Abstract
Purpose
Data on endometrial cancer outcomes among immigrant women in the USA are lacking. The objective was to determine the effect of Caribbean nativity on outcomes in black women with endometrial cancer compared with women born in the USA, with attention paid to the effects of tumor grade, sociodemographic factors, and treatment approaches.
Methods
A review of the institutional cancer registry was performed to identify black, non-Hispanic women with known nativity and treated for endometrial cancer between 2001 and 2017. Sociodemographic, treatment, and outcomes data were collected. Analyses were done using the χ2 test, Cox proportional hazards models, and the Kaplan–Meier method, with significance set at P<0.05.
Results
195 women were included in the analysis. High grade histologies were present in a large proportion of both US born (64.5%) and Caribbean born (72.2%) patients. Compared with US born women, those of Caribbean nativity were more likely to be non-smokers (P=0.01) and be uninsured (P=0.03). Caribbean born women had more cases of stage III disease (27.8% versus 12.5%, P<0.01), while carcinosarcoma was more common in US born black women (23.6% versus 10.6%, P=0.05). Caribbean nativity trended towards improvement in overall survival (hazard ratio (HR) 0.65 (0.40–1.07)). Radiation (HR 0.53 (0.29–1.00)) was associated with improved survival while advanced stage (HR 3.81 (2.20–6.57)) and high grade histology (HR 2.34 (1.17–4.72)) were predictive of worse survival.
Conclusions
The prevalence of high grade endometrial cancer histologies among black women of Caribbean nativity is higher than previously reported. Caribbean nativity may be associated with improved overall survival although additional study is warranted.
INTRODUCTION
Over the past 50 years, the incidence of endometrial cancer has risen globally.1 This trend is also reflected in the number of new cases in the USA where more than 63 000 women are diagnosed with endometrial cancer annually.2 While much of this rise may be attributed to increasing rates of obesity in many nations, endometrial cancer actually represents a diversity of histologies, with variable risk factors, genetic susceptibilities, and outcomes.3 Endometrial cancer can be classified into two different types by histologic grade. Type I, or low grade, tumors are characterized by predominantly glandular components, are slow growing, and are driven by hyperestrogenism. In contrast, type II, or high grade, tumors are aggressive, metastasize early, and are independent of a hormone pathway for pathogenesis.4 The majority of women will be diagnosed with low risk disease but certain minority groups, including black women, are at higher risk for the type II histologies with resultant poorer survival.5 In fact, it has been well described that the proportion of type II histologies among black women is nearly double that of white women.6
While only 7% of new endometrial cancer cases are diagnosed in black women, these patients account for approximately 14% of endometrial cancer deaths.7 A number of factors have been suggested as contributing to poorer outcomes among black women, including reduced access to care, lower clinical trial participation, and higher rates of genetic mutations that promote metastatic phenotypes.8 Country of birth, however, has been relatively understudied, but may be an important contributor to outcome as varying nativities may predispose to different environment exposures and molecular epigenetic changes. Considering that 1 of every 10 blacks in the USA are immigrants, 50% of whom are Caribbean, and that immigrants from the Caribbean now outnumber new immigrants from Europe, it is important to understand if Caribbean nativity affects cancer outcomes.9 10 Few studies have evaluated the role of nativity in women with endometrial cancer, and the data reported are conflicting in terms of the effect of nativity on survival and as a determinant of prognostic factors.11 12 Significant limitations of these studies include failure to consider the influence of tumor grade, or inclusion of uterine histologies that were not endometrial in origin, thus confounding the results. As such, our objective was to explore the effect of Caribbean nativity on outcomes in black women with endometrial cancer, with attention paid to the mediating effects of tumor grade, sociodemographic factors, and treatment approaches.
METHODS
After approval from the University of Miami institutional review board (protocol 2015–1022), a total of 1964 women diagnosed and treated for invasive endometrial cancer between 2001 and 2017 were identified through the institutional cancer registry. All women who were identified as non-Hispanic black, regardless of tumor grade and histology, were included. Patients who did not have data on country of birth, who identified as Hispanic black, or whose country of birth was not located in the Caribbean or the US were excluded. Black women with Hispanic ethnicity were excluded due to low numbers, which precluded stratification of them as a separate group, and because previously reported data have demonstrated variable risk among women of Caribbean ancestry.13 Additionally, patients with non-endometrial malignancies, or whose grade/histology were unknown, were excluded.
