Abstract
Introduction
Transgender and gender diverse (TGD) populations with hereditary cancer syndromes face unique barriers to care and thus may not be accessing appropriate cancer screening or risk-reducing procedures. Our objective was to evaluate health care utilization of TGD patients with hereditary cancer syndromes. This includes counseling received, cancer screenings conducted, and risk-reducing procedures performed.
Methods
A case series of TGD patients (N = 11) with hereditary breast and ovarian cancer (n = 9) or Lynch syndrome (n = 2) who received care within Kaiser Permanente Northern California between 2009 and 2019.
Results
All patients received counseling and prophylactic options. Three patients (27%) completed all recommended screening, 6 (54%) had partial screening, 1 (9%) received no screening, and 1 (9%) did not require any screening. Six (55%) underwent a risk-reducing procedure.
Discussion
This case series highlights that despite all the study participants being appropriately counseled by practitioners about their risk of cancer, screening, and prophylactic options, in many cases, the screening received was partial or absent. Relatively few completed all the recommended screenings based on their clinical risk factors.
Conclusion
Many of the TGD patients with hereditary cancer syndromes in this cohort did not complete all the recommended cancer screening. This can be an area of focus in order to improve the quality of care provided to this vulnerable population.
Keywords: transgender, hereditary cancer syndrome, cancer screening, prophylactic surgery
Introduction
Hereditary cancer syndromes, including hereditary breast and ovarian cancer (HBOC) syndrome and Lynch syndrome, account for a large proportion of cancer diagnoses. HBOC, caused by a mutation of a tumor suppressor gene, either BRCA1 or BRCA2, accounts for 5% to 10% of female breast cancer diagnoses and 5% to 20% of male breast cancer diagnoses. 1 The risk of developing breast cancer by age 70 years among individuals with HBOC syndrome is 45% to 65%, compared to 12.3% in the general population. The risk of developing ovarian cancer is 39% and 10% to 17% in BRCA1- and BRCA2-positive individuals, respectively, although the risk of developing ovarian cancer is only 1.4% in the general population. 2 Cisgender men with HBOC syndrome are also at approximately a twofold increased risk of prostate cancer. Lynch syndrome causes increased risk of multiple cancers, including colorectal, endometrial, ovarian, and possibly breast cancer. The risk of developing colorectal, endometrial, and ovarian cancers by age 70 years in individuals with Lynch syndrome is 46% to 49%, 43% to 57%, and 5% to 20%, respectively. In contrast, the risk of developing colorectal cancer and endometrial cancer in the general population is only 4.5% and 2.7%, respectively. 3
In order to mitigate the morbidity and mortality associated with these hereditary cancer syndromes, health care organizations have recommended various screening and surveillance strategies for patients with HBOC and Lynch syndrome. The National Comprehensive Cancer Network (NCCN) has made screening recommendations for both HBOC and Lynch syndrome (Table 1). 3,4 The NCCN also recommends patients undergo a risk-reducing bilateral salpingo-oophorectomy (RRBSO) between ages 35 and 40 years for BRCA1-positive patients and between ages 40 and 45 years for BRCA2-positive patients. 4
Table 1:
The National Comprehensive Cancer Network recommended screening for patients with genetic mutations in BRCA1, BRAC2, and CHEK2, or patients with hereditary breast and ovarian cancer or Lynch syndrome
| Hereditary cancer syndromes | Age criteria | Recommended screening |
|---|---|---|
| Hereditary breast and ovarian cancer | 24–29 | Clinical breast examination every 6 mo and breast MRI every 12 mo |
| 30–75 | Breast MRI every 12 mo and mammogram every 12 mo | |
| < 30 until RRBSO a | Transvaginal ultrasound every 12 mos and Ca125 level every 12 mo | |
| Lynch syndrome | Starting at 20–25 for indefinite time | Colonoscopy every 1-2 y |
| Starting at 30–35 for indefinite time | Endometrial biopsy every 1 y b |
RRBSO for patients with BRCA1 is considered at age 35 to 40 years and for patients with BRCA2 at age 40 to 45 years.
Not required for PMS2 mutation.
MRI, magnetic resonance imaging; RRBSO, risk-reducing salpingo-oophorectomy.
Though recommendations among different organizations vary and efficacy has not been established for certain aspects of screening and surveillance protocols, there is a consensus that individuals with these hereditary cancer syndromes should receive some form of enhanced screening. Patients with these syndromes should discuss cancer risks with their health care practitioners and participate in shared decision making about prophylactic procedures and screening.
