Endometrial Cancer Knowledge and Guideline-Concordant Practice Patterns Among First-Line Providers

Abstract

Background:

Provider uncertainty about the appropriate guideline-concordant evaluation of endometrial cancer (EC) symptoms may be a factor in racial inequities in EC. To evaluate the relationship between EC knowledge and reported practice patterns in a nationally representative survey of first-line providers for initial EC symptoms.

Materials and Methods:

This was a mailed cross-sectional survey of physicians and nurse practitioners from professional organization roster of providers from Obstetrics and Gynecology (OBGYN), Family Medicine, Internal Medicine, and Emergency Medicine. It queried demographics, practice characteristics, EC knowledge, and guideline-concordant practice patterns via three case vignettes. Regions of low response were retargeted to ensure strong representation among providers caring for Black women patients. EC knowledge was analyzed via a composite score (range: −3 to 10, with higher scores representing more EC knowledge), and adjusted prevalence ratios (PRs) used to test the association between knowledge and reported practice patterns.

Results:

Among 531 returned surveys (response rate = 38%), OBGYN had highest (53%) frequency of >6 (median) EC knowledge score, and Emergency Medicine had the lowest (15%) (p < 0.001). Nonguideline-concordant practice patterns were reported in 14%, 41%, and 35% of the three EC cases presented. Providers with knowledge >6, (n = 205) were significantly more likely to report guideline-concordant care on case vignettes (PR 1.28–1.36).

Conclusions:

In a national survey of multi-specialty backgrounds, there were basic knowledge gaps about EC and EC risk factors among providers, and a sizeable proportion reported nonguideline concordant practices. These findings indicate the importance of targeted education and training for first-line providers, as EC incidence rises.

Introduction

Endometrial cancer (EC) is the most common gynecologic malignancy in the United States, with an estimated 65,950 new diagnoses and 12,550 deaths in 2022.¹ The EC racial mortality gap is significant and increasing.² Black women have a 5-year mortality rate of 39%, nearly double their White counterparts (20%).^3,4 This disparity is partly attributable to advanced stage at diagnosis and more aggressive tumor characteristics among Black women.⁵ With early-stage diagnosis, the 5-year survival rate is 94.9%,¹ the highest among all gynecologic cancers.³ Survival decreases to 70% with regional spread and 20% with distant metastasis.⁶ Only 53% of Black women receive an early diagnosis compared to 70% of White women.^7,8

National guidelines for appropriate workup of postmenopausal bleeding, a cardinal symptom of EC, include transvaginal ultrasound (TVUS) followed by endometrial biopsy or dilation and curettage for definitive diagnosis. Alternatively, the guidelines also allow for providers to choose endometrial biopsy as a first step, before ultrasound.⁹ Among 4,891 Medicare enrollees with EC, Black women were less likely to have both bleeding symptoms documented and receive guideline-concordant evaluation. Receiving nonguideline-concordant care was associated with more advanced stage at diagnosis.⁸

Provider uncertainty regarding the workup for abnormal uterine bleeding may be a modifiable factor in delayed diagnosis. Patient knowledge of EC risk factors¹⁰ and provider referral patterns for gynecologic cancers have been studied¹¹; our goal was to evaluate providers' awareness of EC facts and inequities in a national survey.

Materials and Methods

To quantify EC knowledge and identify current practice patterns, we conducted a national survey of providers from multiple specialties. Our survey outreach sample consisted of 1,637 physicians and nurse practitioners, identified via purchased mailing lists of the American Medical Association (AMA) and the Nurse Practitioners in Women's Health (NPWH), respectively. The AMA mailing list contained a nationally representative random sample of active Internal Medicine, Family Medicine, Emergency Medicine, and Obstetrics and Gynecology providers (MD and DO). The NPWH list contained the entirety of their active membership list (RN, NPs, and Certified Nurse Midwife [CNM]). We chose to mail paper surveys with cash incentives as this method has been reported to have the highest response rate compared to email outreach or to: incentives in the form of a lottery, donation to a charity of participant's choosing, or e-gift card.^11
–13 Surveys were distributed via three waves of postal mailings, including a study introduction letter, the paper survey, a self-addressed return envelope, and $20 cash. The survey introduction letter contained instructions about accessing an opt-in online supplemental survey, with three additional questions. Participants were entered into a raffle for an additional $500 for completing both survey components.