Data obtained from the cancer registry included date of diagnosis, age of diagnosis, country of birth, tumor grade and histology, stage at diagnosis, insurance status, history of alcohol and tobacco use, and receipt of surgery, hormone antagonism, chemotherapy, and radiation as components of their individual treatment plans. The date of diagnosis was defined as the day of pathologic confirmation of cancer. Age was recorded as a continuous variable. Patient country of birth was dichotomized as either US born or Caribbean born. Caribbean born patients were self-identified. Histology and grade were reviewed by the principal investigator to ensure that the two were consistent, with tumors being segregated as low grade (grade I or II endometrioid) or high grade (grade III endometrioid, clear cell, carcinosarcoma, serous, or undifferentiated/other). Stage at diagnosis was recorded according to the American
Joint Committee on Cancer classifications. Alcohol and tobacco use were classified as either never/former or current. Insurances status was classified as insured or uninsured. Surgery, hormone antagonism, chemotherapy, and radiation were dichotomized as given or not given. Overall survival was defined as time from date of diagnosis to date of death (all cause).
Statistical analyses were performed using STATA IC 14.2 (StataCorp, College Station, Texas, USA). All patients were included in the analyses, even when missing specific data points, and all available data were included. Summary statistics were used to describe the patient cohort. Wilcoxon rank sum was used for continuous variables in non-parametric distributions. The χ2 test (or Fisher’s exact test, when appropriate) was used to analyze associations between categorical variables. Univariable and multivariable Cox proportional hazards regression, the log rank test, and the Kaplan–Meier method were used to assess survival outcomes, with 95% confidence intervals (CI) generated. Given that our small sample limited multiple comparisons, stepwise backwards multivariable regression analyses only included covariates with P values <0.05 from the univariable models. However, as nativity was the specific variable of interest, this was also included in the multivariate models. All tests were two sided, with significance set at P<0.05.
RESULTS
During the study interval, 1964 women were diagnosed with endometrial cancer at our institution. Of these, 195 met inclusion criteria (Figure 1). Demographics of these patients are shown in Tables 1 and 2. A total of 105 patients were US born and 90 were Caribbean born. There were no differences between US born and Caribbean born black women by age of diagnosis, treatments received (surgery, radiation, chemotherapy, and hormone antagonism), or current alcohol use. A larger proportion of US born women were current smokers (11% vs 1.2%, P=0.01). A larger proportion of Caribbean born women were also uninsured (27% versus 14.4%, P=0.03). More Caribbean born women had advanced stage (stages III/IV versus stages I/II) disease compared with US born women although the difference was not statistically significant (44.3% versus 32.9%, P=0.09). However, there were differences in distribution of stage, with Caribbean women more often being diagnosed with stage III disease (27.8% versus 12.5%, P<0.01). In contrast, US born women had a higher percentage of stage II disease although this did not reach statistical significance (13.6% versus 3.8%, P=0.10). There was no difference by nativity in the distribution of histologic grade, with type II being more common in both groups (72.2% Caribbean born versus 64.5% US born, P=0.27). There was significant variability by specific histology, with a larger proportion of US born women having carcinosarcoma (23.6% versus 10.8%, P=0.05), and more Caribbean born women having serous carcinoma (36.9% versus 25%, P=0.14).
Figure 1.
Flow diagram of patients included in the analysis.
Table 1.
