Association of surgeon−patient sex concordance with postoperative outcomes following complex cancer surgery

Sex concordance may impact the therapeutic relationship and provider−patient interactions. We sought to define the association of surgeon−patient sex concordance on postoperative patient outcomes following complex cancer surgery.


| INTRODUCTION
5][6][7][8] Many factors can contribute to the provider−patient relationship including communication style, as well as the ability to cultivate trust and confidence. 2 Our own group previously reported that patients consider several factors when choosing a cancer surgeon. 94][15][16][17][18][19] In turn, the predominance of male physicians in surgery may carry implications for the ability of patients to choose sex-concordant providers, as well as impact provider−patient interactions and healthcare outcomes. 14,161][22][23][24] For example, Anderson et al.
reported lower use of screening mammography among female patients who were treated by male primary care physicians. 22milarly, Frant et al. noted that female physicians referred patients more often for counseling about unhealthy behaviors than male colleagues. 25Sex based differences have also been identified in the perioperative setting. 1,20,26,27Etherington et al. reported on sex/ gender differences related to processes of care and clinical outcomes in cardiac operative care. 27In this systematic review, patients treated by female versus male surgeons had a lower 30-day mortality.A separate study, which looked at 1.3 million adult patients in Canada over a 12-year period, reported that women were 15% more likely to suffer a complication, 11% more likely to require readmission, and 32% more likely to die when operated on by a male doctor rather than a female doctor. 1 Of note, among patients undergoing common elective or emergent surgical procedures, sex discordance between surgeons and patients negatively affected outcomes. 1ng et al. have suggested that the impact of such sex inequities may be magnified in oncology, where patients often face a lifelimiting illness and physicians assume a "existential" role in providing potential "curative" care. 28In a study involving patients and medical oncologists, sex discordance was associated with worse outcomes among patients being treated for stage II−IV colon or lung cancer. 28 date, the impact of provider−patient sex concordance (or discordance) on cancer-specific postoperative outcomes has not been investigated.Therefore, the objective of the current study was to define the impact of sex concordance on postoperative outcomes following complex cancer surgery.Specifically, we hypothesized that sex discordance would adversely impact postoperative outcomes among both male and female patients.Services between 2014 through 2020 to identify patients who underwent surgery for lung, breast, hepato-pancreato-biliary (HPB), or colorectal cancer. 29As lung, breast, HPB, and colorectal cancers are some of the most prevalent cancers and the leading causes of cancer related deaths in the United States, these cancers were the focus of the current study. 30The CMS maintains the Medicare SAF, an administrative claims database that provides patient-level data on demographics, diagnoses, procedures, and expenditures. 31 Procedure Coding System codes were used to identify beneficiaries who had undergone surgery for any of the above-mentioned cancers (Supporting Information S1: Tables 1 and 2).This study was approved by The Ohio State University Institutional Review Board, and the need for informed patient consent was waived because the data were deidentified.

| Study and outcome measures
Information on age, race, region, social vulnerability index (SVI), and Charlson comorbidity index (CCI) were collected. 32,33The SVIdeveloped and maintained by the Center for Disease Control and Agency for Toxic Substances and Disease Registry-is a validated measure used to assess community vulnerability to external pressures. 34I was linked with the Medicare Standard Analytical Files using county-level Federal Information Processing System codes; SVI was categorized into tertiles.34 For the study cohort, hospital volumes were calculated and the hospitals were categorized as low, medium, and high volume based on tertiles.35 The CCI was assessed using ICD-9-CM and ICD-10-CM codes and dichotomized as ≤2 versus >2.32,33 Race/ ethnicity were recorded as self-reported social constructs, which are not a reflection of genetic ancestry and were categorized as Non-Hispanic White, Non-Hispanic Black, Hispanic, and Non-Hispanic Other race/ ethnicity.36 The Non-Hispanic Other race/ethnicity group was categorized as American Indians, Alaskan Natives, Native Hawaiians, Asians, Pacific Islanders, and self-reported "Other" race/ethnicity groups due to small sample sizes. 36Sex concordance was defined as a patient of male sex treated by a male surgeon or a patient of female sex treated by a female surgeon.Sex discordance was defined as a patient of female sex treated by a male surgeon or a patient of male sex treated by a female surgeon.1,37 The primary outcome of interest was the textbook outcome (TO), a composite measurement of desirable postoperative outcomes, which includes no 30-day complications at index surgery, no 90-day mortality, no prolonged length of hospital stay (<75th percentile for each procedure), and no readmission within 90 postoperative days. 38Complications were defined as respiratory failure, pneumonia, myocardial infarction, venous thromboembolic disease, acute renal failure, gastrointestinal bleeding, postoperative hemorrhage, and surgical site infection (Supporting Information S1: Table 3).Mortality data were derived based on the date of death in Medicare Standard Analytical Files.