We created a feasibility test pilot sample by randomly selecting 30 recipients from each specialty (n = 150) and completed this mailing in December 2019. In early 2020, the demographics (region, provider type/specialty) of respondents were assessed and lower response rates noted from the U.S. South. Thus, we adjusted sampling in the full outreach to oversample this category and ensure adequate representation from the southeast United States, where the population of Black women is the largest in the United States. Subsequent mailings took place from March to July 2020 (n = 1,487). This study was reviewed by an institutional human subjects division. The study was determined to be an educational survey. Identifying information could not be readily ascertained and risk was minimal deeming this study exempt (STUDY00008234).

The survey (Supplementary Data S1) consisted of three sections: demographic and practice information, EC knowledge questions, and case vignettes. Demographic and provider information included gender identity, age, race, Hispanic ethnicity, years in medical practice, clinical certification type, specialty, and academic affiliation; and practice setting (Federally Qualified Health Center, emergency department, outpatient clinic, urgent care, and hospital). For both gender and race, respondents self-identified from a pre-determined list that included an option to write-in any identities that were not listed (Supplementary Data S1).

The EC knowledge assessment asked participants to rank several types of cancer (gynecologic and breast cancers) by commonality; to identify the correct age decade of diagnosis for EC; and to identify the most common EC risk factors. For the case vignettes, there were four cases. One initial case served was designed as an “attention check” and asked respondents to choose the best next step in a suspected breast cancer diagnostic workup with a woman presenting with new breast mass. Breast cancer was chosen as an attention check, due to the significant public health education efforts related to mammography following the detection of a breast mass. The confirmatory diagnostic procedure of mammography is uniquely well-known to patients and providers. The subsequent three case vignettes introduced a woman with either postmenopausal or abnormal uterine bleeding, varied by patient ultrasound findings, age, bleeding symptom characteristics, and comorbidities (Table 1). Each of these three cases asked respondents to choose the best next step in management, among a list of options, based on the case presentation.

Table 1.

Overview of Case Vignettes for Abnormal and Postmenopausal Bleeding

Case characteristics	Case 1 (breast)	Case 2	Case 3	Case 4 ^a
Patient age	52	62	55	32
Other patient history and comorbidities	Not given	BMI 28, hypertension, high cholesterol	Fibroids	BMI 43; heavy menstrual cycles, anemia, no birth control
Presentation setting	Not given	Annual wellness	Ongoing management of irregular cycles	Emergency room
Current symptoms	Common cold, breast lump, no trauma	Light vaginal spotting one time, no pain	Menopausal symptoms with irregular and heavy cycles	Lightheadedness
Recent treatment, diagnostic tests, findings	Mammogram, small mass	Normal pelvic examination	Ultrasound confirmed fibroids; endometrial thickness 8 mm, normal hematocrit	Hemoglobin 6, negative pregnancy test, small fibroids, endometrial thickness 20 mm
Guideline concordant answers	Biopsy Order breast ultrasound	Transvaginal ultrasound Endometrial biopsy D&C	Endometrial biopsy D&C	Endometrial biopsy D&C
Nonguideline concordant answers	Repeat mammography in 3–4 months Observe for new growth or symptoms I'm not sure	Observe and initiate workup if she has episodes of repeated bleeding Hormonal treatment to prevent further bleeding Sexually transmitted infections screening A pap smear Unsure

For Case 4, although some literature supports BMI as threshold for biopsy,²⁰ there is no BMI threshold included in practice bulletin recommendations^9,16 and thus for Case 4 we reported the results descriptively without applying the guideline-concordant versus not classification in the text.

