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American Journal of Epidemiology logoLink to American Journal of Epidemiology
. 2024 May 22;193(11):1564–1575. doi: 10.1093/aje/kwae086

Endometrial cancer survival in populations of African descent

Heidy N Medina 1,2,✉, Frank J Penedo 3,4, Jacqueline Deloumeaux 5, Clarisse Joachim 6, Tulay Koru-Sengul 7,8, Jonathan Macni 9, Bernard Bhakkan 10, Jessica Peruvien 11, Matthew P Schlumbrecht 12,13, Paulo S Pinheiro 14,15
PMCID: PMC13070522  PMID: 38778751

Abstract

To examine whether the endometrial cancer (EC) survival disadvantage among Black populations is US-specific, a comparison between African-descent populations from different countries with a high development index is warranted. We analyzed 28 213 EC cases from cancer registries in Florida (2005-2018) and the French Caribbean islands of Martinique (2005-2018) and Guadeloupe (2008-2018) combined. Kaplan-Meier and all-cause Cox proportional hazards models were used to compare survival. Models were stratified by EC histology type and the main predictor examined was race/ethnicity (non-Hispanic White [NHW] and no-Hispanic Black [NHB] women in the United States versus Black women residing in the Caribbean). For endometrioid and nonendometrioid EC, after adjusting for age, histology, stage at diagnosis, receipt of surgery, period of diagnosis, and poverty level, US NHB women and Caribbean Black women had a higher risk of death relative to US NHW women. There was no difference between US NHB and Caribbean Black women (hazard ratio [HR] = 1.07; 95% CI, 0.88-1.30) with endometrioid EC. However, Caribbean Black women with nonendometrioid carcinomas had a 40% higher risk of death (HR = 1.40; 95% CI, 1.13-1.74) than US NHB women. The low EC survival among US Black women extends to foreign populations of African descent. For the aggressive nonendometrioid ECs, survival among Caribbean Black women outside of the United States is considerably worse.

This article is part of a Special Collection on Gynecological Cancers.

Keywords: endometrial cancer, Black, African descent, Caribbean, survival, endometroid, nonendometrioid, registry

Introduction

Women of African descent in the United States have higher mortality rates and the lowest survival of any racial/ethnic group for most cancers.1,2 This disparity is particularly evident for endometrial cancer (EC), the fifth leading cause of cancer death among women of African descent, with a mortality rate that has increased nearly 2% annually from 2004 to 2019, almost double that of White women.2 The 21% gap in 5-year survival between Black and White women for EC as a whole is the most pervasive inequality of any cancer site.1,2

The nature of this Black-White disparity in EC outcomes is suggested to be multifactorial, encompassing clinical, genetic, and sociodemographic factors.3-5 This constitutes tumor characteristics such as later stage at diagnosis, higher grade, as well as biological factors such as aggressive histologies and distinct molecular genetic mutations.3,5-12 Studies have shown that women of African descent have worse survival outcomes by histology type at every stage at diagnosis,2,10-14 suggesting the interplay among multiple factors, including social factors, in determining health outcomes. These include treatment-related disparities in access and use of health care resources, timeliness and receipt of guideline-concordant care, and comorbidities.3,6,15-18 Socioeconomic status and cultural barriers (eg, fatalism, mistrust) that lead to differences in treatment have also been cited as contributing factors to this marked racial/ethnic disparity.3,6,18

Past research has compared survival outcomes between White women and women of African descent, considering the latter as a homogenous group.4,8,9,11-14,19,20 To our knowledge, only 1 study has examined the intraracial difference in survival for EC among African-descent populations, specifically among the more aggressive EC histology types (ie, high-grade endometrioid, serous, clear cell, carcinosarcoma, mixed cell), for US-born, Caribbean-born, and Hispanic Black women.21 However, this prior work was limited to examining African-descent populations only residing in the United States.

