS Data Core is supported by a National Institutes of Health National Center for Advancing Translational Science Clinical and Translational Science Award (UL1 TR001085) and from internal Stanford funding. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. This work was also supported by a National Institutes of Health National Center for Advancing Translational Science, Clinical and Translational Science Award (KL2TR001083 and UL1TR001085). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Additional support came from The Donna and Frederick Fleugel Colorectal Surgery Fund, and from a seed grant from Women & Sex Differences in Medicine (Stanford University).

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Sex differences; Inflammatory bowel disease; Medical therapy; Surgery; Ulcerative colitis

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