BMI, body mass index; D&C, dilation and curettage.

The opt-in, online-only supplement then asked three questions specifically about Black women and EC, related to mortality rate inequities, barriers to care, and factors that providers believe they can influence as individuals to improve care for Black women. This was created as a separate component to avoid priming respondents to the focus on racial disparities when they completed the initial knowledge questions and vignettes.

We used descriptive statistics to summarize the survey results in the overall sample and stratified by provider characteristics. Chi-squared testing was used to test for significant differences across groups, if sample size within groups were ≥10. For smaller sample sizes within a group (N < 10) Fisher's exact test was used.

The EC knowledge questions were summarized in a knowledge score that gave respondents one point for each risk factor correctly identified and subtracted one point for each incorrect answer (Table 2). Although racial categories were included in the list of risk factors (Supplementary Data S1), they were not included in the knowledge score construction due to lack of clarity of a consistent referent group within the body of the question; therefore, we omitted this question in the score. To test the hypothesis of whether EC knowledge was related to correct choice of guideline-concordant care, Poisson regression was used to compare correct responses by those above and below the median EC knowledge score. Unadjusted prevalence ratios (PRs) and 95% confidence intervals were calculated to summarize the association between knowledge score and case vignette practice patterns. For the opt-in, online-only supplement, simple frequencies were calculated and presented as hypothesis generating, as the study was not powered for these items and the extent of participation in the secondary supplement was unknown a priori.

Table 2.

Endometrial Cancer Knowledge Score Construction from Survey Responses

Add one point for each of the following:

+ Selected any of these risk factors from a list: Diabetes, Obesity, Irregular menstrual cycles, Postmenopausal bleeding, Tamoxifen, Genetics, Family history, Polycystic Ovarian Syndrome

+ Correctly identified that endometrial cancer is more common than ovarian cancer

+ Correctly identified 60–70 as the most common decade for age at diagnosis

Subtract one point for the following:

− Selected smoking, endometriosis, uterine fibroids from a list of risk factors

A p-value of <0.05 indicated a statistically significant association. All analyses were completed in R (Version 4.1.1).¹⁴

Results

Of 559 returned surveys, 531 were complete enough to include in analysis for a total response rate of 38%. Surveys were considered “complete enough” and included in the analysis if they were returned with any portion of the questions answered. There were no significant differences between responders and non-responders based on region or certification type. A significantly higher proportion of respondents were NPs rather than MD/DO, compared to nonrespondents. Most respondents were physicians (63%), female (65%), 40–59 years (55%), and self-identified as White (79%). Race and ethnicity were not treated as mutually exclusive categories, and respondents were included in all categories selected. Most (73%) had no university affiliation, and 77% reported at least a weekly frequency of seeing Black women. The majority (58%) of respondents specialized in Obstetrics and Gynecology (OBGYN) or women's health (all NPs), followed by Primary Care or Family Medicine (25%), Emergency Medicine (12%), and Internal Medicine (10%). In accordance with the sampling plan, a plurality of respondents was located in the Southern United States (43%) (Table 3).

Table 3.

Demographics of Health Care Provider Survey Respondents

Characteristics	N (%)
Total	531 (100)
Gender
Female	346 (65)
Male	178 (34)
Non-binary	2 (0.4)
Prefer not to answer	2 (0.4)
Age
20–39	94 (18)
40–59	292 (55)
60+	141 (27)
Race and ethnicity
American Indian or Alaska Native	4 (0.8)
Asian	65 (12)
Black or African American	32 (6)
Hispanic or Latino	29 (6)
Native Hawaiian or Other Pacific Islander	7 (1)
White	424 (80)
Practice years/clinician years
0–4 years	36 (7)
5–10 years	64 (12)
11+ years	378 (71)
Certification type
Medical Doctor/Doctor of Osteopathy	334 (63)
Nurse Practitioner/Certified Nurse Midwife/Registered Nurse	195 (37)
Specialty
Obstetrics and Gynecology/Women's Health	309 (58)
Primary Care/Family Medicine	135 (25)
Emergency Medicine	62 (12)
Internal Medicine	55 (10)
Academic affiliation
No university affiliation	390 (73)
University affiliation	134 (25)
Region
Northeast	100 (19)
South	229 (43)
West	111 (21)
Midwest	86 (16)