Structural racism has been suggested to have direct and indirect effects on poor health outcomes in the United States through deficient social and built environments, exposures to pollutants and toxins, limited educational opportunities and employment, and less-than-ideal access to quality health care.22 In this context, we wanted to disentangle whether the well-documented survival disadvantage among women of African descent is a phenomenon specific to the United States. Currently, a comparison between populations of African descent from countries with a high development index is lacking. By comparing populations with a shared ancestral background that are exposed to geographically diverse environments with differing health care systems, we will be able to shed light on the specific context of this persistent racial/ethnic disparity. Leveraging population-based registry data, we will examine regional differences in EC disparities among African-descent populations that have yet to be explored and would otherwise prove difficult to discern. This comparative analysis can inform current research priorities, public health strategies, and studies focused on targeted interventions to address the interplay between the role of ancestry and structural and social determinants of health in cancer outcomes.

International population-based analyses of African-descent groups can be difficult because demographic data on race are not commonly collected in Europe, Latin America, or the Caribbean. Due to low resource settings in African country registries, data availability and completeness of registry data are problematic.23 Two likely exceptions are the islands of Martinique and Guadeloupe, Caribbean departments of France of majority African-origin populations with a high level of development, universal basic health coverage, and complete and high-quality registry data.24,25 In the United States, Florida is uniquely positioned, having the second-highest number of newly diagnosed cancer cases and also being home to the second largest Black population (n = 3.8 million) in the country.26,27 Florida is demographically diverse, with Black people composing 17% of the total population, and nearly 20% are of Caribbean origin.28 In this study, we aimed to elucidate the survival differences for EC among African-descent populations in the United States (US-born Black women residing in Florida) and the French Caribbean (Martinique and Guadeloupe).

Methods

Data sources and population

Data were retrieved for first primary EC cases diagnosed during 2005 to 2018 from the Florida Cancer Data System, the statewide cancer registry; 2005 to 2018 from the Martinique Cancer Registry; and 2008 to 2018 from the Guadeloupe Cancer Registry. Cases of primary site codes C54.X and C55.9 and morphology codes 8000-8951 per the International Classification of Disease, for Oncology, 3rd edition (ICD-O-3)29 were included. The Florida Cancer Data System has consistently met the North American Association of Central Cancer Registries’ Gold Standard for Registry Certification, with greater than 95% complete, accurate, and timely data.30 The cancer registries of Martinique and Guadeloupe are both members of the International Association of Cancer Registries, the French Network of Cancer Registries, and the European Network of Cancer Registries.31,32 High-quality data are guaranteed by cross-matching and evaluating various data sources, which include pathology reports, hospital discharge records, laboratory results, long-term illness registration by the health insurance system, and individual medical files.31-33

Variables obtained from the registries included sociodemographic characteristics such as race/ethnicity and birthplace (Florida only), age at diagnosis, and a socioeconomic status indicator, as well as tumor-related characteristics such as date of diagnosis, vital status, date of death, morphology (histology), stage at diagnosis (according to the Fédération Internationale de Gynécologie et d'Obstétrique [FIGO; International Federation of Gynecology and Obstetrics]), sequence number, and receipt of surgery. Among all non-Hispanic Black women in Florida (hereafter referred to as US NHB women), there are 3 distinct groups that can only be categorized based on birthplace: 2 major ones, US-born Black women (ie, African American women) and US Afro Caribbean women,34,35 and another much smaller group of US women of African descent born in Africa, Europe, or other regions (ie, “other birthplace”). US NHB women with unknown birthplace were assigned to either the US-born Black, US Afro-Caribbean, or the other birthplace African-descent group based on the majority group in the defined census-tract, using methodology described elsewhere.21 We excluded the US Afro-Caribbean and the other birthplace group from our study to exclusively compare US-born Black women and the French Caribbean women, 2 African-descent populations that are distinct and without intermigration between the United States and the Caribbean. Differences between US-born Black women and US Afro-Caribbean women were reported in a prior study.21 Non-Hispanic White women in the United States (US NHW women) were included as a reference population. The aggregate population of Martinique and Guadeloupe is subsequently referred to as Caribbean Black. Socioeconomic status was categorized, using census tract data in Florida, into a poverty indicator as follows: low (<10%), moderate (between 10% and 20%), high (>20%) poverty, and unknown.36 In the case of Martinique and Guadeloupe, a social deprivation index previously created using census data37 was also categorized as a poverty indicator according to low, moderate, and high levels of poverty.