Cohort demographics
| Caribbean born |
US born |
||
|---|---|---|---|
| Variable | N(%) | N (%) | P value |
| Age at diagnosis (years) | |||
| Median (range) | 62.5 (29–86) | 64 (26–83) | 0.19 |
| Stage at diagnosis | |||
| I | 40 (50.6) | 47 (53.4) | 0.37 |
| II | 3 (3.8) | 12 (13.6) | 0.1 |
| III | 22 (27.8) | 11 (12.5) | <0.01 |
| IV | 14 (17.8) | 18 (20.5) | 0.91 |
| Uninsured | |||
| Yes | 24 (27.0) | 15 (14.4) | |
| No | 65 (73.0) | 89 (85.6) | 0.03 |
| Histologic grade | |||
| Low grade | 25 (27.8) | 37 (35.5) | 0.27 |
| Endometrioid | 25 (100) | 37 (100) | |
| High grade | 65 (72.2) | 68 (64.5) | |
| Clear cell | 3 (4.6) | 7 (10.3) | 0.18 |
| Endometrioid | 13 (20) | 9 (13.2) | 0.29 |
| Carcinosarcoma | 7 (10.8) | 16 (23.6) | 0.05 |
| Serous | 24 (36.9) | 17 (25) | 0.14 |
| Other/undifferentiated | 18 (27.7) | 19 (27.9) | 0.97 |
| Surgery performed | |||
| Yes | 69 (76.7) | 76 (73.8) | |
| No | 21 (23.3) | 27 (26.2) | 0.64 |
| Chemotherapy | |||
| Yes | 41 (46.6) | 43 (43) | |
| No | 47 (53.4) | 57 (57) | 0.62 |
| Radiation | |||
| Yes | 22 (25.3) | 22 (21.8) | |
| No | 65 (74.7) | 79 (78.2) | 0.57 |
| Hormones | |||
| Yes | 6 (6.7) | 8 (7.8) | |
| No | 83 (93.3) | 95 (92.2) | 0.79 |
| Tobacco use | |||
| Current | 1 (1.2) | 10 (11) | |
| Never/former | 81 (98.8) | 81 (89) | 0.01 |
| Alcohol use | |||
| Current | 6 (7.6) | 9 (9.8) | |
| Never/former | 73 (92.4) | 83 (90.2) | 0.61 |
Table 2.
Caribbean representation by country
| Country | No (%) of women |
|---|---|
| Bahamas | 7 (7.8) |
| Dominica | 1 (1.1) |
| Guyana | 1 (1.1) |
| Haiti | 51 (56.7) |
| Jamaica | 22 (24.4) |
| Trinidad and Tobago | 5 (5.6) |
| Other | 1 (1.1) |
| Suriname | 1 (1.1) |
| US Virgin Islands | 1 (1.1) |
Table 3 shows the proportional hazards models for overall survival for the entire cohort. Age at diagnosis (hazard ratio (HR) 1.03 (95% CI 1.01 to 1.05), P=0.016), advanced stage (HR 4.84 (95% CI 2.11 to 6.19), P<0.001), and high grade histology (HR 4.81 (95% CI 2.53 to 9.14), P<0.001) were all associated with worse overall survival, while receipt of surgery (HR 0.54 (95% CI 0.33 to 0.86), P=0.01) and radiation (HR 0.50 (95% CI 0.28 to 0.88), P=0.016) were both protective. In the multivariable model, radiation (HR 0.51 (95% CI 0.27 to 0.95), P=0.04), advanced stage (HR 3.61 (2.11–6.19), P<0.001), and high grade histology (HR 2.34 (1.17–4.70), P=0.02) all remained independent predictors of better overall survival, while Caribbean nativity trended towards reduced risk of death (HR 0.65 (0.40–1.07)). When Caribbean born and US born women were evaluated separately, there were several differences. Birth specific regression analyses are shown in Table 4. Among Caribbean born patients, advanced stage (HR 3.25 (95% CI 1.45 to 7.31)) was associated with worse survival, but high grade disease appeared to be associated with an even greater risk of poorer outcomes (HR 5.57 (95% CI 1.28 to 24.25)) in the multivariable model. In contrast, for US born black women, advanced stage (HR 4.22 (95% CI 2.10 to 8.51)) and surgical resection (HR 0.42 (95% CI 0.20 to 0.89)) were independently predictive of worse survival although higher grade approached significance (HR 2.23 (95% CI 0.98 to 5.08), P=0.06). Because Haitian women constituted a significant proportion of the cohort, they were evaluated separately, with similar findings. These results are shown in online supplement 1.
Table 3.