Transgender describes individuals whose gender identity differs from their sex assigned at birth. In this paper, the authors use the term gender diverse to describe individuals whose gender identity does not align with the male/female binary. This may include nonbinary, gender nonconforming, or gender queer, among other gender identities. These terms are used although the authors acknowledge the vast diversity of gender identities and preferred terminology that exist. There are 700,000 individuals in the US who identify as transgender or gender diverse. This represents 0.6% of the US population. 5 Transgender and gender diverse (TGD) people face unique challenges when it comes to accessing health care services, including appropriate cancer screening. These challenges include but are not limited to bias in the health care system, lack of standardized protocols for screening in this population, heterogeneity among the population about risk factors such as hormone therapy and gender-affirming surgery, and lack of education among practitioners. There is very little research about cancer risk and screening strategies among TGD patients. These patients have unique risk factors such as hormone therapy and mitigating factors such as gender-affirming surgery, which makes finding the appropriate strategy for screening complicated. For example, a transgender woman with HBOC has an increased risk of breast cancer if she takes hormone therapy but may have limited breast tissue for usual mammography. In another example, a transgender man may choose to pursue surgery in the form of breast reduction, subcutaneous mastectomy, or total mastectomy, all of which will change the baseline risk for breast cancer to different degrees.
Few studies have assessed the risk of breast cancer in transgender patients. In the Netherland, a retrospective cohort study of 2260 transgender women and 1229 transgender men who were all on hormone therapy found that there was an increased risk of breast cancer in transgender women compared to cisgender men, and this risk was increased with hormone treatment. 6 The same study also found a decreased risk of breast cancer in transgender men compared to cisgender women. By comparison, one Dutch study of 2307 transgender women and 795 transgender men who were all on hormone therapy found the incidence rates of breast cancer among both transgender women and transgender men were not significantly increased compared to cisgender men in the general population. 7 Another study looked at 5135 transgender veterans using data from the Veterans Health Administration and found that the incidence rate of breast cancer between 1996 and 2013 was 20.0 per 100,000 patient-years, which was consistent with the expected rate in the general population. This study also suggested no evidence of an increased incidence rate of breast cancer in transgender patients, regardless of hormone therapy, compared to the general population. 8 None of these studies looked specifically at patients with hereditary cancer syndromes, however.
Recommendations for cancer screening for TGD patients is limited. As a rule, screening should be done based on the anatomical parts of each individual and not based on their gender identity or hormone use. It is recommended that breast cancer screening in transgender women be initiated after 5 years of feminizing hormone use, regardless of age. 9
For TGD individuals with hereditary cancer syndromes, accessing adequate and appropriate cancer screening is of utmost importance. However, research on this topic is limited. A literature review found only 3 case reports on TGD patients with hereditary cancer syndromes. Given the lack of literature, this study aimed to describe 1) counseling, 2) cancer screening, and 3) prophylactic treatment received among TGD patients within an integrated health care system. The authors hypothesized that within an integrated health care system that prioritizes preventative and TGD care, the TGD patients with hereditary cancer syndromes received counseling regarding their risk of cancer, were appropriately screened, and underwent prophylactic surgeries.
Methods
Study population
This case series included TGD patients with HBOC or Lynch syndrome who received care within Kaiser Permanente Northern California (KPNC) between January 1, 2009 and December 31, 2019. The study was approved by the KPNC Institutional Review Board with a waiver of informed consent.
Patients were identified as TGD if they fulfilled 1 of the following 3 criteria prior to December 31, 2019: 1) had a diagnosis code indicating possible transgender status; 2) had a gender dysphoria, gender identity disorder, or gender status transition noted on their problem lists; and/or 3) their gender identities were noted to be different from their assigned sex at birth. Subsequently, the authors searched for evidence of hereditary cancer syndromes among these patients by looking for diagnosis codes (see Appendix A), indication of genetic mutations from patients’ problem lists, and from the Breast Cancer Tracking System, which documents breast cancer patients and their genetic mutations within KPNC (1) . Patients were excluded if they did not have any utilization records between 2009 and 2019. All potential patients were reviewed by a clinician to confirm their assigned sex at birth, gender identity, and whether they had a hereditary cancer syndrome. Index date was assigned as the date when genetic mutation was identified.