| Statistical analyses
Descriptive statistics were presented using median (interquartile range [IQR]) for continuous measures and frequency (percentage) for categorical measures.Univariate analysis of demographic and clinical characteristics was performed using the χ 2 test for categorical variables and the independent sample t-test or Wilcoxon test for continuous variables.Multilevel multivariable logistic regression models were employed to assess the association between sex concordance and TO.Models for TO and individual components of TO were adjusted for sex, race, age, CCI, SVI, type of case (elective vs. urgent), region, index year, rurality (nonmetropolitan vs. metropolitan), cancer type, and hospital volume.The multivariable model was also adjusted for hospital fixed effects, which controlled for the unmeasured characteristics of hospitals that were constant over time.
Moreover, on multivariable logistic regression analysis, male patients being treated by a female surgeon (OR: 0.88, 95% CI: 0.84−0.92;p < 0.001) were associated with the lowest odds of achieving TO and female patients being treated by a female surgeon (OR: 1.30, 95% CI: 1.25−1.34;p < 0.001) were associated with the highest odds of achieving TO (Supporting Information S1: Table 6).
On stratification by SVI status, sex discordance was associated with lower odds of achieving TO among patients living in low (OR: 0.94,

| DISCUSSION
According to the National Academy of Medicine, quality healthcare is care that is safe, effective, patient-centered, timely, efficient, and equitable. 39The ability to deliver quality care is critical in determining the likelihood of positive outcomes and satisfactory care experiences among cancer patients.In 2005, Donabedian proposed three components to evaluate quality of care: structure, process, and outcomes. 406][47][48][49] In surgery, outcomes can also be related to teamwork in the perioperative setting.In particular, the operating room has a unique set of team dynamics, as professionals from multiple disciplines, whose training and goals often differ, are required to work in a closely coordinated fashion. 502][53] Of note, sex discordance related to the provider −patient dyad has been reported to influence processes of care and outcomes in noncardiac medical and surgical care, as well as in primary cardiac care. 12,27,54To date, the association between sex concordance and patient outcomes following complex oncologic surgery remains ill-defined.Therefore, the current study was important as we specifically investigated the relationship of provider−patient sex concordance on perioperative outcomes.In particular, we assessed achievement of TO following surgery for breast, lung, HPB, or colorectal cancer.Interestingly, sex discordance was associated with worse postoperative outcomes among both male and female cancer patients.
Sex concordance has been previously associated with an improved provider−patient relationship in primary care and inpatient medicine settings. 10,12,23,54For example, Tsugawa and colleagues reported that elderly hospitalized patients treated by female internists had lower mortality and readmissions compared with individuals cared for by male internists. 21In a separate study, Gross | 493 et al. noted that sex concordant provider−patient relationship was associated with better patient rapport, while a sex discordant provider−patient relationship correlated with a higher diagnostic uncertainty. 54Although these findings suggested differences in practice patterns between male and female physicians, few studies have examined the association of provider−patient sex concordance (or discordance) with postoperative outcomes. 1,37Wallis et al. did report that sex discordance was associated with worse postoperative outcomes among patients undergoing elective general surgery procedures. 1 In the current study, we similarly noted that sex discordance was associated with differences in perioperative surgical outcomes.Notably, sex discordant provider−patient treatment dyads were related to a higher risk-adjusted rates of complications, mortality, and readmission among Medicare beneficiaries with cancer.Specifically, sex discordance had a greater effect on mortality among female versus male patients.Taken together, these findings highlight that a discordant patient−provider dyad may negatively affect outcomes following oncologic surgical procedures.
Sex/gender discordance may adversely affect the physicianpatient relationship and interaction in several ways.For example, the predominance of male physicians in surgery compared with other medical specialties may carry implications for operative communication and teamwork related to gendered hierarchies. 55Jones et al.
noted that cooperation and communication decreased when more than half of the providers in an operating room were male. 56Related to this finding, relational coordination, defined as "communicating and relating for the purpose of task integration," has been found to contribute to quality treatment, psychological safety, and better patient outcomes. 57In fact, some data have suggested that operating room female staff members are challenged more often than their male colleagues when an incorrect clinical decision is made. 56,58,59x/gender based differences may also extend to the postoperative period.A prospective study of patient pain intensity after cardiac surgery noted an effect of examiner sex/gender on patient reporting, with patients reporting less postoperative pain to male assessors. 60tient also often prefer sex concordance with their surgeon for sensitive examinations, and sex discordance may lead to incomplete examinations in the postoperative setting. 1 These issues may contribute to a failure to recognize complications early when patients have deviations from postoperative pathways. 61Failure to appropriately identify complications early and intervene may lead to higher risk of more serious adverse postoperative outcomes, readmission, and mortality. 62,63To this point, in the current study, sex discordance was associated with greater odds of experiencing a complication at 30-days, readmission, and 90-day mortality.Moreover, the findings suggest that irrespective of patient's sex, female surgeons were more likely to have better postoperative outcomes than male surgeons.
These data are consistent with other evidence in literature, which demonstrated that female physicians and surgeons tend to have better outcomes. 20,21spite recent advances in surgical care, there are persistent disparities due to race/ethnicity among patients undergoing complex cancer surgery.For instance, Artinyan et al. demonstrated that among patients with hepatocellular carcinoma, Black patients were more likely to experience poor long-term survival. 64Similarly, Ramkumar et al. reported that not only were Black patients less likely to undergo surgery for colorectal cancer, but that they also experienced higher risk-adjusted mortality. 65In another study, Kim et  treatment for gastric cancer. 66Prior studies from our own group have also demonstrated that Black patients with cholangiocarcinoma were more likely to present with advanced stage disease and were less likely to undergo resection for localized disease. 67 line with these studies, the current work noted that sex discordance was associated with worse odds of achieving a TO among patients with Black race/ethnicity.These findings highlight the racial/ethnic disparities that are prevalent among patients undergoing cancer surgery and may exacerbate postoperative outcomes, especially when these patients face further challenges, such as sex discordance.
Given the potential importance of sex concordant care, there is a pressing need to address this issue in surgical and oncologic care. 68 note, among the 495 628 Medicare beneficiaries who underwent a cancer operation, only 62 205 (12.6%) had a female surgeon.These active physicians, women remain scarce in the surgical field. 69cording to data from the American Association of Medical Colleges, women make up less than one-quarter of physicians within the surgical specialties.The field of surgical oncology has similar challenges with female representation as there are 431 boardcertified surgical oncologists, only 31% of whom are female. 70cently, the Association of American Medical Colleges launched an initiative to address and eliminate sex-based inequalities in healthcare by aiming to increase female representation in all areas and fields of medicine. 71Holistic review and longitudinal mentoring programs are needed to increase female representation among surgical trainees and faculty. 72In addition, attention to recruitment and promotion of female faculty is critical to enhance representation and inclusion in surgery. 73,74Such initiatives are essential to improve equitable cancer care and reduce disparities by facilitating broader representation and more opportunities for sex/gender concordant care within surgery and surgical oncology. 75e current study should be interpreted considering several limitations.As the study was limited to Medicare beneficiaries, the