COX proportional hazards models for overall survival for the entire cohort
| Univariable |
Multivariable |
|||
|---|---|---|---|---|
| Variable | HR | 95% CI | HR | 95% CI |
| Place of birth | ||||
| USA (reference) | -- | -- | ||
| Caribbean | 0.81 | 0.52 to 1.27 | 0.65 | 0.40 to 1.07 |
| Age at diagnosis (continuous) | 1.03 | 1.01 to 1.05 | 1.01 | 0.98 to 1.04 |
| Surgery | ||||
| No (reference) | -- | |||
| Yes | 0.54 | 0.33 to 0.86 | 0.58 | 0.33 to 1.02 |
| Hormone antagonism | ||||
| No (reference) | -- | |||
| Yes | 0.46 | 0.17 to 1.27 | ||
| Chemotherapy | ||||
| No (reference) | -- | |||
| Yes | 1.55 | 0.99 to 2.43 | ||
| Radiation | ||||
| No (reference) | -- | |||
| Yes | 0.5 | 0.28 to 0.88 | 0.53 | 0.29 to 1.00 |
| Tobacco use | ||||
| Never/former (reference) | -- | |||
| Current | 1.32 | 0.57 to 3.06 | ||
| Alcohol use | ||||
| Never/former (reference) | -- | |||
| Current | 0.59 | 0.21 to 1.61 | ||
| Stage of disease | ||||
| Stages I and II (reference) | -- | |||
| Stages III and IV | 4.84 | 2.97 to 7.91 | 3.81 | 2.20 to 6.57 |
| Histologic grade | ||||
| Grades I and II (reference) | -- | |||
| Grade III or undifferentiated | 4.81 | 2.53 to 9.14 | 2.34 | 1.17 to 4.72 |
| Insurance status | ||||
| Insurance (reference) | ||||
| No insurance | 0.89 | 0.50 to 1.60 | ||
Table 4.
Univariate COX proportional hazards models for overall survival by country of birth
| Caribbean born |
US born |
|||
|---|---|---|---|---|
| Univariable | Multivariable | Univariable | Multivariable | |
|
|
||||
| Variable | HR (95 % CI) | HR (95% CI) | HR (95% CI) | HR (95% CI) |
| Age at diagnosis (continuous) | 1.03 (0.99 to 1.07) | 1.03 (0.99 to 1.06) | ||
| Surgery | ||||
| No (reference) | -- | -- | -- | |
| Yes | 0.58 (0.27 to 1.21) | 0.49 (0.26 to 0.93) | 0.42 (0.20 to 0.89) | |
| Hormone antagonism | ||||
| No (reference) | -- | -- | ||
| Yes | 0.37 (0.05 to 2.74) | 0.47 (0.14 to 1.54) | ||
| Chemotherapy | ||||
| No (reference) | -- | -- | ||
| Yes | 1.44 (0.73 to 2.87) | 1.64 (0.91 to 2.96) | ||
| Radiation | ||||
| No (reference) | -- | -- | ||
| Yes | 0.56 (0.24 to 1.30) | 0.47 (0.22 to 1.01) | ||
| Tobacco use | ||||
| Never/former (reference) | -- | -- | ||
| Current | 4.27 (0.56 to 32.4) | 1.07 (0.42 to 2.73) | ||
| Alcohol use | ||||
| Never/former (reference) | -- | -- | ||
| Current | 1.09 (0.26 to 4.63) | 0.36 (0.09 to 1.50) | ||
| Stage of disease | ||||
| Stages I and II (reference) | -- | -- | -- | -- |
| Stages III and IV | 4.79 (2.16 to 10.62) | 3.25 (1.45 to 7.31) | 5.22 (2.77 to 9.82) | 4.22 (2.10 to 8.51) |
| Insurance status | ||||
| Insured (reference) | -- | -- | ||
| No insurance | 0.97 (0.45 to 2.08) | 0.91 (0.36 to 2.32) | ||
| Histologic grade | ||||
| Low grade (reference) | -- | -- | -- | -- |
| High grade | 8.72 (2.08 to 36.51) | 5.57 (1.28 to 24.25) | 4.36 (2.07 to 9.16) | 2.23 (0.98 to 5.07) |
Given the apparent importance of grade in overall survival in the cohort, survival analyses were performed with stratification by grade. The median overall survival among patients with low grade histologies could not be calculated as it was not reached for Caribbean born or US born women. Among women with high grade histologies, the median overall survival was 25.9 months in US born women versus 39.6 months in Caribbean born women, although the difference was not statistically significant (log rank, P=0.25). Figure 2 shows the Kaplan–Meier curve for overall survival among women with high grade histologies. The survival curves intersect, although Caribbean born women appear to have improved long term survival compared with US born women.
Figure 2.
Overall survival by country of birth among women with high grade (type II) endometrial cancers. Caribbean born women had a significantly longer median overall survival (39.6 months versus 25.9 months), with improved long termsurvival, although survival curves do intersect (log rank, P=0.25).