Data collection
Demographic information included age at index date, gender status, race/ethnicity, and KPNC membership length during the study period. Clinic information included specific genetic mutation, whether patients were on hormone therapy, and whether patients had gender-affirming surgeries and prophylactic surgeries (RRBSO, total laparoscopic hysterectomy [TLH], mastectomy) performed. All clinic information and gender status were acquired through chart review, and other demographic information was obtained through electronic databases.
Outcomes
Patients were followed from their index date until death, termination of membership, or the study end date, December 31, 2019, whichever came first. Outcomes were collected through chart review. For all eligible patients, the authors were interested in whether they were counseled for risk of cancer and prophylactic options. For HBOC patients, the dates of mammogram, breast magnetic resonance imaging (MRI), CA125 values, and ultrasounds were collected. For patients with Lynch syndrome, their colonoscopy dates were collected.
Analyses
All demographic and clinical information was presented using descriptive statistics only. Continuous variables were presented as means with standard deviation (SD), minimum and maximum values, and medians with the interquartile range (IQR). Categorical variables were presented as numbers and percentages. For our outcome of interest, screening was categorized as complete, partial, or none and reported by cancer site. Complete screening was defined if patients received all recommended screenings in time and frequency. If patients had some recommended screenings or if they did not receive screenings in time and frequency, they were regarded as receiving partial screenings. For prophylactic treatments, the authors differentiated procedures that followed risk-reducing protocols from procedures that were incidentally risk reducing. These results are presented in detail.
Results
Demographic and clinical information
A total of 11 TGD patients with hereditary cancer syndromes of interest were identified (Figure), including 4 female-to-male (FTM) patients, 2 male-to-female (MTF) patients, and 5 nonbinary patients. Nine patients (82%) were identified to have HBOC, and the remaining 2 (18%) were diagnosed with Lynch syndrome. Among patients with HBOC, there were 7 patients (64%) with BRCA1 mutation, 1 with BRCA2 mutation, and 1 with CHEK2 mutation. For patients with Lynch syndrome, 1 had a MSH2 mutation, and 1 had a PMS2 mutation. Most of these patients were White (81.8%), the median age when genetic mutation was identified was 31.0 years (IQR, 26.0–38.0), and their median membership length was 6.5 years (IQR, 3.7–10.3). Seven patients (64%) were using hormone therapy between 2009 and 2019, and 1 patient had used hormone therapy prior to 2009 (Table 2).
Figure:
Consort diagram of cohort identification of transgender and gender diverse patients with hereditary cancer syndromes, 2009 to 2019.
Table 2:
Demographic and clinical characteristics of transgender and gender diverse patients with hereditary cancer syndromes, 2009 to 2019
| Demographic characteristics | Total (N = 11) | HBOC (n = 9) | Lynch syndrome (n = 2) |
|---|---|---|---|
| Age when genetic mutation was identified | |||
| Mean ± SD | 32.2 ± 6.7 | 32.2 ± 6.9 | 32.0 ± 8.5 |
| Min-Max | 24.0–43.0 | 24.0–43.0 | 26.0–38.0 |
| Median (Q1–Q3) | 31.0 (26.0–38.0) | 31.0 (27.0–36.0) | 32.0 (26.0–38.0) |
| Gender –status, n% | |||
| FTM | 4 (36.4) | 3 (33.3) | 1 (50.0) |
| MTF | 2 (18.2) | 2 (22.2) | 0 (0.0) |
| Nonbinary | 5 (45.5) | 4 (44.4) | 1 (50.0) |
| Race and ethnicity, n% | |||
| White | 9 (81.8) | 7 (77.8) | 2 (100.0) |
| Asian | 1 (9.1) | 1 (11.1) | 0 (0.0) |
| Unknown | 1 (9.1) | 1 (11.1) | 0 (0.0) |
| Hispanic | 1 (9.1) | 1 (11.1) | 0 (0.0) |
| Membership length between 2009 and 2019 | |||
| Mean ± SD | 6.8 ± 3.3 | 6.9 ± 2.9 | 6.0 ± 6.3 |
| Min-Max | 1.6–11.0 | 2.8–11.0 | 1.6–10.4 |
| Median (Q1–Q3) | 6.5 (3.7–10.3) | 6.5 (4.5–9.3) | 6.0 (1.6–10.4) |
| Clinical characteristics | |||
| Genetic mutation, n% | |||
| BRCA1 | 7 (63.6) | 7 (77.8) | -- |
| BRCA2 | 1 (9.1) | 1 (11.1) | -- |
| CHEK2 | 1 (9.1) | 1 (11.1) | -- |
| MSH2 | 1 (9.1) | -- | 1 (50.0) |
| PMS2 | 1 (9.1) | -- | 1 (50.0) |
| Hormone therapy, n% | |||
| Past | 1 (9.1) | 1 (11.1) | 0 (0.0) |
| Current | 7 (63.6) | 5 (55.6) | 2 (100.0) |
| No | 3 (27.3) | 3 (33.3) | 0 (0.0) |
| Gender-affirming surgery, n% | 6 (54.5) | 4 (44.4) | 2 (100.0) |
| Risk-reducing surgery, n% a | 4 (36.3) | 4 (44.4) | 0 (100.0) |
| BSO | 3 (27.2) | 3 (33.3) | 0 (0.0) |
| Hysterectomy | 2 (18.2) | 2 (22.2) | 0 (0.0) |
| Mastectomy | 3 (27.2) | 3 (33.3) | 0 (0.0) |
Surgeries performed after the diagnosis of hereditary cancer syndrome and which followed risk-reducing protocol.