EC knowledge

Less than half of all respondents (48%) correctly identified EC as being more common than both ovarian and cervical cancer, and fewer (35%) identified the correct decade of median age of EC diagnosis (60–70 years). Neither of these differences was significantly associated with provider type or any other participant characteristics. When asked to select all factors that increase an individual's risk of being diagnosed with EC, there was wide variation in endorsement of factors that increase risk (Table 4). Nurse practitioners were significantly more likely to endorse correct answers (true) for the following factors: obesity, polycystic ovarian syndrome, family history, and genetics. Across all provider types, treating Black women in clinic more frequently (either daily or a few times per week) was significantly associated with correctly identifying postmenopausal bleeding as a risk factor. No significant relationships between participant characteristics and correct endorsements of other risk factors were found (Table 4). Overall, the median EC knowledge score was 6 (IQR = 25th, 75th percentile). Physicians were slightly more likely to score above the median than NPs, but this relationship was insignificant. By specialty, OBGYN and women's health providers were significantly more likely to score above the median compared to all other specialties (Table 5). There were no significant differences between physicians and NPs overall in scoring above or below the median.

Table 4.

Survey Results of Provider Knowledge of Endometrial Cancer Risk Factors

Response correctness	Listed potential risk factors that increase likelihood of developing endometrial cancer	% Survey respondents that selected the risk factor
TRUE	Diabetes	55.6
	Obesity	89.5
	Irregular menstrual cycles	64.4
	Postmenopausal bleeding	84.4
	Tamoxifen	62.7
	Genetics	56.1
	Family history	72.1
	Polycystic ovarian syndrome	60.3
FALSE	Smoking	50.5
	Uterine fibroids	8.9
	Endometriosis	13.9

Table 5.

Endometrial Cancer Knowledge Score Results by Provider Characteristics

Provider characteristics		Respondents above Median knowledge score of 6, % (N)	p
All respondents		38.7 (205)
Certification type	Medical Doctor/Doctor of Osteopathy	38.9 (130)	0.097
Certification type	Nurse Practitioner/Certified Nurse Midwife/Registered Nurse	38.2 (73)	0.097
Specialty	Obstetrics and Gynecology/Women's Health	53.1 (164)	<0.001
	Primary Care/Family Medicine	28.2 (38)
	Emergency Medicine	14.5 (9)
	Internal Medicine	21.8 (12)
Frequency of treating Black women	Daily or few times per week	39.4 (162)	0.8258
Frequency of treating Black women	Less than daily or weekly	37.7 (43)	0.8258

Practice patterns in evaluation of postmenopausal and abnormal uterine bleeding

The EC case vignettes were designed to get progressively less diagnostically straightforward and yielded much variability across provider type and other characteristics. In case 2, a “classic” presentation of the cardinal EC symptom of postmenopausal bleeding, we found that 13.4% of participants selected a nonguideline-concordant answer. Within participants who chose a guideline-concordant answer for this case, there was a preference for TVUS as the next step in diagnostic workup (53.5%) over endometrial biopsy or D&C (36.0%). For case 3, where TVUS results were provided for a woman with menopausal symptoms, irregular bleeding, and a thickened endometrium (8 mm), 35% incorrectly selected a nonguideline-concordant answer that did not involve tissue biopsy. In case 4, where TVUS results were provided for a premenopausal woman with severe menorrhagia and anemia requiring blood transfusion, 34.5% did not elect for tissue evaluation (Supplementary Data S2). In contrast, for the control case focused on treatment patterns after a 62-year-old woman identifies a breast lump, the choice of a nonguideline-concordant option for the next step in treatment was rare (2.2%). Although differences were observed between cases in the proportion of guideline-concordant care options chosen, no additional significance testing was conducted, to avoid multiple comparison errors.