DISCUSSION
Differences clearly exist between black women with endometrial cancer depending on nativity. Here we have shown in our population that Caribbean women are more frequently uninsured, are non-smokers, and have different histologic distributions of high risk disease compared with their US born counterparts. Despite these differences, no survival advantage was appreciated based on nativity. These data are consistent with previous studies in women of similar backgrounds, although in different geographies, and without prior consideration of tumor grade.12
Perhaps the most striking finding of the study was the large proportion of women with high risk, or type II, histologies. Among US born women it was 64.5%, and among Caribbean born women it was 72.2%. Previous epidemiologic studies have reported a much lower prevalence of high grade endometrial cancer in black women. In 2012, Jamison et al published a Surveillance, Epidemiology, and End Results evaluation of women with endometrial cancer diagnosed between 1992 and 2008.6 Among black patients, only 29% had high grade tumors—a stark contrast with that observed in our cohort. This study, however, utilized data from the Surveillance, Epidemiology, and End Results Program, which draws from populations throughout the USA, many of which do not have robust representation from women of Caribbean ancestry. Similar findings to Jamison were reported among black women in a separate population based study by Setiawan et al, in which only 32.7% of women had high grade disease.14 This study, however, used data from Healthcare Financing Administration data files, with representation from only Hawaii and Los Angeles. Interestingly, in a study evaluating a population of black women with uterine cancer in Brooklyn, of whom 61.4% were known to be African or Afro-Caribbean immigrants, 59.3% of the women had high grade tumors.12 Population based studies have also demonstrated that the risk of high grade endometrial cancer varies by Caribbean island, although these data are limited to Latin countries.13 There are clearly factors about this population of black women, and specifically women from the Caribbean, that puts them at greater risk for aggressive histologies. Recent studies have shown that Caribbean women have high rates of inherited mutations in breast cancer genes, which can reach up to 25% of breast cancer patients in some Caribbean islands. Thus genetic predisposition may play a significant role in the pathogenesis of the high grade phenotype in this population.15–17 Additionally, given the recent association between BRCA1 mutations and an increased observation of uterine serous carcinoma,18 genetic predisposition, or potentially epigenetic modification, may also be driving pathogenesis. Thus our finding that more than one-third of Caribbean natives had uterine serous carcinoma is significant, and additional research to understand this observation is needed.
In the multivariable model, patients of Caribbean nativity showed a trend towards improved overall survival. This finding is interesting as, compared with US born women, Caribbean born women had greater risk factors generally associated with worse outcomes. Nearly twice as many Caribbean born women were uninsured compared with US born women in this cohort. Such trends are not uncommon. Immigrants have lower rates of employer provided medical insurance, as well as significant reductions in government insurance programme.19 It has also been reported that immigrants have very little access to information about health insurance plans in their native languages.20 Smoking among Caribbean women, much like US born women, has been on the decline in recent years, and our cohort demonstrated very low rates of smoking.21 Smoking has a well defined protective effect on endometrial cancer development, independent of grade, although no strong impact on survival.22 23 In our study, Caribbean born women also had a higher percentage of stage III diagnoses. No data currently exist on stage distribution or patterns of metastasis in endometrial cancer patients by race or nativity.
Taken in toto, despite greater challenges to accessing care and more cases of advanced stage disease, Caribbean born women had at worst equivalent outcomes with US born blacks, the difference in median overall survival notwithstanding. Creque et al reported similar survival findings in a cohort of multinational urban black women with uterine cancer, although they included uterine sarcomas in the analyses.12 Pinheiro et al used statewide cancer registry data to evaluate mortality among women with endometrial cancer and found that Jamaicans had higher mortality than US born blacks, but that mortality among Haitians and other West Indian women was lower.11 However, patients were not stratified by histologic grade in their analyses. Given that patients with low grade endometrial cancer have an overall excellent prognosis, as seen in the current study when median survival was not reached for either nativity group, failing to consider the influence of grade limits the interpretation of the data.