BSO, bilateral salpingo-oophorectomy; FTM, female to male; HBOC, hereditary breast and ovarian cancer; MTF, male to female; SD, standard deviation.
Follow-up and counseling
Three patients were lost to follow-up due to termination of membership. The median follow-up was 4.2 years (IQR, 2.5–4.6). All 11 patients were counseled about their risk of cancer and prophylactic options and had consultations with a genetic counselor.
Screening
The patients’ level of screening for breast, ovarian, endometrial, and colorectal cancer based on NCCN recommendations and the recommendations each patient received during their care were evaluated. For instance, for an MTF patient with HBOC on hormone therapy, NCCN does not have a specific recommendation for breast cancer screening. In this case, the authors looked for recommendations made by the patient’s care team and found they were recommended to have a baseline mammogram and annual mammograms if gynecomastia was present. The authors then evaluated whether this patient received those recommended tests. Overall, only 3 out of the 11 (27%) patients completed all recommended screenings, 6 of the 11 (55%) patients had partial screenings, 1 (9%) patient did not receive any screening, and 1 (9%) did not require any screening.
With regard to breast cancer screening, among the 9 patients with HBOC, 8 met criteria for breast cancer screening and only 2 completed the recommended screening (Table 3). One of these 2 patients received a single mammogram and an MRI prior to mastectomy. The other patient had already completed gender-affirming mastectomy, and the screening recommendation was for annual breast MRI that was performed on schedule. One patient did not require any screening because the risk-reducing mastectomy was pereformed shortly after the HBOC diagnosis.
Table 3:
Screening patterns among transgender and gender diverse patients with hereditary breast and ovarian cancer
| Cancer type | Total required screening N | Complete screening
a
n (%) |
Partial screening
b
n (%) |
No screening n (%) |
|---|---|---|---|---|
| Breast cancer | 8 | 2 (25.0) | 4 (50.0) | 2 (25.0) |
| Ovarian cancer | 4 | 1 (25.0) | 0 (0.0) | 3 (75.0) |
Complete screening: Patients received all recommended screenings based on National Comprehensive Cancer Networt criteria (Table 1) or based on health care practitioners in time and frequency.
Partial screening: Patients had some screenings but not all recommended screenings or screenings were not performed in time and frequency.
Two of the 8 patients did not receive any required breast cancer screenings. One of these 2 patients identified as MTF and was on hormone therapy. She was recommended to have a baseline mammogram at age 40 years followed by annual mammograms if gynecomastia was present, but no mammogram was performed. The other patient identified as FTM and had already completed a gender-affirming subcutaneous mastectomy. He received no screening despite being recommended to start annual mammogram and breast MRI screening at age 30.
The other 4 patients received some form of the required breast cancer screenings, but their screenings were not complete. One patient had MRIs and mammograms but had gaps greater than 1 year on multiple occasions. Two patients received annual or close to annual mammograms but did not complete all the required MRIs. One patient was having breast MRIs prior to age 30 years but did not initiate mammograms after age 30 years.
Four of the 9 patients with HBOC met criteria for ovarian cancer screening (Table 3); the other 5 had already had their ovaries and fallopian tubes removed or were MTF. Among the 4 patients, 1 (25%) received complete screening prior to RRBSO, and the other 3 (75%) did not have any ovarian cancer screening. Two patients were due to start annual transvaginal ultrasound/CA125 in 2018 but did not initiate screening as of 2019. One patient would have met criteria for two screenings prior to RRBSO, but screenings were never performed.