For Florida, Martinique, and Guadeloupe, EC cases were classified as endometrioid, nonendometrioid, and other histology subtypes (with ICD-O-3 codes) as follows: endometrioid (8050, 8140, 8143, 8210–8211, 8260–8263, 8340, 8380–8384, 8560, 8570) and nonendometrioid (clear cell [8310], carcinosarcoma [8950–8951, 8980–8981], and serous [8441, 8460–8461]), and other (neuroendocrine [8013, 8041, 8045–8046, 8574], undifferentiated [8020], and general histologic descriptions [eg, 8000, 8010]) as in previous research.12 Sarcomas of the corpus uterus and gestational trophoblastic tumors were excluded. The stage at diagnosis was classified according to FIGO staging: FIGO I (FIGO IA, IB, IC, and FIGO stage I not further specified), FIGO II (FIGO stage IIA, IIB, or FIGO stage II not otherwise specified), FIGO III (FIGO stage IIIA, IIIB, and IIIC), FIGO IV (IVA, IVB), and unknown.38

Data analyses

We assessed the frequency distributions for all sociodemographic and tumor-related characteristics for US NHW, US NHB, and Caribbean Black women and used χ2 tests to determine differences. We excluded patients who had negative survival time and those diagnosed at autopsy or by death certificate only. For all 3 cancer registries, survival was defined as the elapsed time, in days, from the date of EC diagnosis to the date of death, or the date of last mortality linkage, December 31, 2018, whichever occurred first. The outcome of interest was death from all causes. Those cases not found to be deceased on the last date covered (December 31, 2018) were censored as alive. The Kaplan-Meier method39 was used to estimate the survival proportions for US NHW, US NHB, and Caribbean Black women among all EC cases combined and by histology type (Figure 1). The log-rank test with a Bonferroni correction was used to compare survival functions across groups. Univariable and multivariable Cox proportional hazard regression models for all-cause survival were used to produce hazard ratios (HRs) with corresponding 95% CIs reflecting the risk of death by specific racial/ethnic group and African-descent group after adjustment for relevant covariates (ie, age, histology, stage at diagnosis, grade, receipt of surgery, period of diagnosis, and poverty level). Models were stratified by histology type (endometrioid versus nonendometrioid). The proportional hazards assumption was tested by inspecting the Kaplan-Meier survival curves by racial/ethnic group and testing the correlation between scaled Schoenfeld residuals and survival time.

Figure 1.

Figure 1

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Kaplan-Meier all-cause survival for US non-Hispanic White (NHW), US non-Hispanic Black (NHB), and Caribbean Black women with endometrial cancer (EC) by histology type: Florida (2005-2018), Martinique (2005-2018), and Guadeloupe (2008-2018). A) All EC combined. B) Endometrioid EC. C) Nonendometrioid EC.

(Figure 1 continues) .

(Figure 1 continues)

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Analyses were conducted using SAS, version 9.4, software (SAS Institute). All statistical tests were 2-sided with a statistical significance of P < .05. Approvals were obtained from the Florida Department of Health and the University of Miami Institutional Review Board for Florida and necessary authorized officials from the respective cancer registries in Martinique and Guadeloupe.

Results

Patient sociodemographic and clinical characteristics

From 2005 to 2018, a total of 28 213 first primary EC cases were identified from Florida, Martinique, and Guadeloupe (Table 1), which included 24 216 cases among US NHW women, 3140 among US NHB women, and 857 among Caribbean Black women. There were 7544 total deaths recorded among all EC cases, with 6005 (25%), 1163 (37%), and 376 (44%) among US NHW, US NHB, and Caribbean Black cases, respectively. US NHB and NHW women were more likely to be diagnosed between 55 and 64 years of age (37% and 33%, respectively), and Caribbean Black women were more commonly diagnosed between 65 and 74 years of age (34%) (P < .0001). Caribbean Black women had a higher proportion of those diagnosed in the oldest age group (ie, >75 years; 29%) than US NHW women (18%) and US NHB women (14%) (P < .0001). US NHB women were more likely to live in areas of relative (within country) high poverty (54%) than US NHW women (17%) and Caribbean Black women with EC (30%) (P < .0001). US NHB women had a higher proportion of nonendometrioid EC histology types (31%), and they had the greatest proportion of stage IV tumors (12%). A higher proportion of patients in the United States (92% for NHW women and 84% for NHB women) underwent surgery than in the Caribbean (73%) (P < .0001).