Our finding that Caribbean born women had non-inferior survival is not necessarily surprising, especially given reported improvements in survival among immigrants for major cancers, cardiovascular disease, and diabetes over the last several decades.24 There are several potential etiologies to explain this finding. The healthy immigrant effect, whereby immigrants have better outcomes, may be a contributing factor. The healthy immigrant effect postulates that immigrants, by the sheer fact that they were healthy enough to leave their home countries, may embody stronger baseline protective factors from disease. Additionally, immigrants more frequently develop robust sociocultural ties, and are thus resistant to the negative effects of acculturation, while also implementing nutritional routines that differ significantly from US natives.11 25 While these effects are not to be minimized, their synergistic effects with other factors such as genetics and pharmacogenomics are important to consider, especially in terms of cancer treatment. Variability in drug metabolism by race has been well described, and although not used in clinical practice routinely to dose chemotherapy, may influence pharmacokinetics that result in prolonged exposure of the tumor to drug or even response to radiotherapy.26 For the larger cohort radiation was associated with survival. This is in contrast with several large prospective trials evaluating postoperative radiation for endometrial cancer, although in those trials race was not reported or evaluated as a mediator of outcome.27 28 The finding that surgery was associated with improved survival for US born black women but not Caribbean born black women is interesting. No data exist regarding gynecologic surgical disparities among immigrants, although disparities in the surgical care of black women have been widely reported.29 Additional study to further explore this finding is needed. Finally, black women with endometrial cancer are known to have unique mutations in the TP53 gene, leading to increased somatic copy number variations,30 as well as chromosomal amplifications, such as chr1q,31 which are associated with higher rates of recurrence and metastatic phenotypes. Epigenetic changes to genes, whether activating or inactivating, may be influenced by nativity mediated environmental exposures, and thus affect expression with appreciable changes in clinical outcomes. Additional study to understand the factors associated with survival in these women is needed.
Our study has several limitations. As a review from the cancer registry over a fixed interval of time, we are limited in our acquisition of patient specific factors that may influence outcome. Compliance with treatment, reasons for treatment delays (eg, complications of surgery or chemotherapy), variations in specific treatment plans, and patient desires for continuation of care are all uncaptured, but in clinical practice are important considerations. Information bias may also be present due to errors in data entry, or incomplete data. A specific consideration for information bias is our limitation in knowing the location of a patient’s death, as migration during treatment will affect data acquisition. The ‘salmon bias’ proposes that immigrants may desire to die in their own birthplace, so as Caribbean born women approach end of life, they may return to their home countries to die.32 While women in our study were censored at the time of the last follow-up, such an effect may skew the data to suggest that immigrant patients are doing better. Additionally, the population was from a single institution. While this may significantly limit treatment variations as patients received similar care from the same physician group, it may limit the interpretation of the results outside of South Florida. Recognizing that there are significant populations of black Caribbean immigrants in other parts of the country, with potentially different environmental exposures or psychosocial approaches to healthcare, future studies should seek to collaboratively involve a greater catchment area to reduce the confounder of geography. Among the US born patients in our cohort, it is likely that many of them had Caribbean ancestry, which dilute the findings given limited admixture with a native US born population. Many of the US born black women may also have been the children of immigrants, practicing the sociocultural norms of their parents. Enforcing strict inclusion criteria, specifically for the nativity variable, was essential to achieve the primary outcome, although likely limited our power to evaluate other covariates in determining survival associations.
As the demographic distribution of the USA continues to diversify, and cancer medicine is increasingly personalized, understanding the effect of immigration, and personal nativity are crucial. Our study suggests that Caribbean born black women may be at a higher risk for aggressive endometrial cancer histologies diagnosed at higher stages, but not suffer negatively in terms of survival. Both endometrial cancer risk and outcomes are likely dependent on factors beyond just surgery and treatment, and may involve complex pharmacogenomics, epigenetic effects, and sociocultural approaches to cancer care. Collaborative research among populations of black Caribbean women across the USA should be encouraged to evaluate the influence of these factors on survival and to better calculate risk estimates for these women. Such endeavors should ultimately suggest interventions aimed at improving screening, individualizing treatments, and optimizing survival outcomes.
Supplementary Material
HIGHLIGHTS.
There are higher rates of type II endometrial cancer histologies among Caribbean black women
Stage distribution varies in black women by nativity
Nativity as a predictor of survival in black women requires further study
Acknowledgments
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial, or not-for-profit sectors.
Footnotes
Additional material is published online only. To view please visit the journal online (http://dx.doi.org/10.1136/ijgc-2019-000347).
Competing interests None declared.
Patient consent for publication None declared.
Ethics approval The study was approved by the University of Miami institutional review board (protocol 2015–1022).
Provenance and peer review Not commissioned; externally peer reviewed.
Data availability statement Data are available upon reasonable request.
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