Both Lynch syndrome patients had colonoscopies within 1 year of their genetic mutation diagnoses. None had enough follow-up time to be tracked for subsequent procedures. One of the 2 patients met criteria for endometrial and ovarian cancer screening but did not receive any.
Gender-affirming and risk-reducing surgery (Table 4)
Table 4:
Screening, gender-affirming and risk-reducing procedures among transgender and gender diverse patients with hereditary cancer syndromes, 2009 to 2019
| Syndrome | Screening | Gender-affirming procedures | Risk-reducing procedures | Other |
|---|---|---|---|---|
| HBOC syndrome | ||||
| Patient 1 | Partial | None | Mastectomy | Hysterectomy (for heavy menses) |
| Patient 2 | Partial | None | None indicated | |
| Patient 3 a | Complete | BSO, hysterectomy, phalloplasty | Mastectomy, BSO, hysterectomy | |
| Patient 4 | None required | None | Mastectomy, BSO | |
| Patient 5 | Partial | Vaginoplasty | None indicated | |
| Patient 6 | No screening | None | None indicated | |
| Patient 7 b | Partial | Mastectomy, BSO, hysterectomy | BSO, hysterectomy | |
| Patient 8 | No screening | Mastectomy | None (age < 40 y) c | |
| Patient 9 | Partial | None | None (age < 40 y) | |
| Lynch syndrome | ||||
| Patient 1 | Complete | Mastectomy, BSO, hysterectomy | None d | |
| Patient 2 | Partial | Mastectomy | None | |
Had risk-reducing mastectomy prior to onset of gender transition. BSO and hysterectomy were for both gender affirmation and risk reduction.
Had gender-affirming mastectomy prior to diagnosis of HBOC. Subsequently had BSO and hysterectomy for both gender affirmation and risk reduction.
The National Comprehensive Cancer Network recommends risk-reducing BSO between ages 35 and 40 years for BRCA1 and 40 and 45 years for BRCA2. There is no specific recommendation for timing of mastectomy.
No specific recommendations for risk reducing procedures from the National Comprehensive Cancer Network.
BSO, bilateral salpingo-oopherectomy; HBOC, hereditary breast and ovarian cancer .
Six of the 11 patients (55%) underwent surgeries for the primary intent of gender affirmation: 3 patients underwent mastectomy; 1 patient underwent vaginoplasty; 1 patient underwent phalloplasty; and 1 patient underwent mastectomy, hysterectomy, and bilateral salpingo-oopherectomy (BSO). Although some of these procedures can decrease the patient’s overall risk of developing cancer, they do not follow the risk-reducing procedure protocol, such as removing breast tissue from below the pectoralis muscle or transecting the infundibular pelvic ligament 2.5 cm from the ovary.
Four of the 11 patients (36%) underwent procedures with the primary intent of risk reduction, or for both risk reduction and gender affirmation. These procedures were performed in accordance with the risk-reducing procedure protocol. All of these patients were in the HBOC group. One patient underwent a risk-reducing mastectomy; 1 patient underwent risk-reducing mastectomy and RRBSO, 1 patient underwent risk-reducing mastectomy, RRBSO, and hysterectomy; and 1 patient underwent RRBSO and hysterectomy (this patient previously had gender-affirming mastectomy). All patients over the age of 40 years who met criteria for a RRBSO had it performed.
If all gender-affirming procedures that were incidentally risk reducing and procedures aimed for risk reduction were included, then 7 of the 11 patients (64%) underwent a procedure that could decrease their risk of breast, ovarian, or uterine cancer.
Discussion
This study aimed to examine whether TGD patients with hereditary cancer syndromes were receiving appropriate counseling, screening, and prophylactic surgery in an integrated health care system. This case series highlights that despite all of the study participants being appropriately counseled by practitioners with regard to their risk of cancer, screening, and prophylactic options, in many cases, the screening received was partial or none. Relatively few completed all the recommended screenings based on their clinical risk factors. Overall, only 3 (27%) completed the recommended screenings for their clinical risk factors, 6 (55%) received partial screenings, 1 (9%) received none of the recommended screenings, and 1 (9%) did not require any screening. These findings can help to inform further efforts to improve screening in this high-risk population.