| CONCLUSIONS
In conclusion, sex discordance was associated with a reduced likelihood of achieving an "optimal" postoperative course following complex cancer surgery.Sex-discordant provider−patient dyads were associated with higher risk of postoperative complications, readmission, and mortality.A diverse surgical workforce that reflects the diversity of the patient population is needed to better address the needs of our patients, as well as to ensure more equitable high quality surgical outcomes.

2 |
MATERIALS AND METHODS 2.1 | Data source & study population Data were extracted from 100% Medicare Standard Analytic Files (SAF) claims data obtained by the Centers for Medicare and Medicaid To be enrolled, individuals were required to have complete Medicare coverage and consecutive enrollment in Medicare Parts A and B for at least 2 years before the index date.The International Classification of Diseases, Tenth Revisions ICD-10 diagnostic and procedure codes, Current Procedural Terminology Codes, and Healthcare Common
generalizability of the findings to younger patients or those with private insurance may be somewhat limited.Even though a surgeon may play a major role in care provision, nurses, residents, and the supporting staff are also involved extensively, and influence the overall postoperative course.Another limitation of this study is the heterogeneity of the data due to different cancer types included in the analytic cohort.The use of administrative data may also be associated with data miscoding and misclassification errors.To address this, we utilized ICD-9-CM diagnosis codes that have been previously demonstrated to have high fidelity for administrative data use.76Due to database limitations, surgeon-specific volume and operative experience could not be adjusted for and may act as an additional confounder.Moreover, the specific surgical details could not be accounted for due to database limitations.Future studies are needed to evaluate the effect of surgeon operative experience, hospital volume, gender, and sex on patient-provider interactions and healthcare outcomes.
were higher among patients residing in a low SVI (56.7% vs. 54.8)area versus individuals living in intermediate (54.9% vs. 53.8%)or high SVI (53.5% vs. 49.9%)neighborhoods when male patients were sex-concordant with their surgeon (p < 0.001).Similarly, females who were sex-concordant with their surgeon were also more likely to achieve a TO among patients who resided in low SVI areas (64.2% vs. 61.5%)versus intermediate (62.3% vs. 60.1%) or

1
Characteristics of study cohort by patient-surgeon sex concordance.
al. reported that Black patients were less likely to undergo chemotherapy and radiotherapy as a mode of T A B L E 2 Postoperative patient outcomes assessing the relationship between surgeon and patient sex concordance.