Knowledge level and guideline-concordant care

Those with knowledge scores above the median (6, n = 205) were statistically significantly more likely to select any guideline-concordant option for two of the cases (PRs 1.28–1.36) and to choose endometrial biopsy, specifically in all three EC cases (PRs 1.34–1.47). This association remained significant after adjusting for presence of university affiliation and number of years in clinical practice, two hypothesized factors in increased guideline-concordant care delivery.

Racial disparity knowledge and provider agency

For the supplemental opt-in questions that were available online, there were 232 responses eligible for inclusion in the analysis. Most demographic characteristics looked similar among the two survey samples, with the online survey group tending to be younger and having a higher proportion of NP/RN/CNMs. Most (87.9%) providers believed that Black and White women do not have equal chances of survival after an EC diagnosis, which is correct. This belief did not differ significantly by certification type (p = 0.25), specialty type (p = 0.87), number of years in practice (p = 0.49), or geographic region (p = 0.46). Among the 12% of providers who believed that there are no survival disparities by race, most were NP/CNMs (61%), had 0–4 years of clinical experience (18%), and practiced in the South (32%) or Midwest (32%) (Supplementary Data S3).

Concerning beliefs about what contributes to racial disparities in EC, 96% endorsed at least one biological contributor (aggressive histology, stage at diagnosis, or comorbidity), 95% endorsed access (lack of access or quality of care), 25% endorsed inherited genetics impacting treatment response, and 16% endorsed treatment refusal. These beliefs did not vary by provider characteristics. With respect to provider agency, most believed that they had the power to impact both access (69%) and quality of care (75%) for Black women, while fewer believed that they could impact the stage at diagnosis (48%) or treatment refusal (19%).

Among the smaller subset of respondents to the online opt-in questions, we found an overall high level (87.9%) of awareness of racial disparities in mortality for EC. In addition to most respondents (95.3%) endorsing issues related to health care access, a quarter (25.4%) also supported the unproven idea that “Black women have inherited genetics that impact how they respond to treatment.” Despite the positive results that many providers are knowledgeable about EC disparities, the results suggest the continued need for EC educational content to incorporate information about multilevel processes (e.g., racism, poverty, and so on) that create EC disparities.

Discussion

Principal findings

To our knowledge, this is the first national survey to assess reported health care provider practice patterns in the diagnostic evaluation of EC across training certification and specialty types. In this sample, higher provider knowledge of EC facts was associated with a significantly higher likelihood of pursuing a guideline-concordant next step in treatment after symptom disclosure. While this is reassuring, we also found that nonguideline-concordant choices are common. As EC incidence increases, driven by higher rates of high-risk histology types,¹⁵ it is critically important to assess and intervene in gaps in provider knowledge and practice patterns that can result in delays in diagnosis.

Overall, there were few significant differences in knowledge scores or other responses by provider certification type; however, there were substantial differences between specialties. OBGYN and women's health providers consistently reported higher knowledge scores than Primary Care, Internal Medicine, or Emergency Medicine respondents. As the median age at EC diagnosis is 62, patients with EC symptoms may not have routine women's health-focused providers and can present in all the settings that were sampled in this work. Non-OBGYN providers can very well be “front line” responders to initial symptom disclosure, and an important target for education to improve care quality and potentially shorten the time to EC diagnosis.