In our study, more than half of the cohort (55%) underwent gender-affirming surgeries, which is higher than what previous studies examining the broader TGD population have found. Previous studies found that the rates of gender-affirming surgery among the TGD population were 25% and 35%. 10,11 This discrepancy in our data may be partially explained by our populations’ access to care, as they were all insured with Kaiser Permanente. Additionally, our population of TGD patients with hereditary cancer syndrome in some cases had surgeries for the dual purpose of gender affirmation and cancer risk reduction, which may also impact the total number of gender-affirming surgeries.
Regarding risk-reducing surgeries, 36% of the cohort underwent surgeries with the primary intent of risk reduction and followed risk-reducing protocols. However, many of the gender-affirming surgeries also reduced the risk of developing cancer. If those are also included, the rate of risk-reducing procedures performed among our cohort is relatively high (55%). Every patient over age 40 years, born with ovaries, who had mutations that required RRBSO had the procedure performed or had previously undergone a BSO for gender affirmation. There were 6 patients with HBOC born with female breast tissue, and only 1 of those patients did not have a mastectomy performed.
This study has several limitations. Although the largest study of its kind, the small number of patients included in our study and lack of diversity among our cohort can merely give us a snapshot of the landscape surrounding cancer screening, counseling, and treatment for TGD patients with hereditary cancer syndromes. Furthermore, Kaiser Permanente health insurance did not begin covering gender-affirming surgeries until 2013. Prior to that, members often chose to have chest surgery at outside institutions, and these surgeries may not have been reflected in the data. Conversely, cancer screenings have historically been prioritized within the integrated health care system, and are likely to capture most screening data.
Given the relative absence of data on this unique population, even a small case series can add knowledge to the existing research. A review of current literature found only two case reports describing the care of two BRCA-positive transgender women who did not go on to develop cancer during the course of the case studies. 12 Additionally, only a single case report of breast cancer in BRCA-positive transgender men was found. Otherwise, there is a striking lack of literature on the subject. 13
Our study suggests that even within an integrated health care system, more consistent screening among this patient population is needed. The authors hope that their findings can motivate more physicians to provide screening and prophylactic surgery options to their TGD patients, promoting a more coordinated and preventative approach to patient care.
Appendix A
Appendix—Table 1.
Diagnosis codes used to identify transgender and gender diverse patients
| Description | Code type | Codes |
|---|---|---|
| Male to female hormone supplementation | Kaiser Permanente-specific codes | 12124952 |
| Transgender | 121141596 | |
| History of sexual reassignment surgery | 12125886 | |
| Female to male hormone supplementation | 12124310 | |
| Trans-sexualism | ICD-9 | 302.5 |
| Trans-sexualism with unspecified sexual history | 302.5 | |
| Trans-sexualism with asexual history | 302.51 | |
| Trans-sexualism with homosexual history | 302.52 | |
| Trans-sexualism with heterosexual history | 302.53 | |
| Gender identity disorder in adolescents or adults | 302.85 | |
| Gender identity disorder in children | 302.6 | |
| Transvestism | 302.3 | |
| Transsexualism | ICD-10 | F64.0 |
| Gender identity disorder in adolescence and adulthood | F64.1 | |
| Gender identity disorder of childhood | F64.2 | |
| Other gender identity disorders | F64.8 | |
| Gender identity disorder, unspecified | F64.9 | |
| Transvestic fetishism | F65.1 |
ICD-9, International Classification of Diseases, Ninth Revision; ICD-10, International Classification of Diseases, Tenth Revision.
Footnotes
Author Contributions: Maia Sakradse, MD, participated in the literature review, study design, data collection, drafting of the final manuscript, and critical review of the final manuscript. Shiyun Zhu participated in study design, data analysis, drafting of the final manuscript, and critical review of the final manuscript. Miranda Ritterman Weintraub, PhD, MPH, participated in study design, drafting of the final manuscript, and critical review of the final manuscript. Julia Jung, BA, participated in drafting of the final manuscript and critical review of the final manuscript. Eve Zaritsky, MD, participated in the literature review, study design, data collection, drafting of the final manuscript, and critical review of the final manuscript. All authors have given final approval to the manuscript.
Conflicts of Interest: This study was made possible by funding from Kaiser Permanente Northern California Graduate Medical Education Department. All authors were involved in the formulation of the research question, choice of study design, data collection, analysis, and decision to publish.
Funding: None declared
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