Results in the context of what is known

The high level of variation in the guidelines regarding the most appropriate next step in EC diagnostic evaluation may explain higher rates of nonguideline choices for cases of perimenopausal or younger women (Case 3 and 4). While TVUS is not a confirmatory diagnostic procedure for EC at any age, TVUS findings should dictate the next step in evaluation of abnormal bleeding.¹⁶ Even when presented with highly concerning TVUS findings (endometrial stripe thickness of 8 and 20 mm, respectively, in cases 3 and 4), a plurality of respondents declined endorsement of a confirmatory diagnosis for EC in both cases. The consistent nature of not immediately prioritizing a tissue-based confirmatory diagnosis has important health equity implications. Previous work has suggested that TVUS may be less accurate in diagnosing high-risk EC in Black women based on cohort simulation.⁵ In addition, TVUS was a poor discriminator for women over 60 with postmenopausal bleeding in another study.¹⁷ Thus, tissue diagnosis early in the evaluation process may be important in narrowing the Black-White mortality gap in EC.

Research implications

Providers with higher levels of EC knowledge were significantly more likely to select guideline-concordant options as the next step in EC treatment. This may indicate that a provider education intervention could result in higher rates of guideline-concordant evaluation after EC symptom disclosure. The implication that a provider education intervention may increase guideline-concordant care is also supported by one of the findings from the online-only supplement: a majority (75%) of respondents believe that they have agency to improve the quality of care for Black women. Further research should explore educational intervention development and increase the use of guideline-concordant care for patients presenting with EC symptoms.

Strengths and limitations

This novel work identifies knowledge gaps and establishes reported practice patterns among first-line providers for patients reporting the initial symptoms of EC. By utilizing a nationally representative sample with a high rate of respondents from non-academically affiliated providers, the results from the mailed survey are generalizable to community-based practices where many Black women seek care (as opposed to only surveyed practitioners at academic medical centers). This study relied on survey responses, which may not indicate actual clinical practice patterns. Although the main intent of this work was to identify gaps in provider knowledge that may contribute to EC health inequities, we did not directly survey or explicitly ask about racial inequities in the primary mailed survey. A background literature review revealed a high rate of false negative results when providers are explicitly asked questions that may reveal preferential treatment of patients across racial differences, stemming from social desirability bias from respondents.¹⁸ To ensure that we captured practice patterns relevant to Black patients, we deliberately oversampled from the South, ensuring an adequate representation of providers who routinely treat Black patients. The most extensive mailing took place in early March 2020, and our response rate is perhaps lower than would have been otherwise, given the additional burden present on physicians and nurse practitioners at the time of the burgeoning SARS-COV-2 global pandemic. We identified one duplicate response after the analysis was complete. The online, opt-in survey responses may be limited in generalizability, as all respondents self-selected to complete the online supplement after returning the mailed survey.

Conclusions

In addition to improving current guidelines with risk-based approaches, we must ensure proper education and dissemination of appropriate care practices for people presenting with EC symptoms. Black women are especially vulnerable to delay, and targeting providers across the spectrum of health care in a systems-based approach may be a key component of minimizing care delay. These findings support the need to develop and implement targeted evidence-based provider EC education programs, based on these measured gaps in knowledge and guideline-concordant care. Given the existing vulnerability for Black women and the growing vulnerability for all women for high-risk EC,¹⁹ providers of all specialties, who encounter EC symptom disclosure, stay abreast of the most up-to-date information on risk-based diagnostic workup recommendations.

Footnotes

Authors' Contributions

L.S.: Writing—Original Draft Preparation, Reviewing and Editing, Project Administration, Investigation. E.D.: Formal Analysis, Data Curation, Visualization, Writing-Reviewing and Editing, Methodology. D.A.G.: Writing—Original Draft, Validation. A.O.: Writing—Reviewing and Editing, Data Curation. P.A.W.: Writing—Reviewing and Editing, Project Administration. R.K.: Methodology, Writing—Reviewing and Editing, Supervision. N.J.Q.: Validation. K.M.D.: Writing—Reviewing and Editing, Finding Acquisition, Supervision, Conceptualization, Methods, Project Administration.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

This work was funded by grant 75203 from the Robert Wood Johnson Foundation. The sponsor had no role in study design, collection, analysis and interpretation of data, writing of the report, nor the decision to submit the report for publication.

Supplementary Material

Supplementary Data S1

Supplementary Data S2

Supplementary Data S3

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Supplementary Material

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