Table 1.

Sociodemographic and clinical characteristics of endometrial cancer cases: Florida (2005-2018), Martinique (2005-2018), and Guadeloupe (2008-2018)

White African descent
US NHW, no. (%) US NHB, no. (%) Caribbean Black, no. (%) P value a
Total 24 216 3140 857
Median age, y
Endometrioid 63 61 67
Nonendometrioid 68 66 68
All combined 64 63 68
Age group, y, no. (%) <.0001
 15-44 1151 (4.8) 230 (7.3) 21 (2.5)
 45-54 3236 (13.4) 367 (11.7) 63 (7.4)
 55-64 7979 (33.0) 1164 (37.1) 233 (27.2)
 65-74 7427 (30.7) 941 (30.0) 295 (34.4)
 ≥75 4423 (18.3) 438 (14.0) 245 (28.6)
Poverty level, no. (%) <.0001
 Low 11 042 (45.6) 498 (15.9) 321 (37.5)
 Moderate 8954 (37.0) 910 (29.0) 245 (28.6)
 High 3992 (16.5) 1701 (54.2) 258 (30.1)
 Unknown 228 (0.9) 31 (1.0) 33 (3.9)
Histologic subtype, no. (%) <.0001
 Endometrioid 20 087 (83.0) 1987 (63.3) 581 (67.8)
 Nonendometrioid 3394 (14.0) 974 (31.0) 216 (25.2)
 Other 735 (3.0) 179 (5.7) 60 (7.0)
FIGO stage, no. (%) <.0001
 I 14 856 (61.4) 1532 (48.8) 310 (36.2)
 II 2375 (9.8) 363 (11.6) 89 (10.4)
 III 2360 (9.8) 359 (11.4) 94 (11.0)
 IV 1454 (6.0) 366 (11.7) 27 (3.2)
 Unknown 3171 (13.1) 520 (16.6) 337 (39.3)
Surgery, no. (%) <.0001
 No 1908 (7.9) 492 (15.7) 136 (15.9)
 Yes 22 215 (91.7) 2630 (83.8) 629 (73.4)
 Unknown 93 (0.4) 18 (0.6) 92 (10.7)
Vital status, no. (%) <.0001
 Dead 6005 (24.8) 1163 (37.0) 376 (43.9)
 Alive 18 211 (75.2) 1977 (63.0) 481 (56.1)
Median survival time, y
 Endometrioid —b — 12.8
 Nonendometrioid 6.1 2.9 1.8
 All combined — 10.1 5.9
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Abbreviations: EC, endometrial cancer; FIGO, Fédération Internationale de Gynécologie et d'Obstétrique; NHB, non-Hispanic Black; NHW, non-Hispanic White.

a  P value from χ2 test.

b Median survival was not estimable.

Kaplan-Meier survival

There was an observed difference in Kaplan-Meier all-cause survival among US NHW, US NHB, and Caribbean Black women for all EC cases combined (Figure 1A) and by histological type (Figure 1B and C) (P < .0001 for all by log-rank test). Overall, for all EC cases combined, Kaplan-Meier, all-cause, 5-year survival was 77.1% (95% CI, 76.5-77.7) for US NHW women, 60.9% (95% CI, 58.9, 62.8) for US NHB women, and 52.3% (95% CI, 48.5, 56.0) for Caribbean Black women. For endometrioid ECs, 5-year overall survival for US NHW women was 82.5% (95% CI, 81.9, 83.1), 74.2% (95% CI,72.0-76.3) for US NHB women, and 63.9% (95% CI, 59.3, 68.1) for Caribbean Black women ; for nonendometrioid ECs, it was 52.5% (95% CI, 50.5, 54.4), 38.4% (95% CI, 34.7-42.1), and 26.1% (95% CI, 19.4-33.2) for US NHW, US NHB, and Caribbean Black women, respectively.

Cox regression: all EC cases combined

For all EC cases combined, US NHB and Caribbean Black women had an approximately 2-fold higher risk of death (HR = 2.05 [95% CI, 1.92-2.18]; HR = 2.00 [95% CI, 1.80-2.22], respectively) from all-causes in comparison with US NHW women after adjustment for age (Table 2, model 1). For intraracial comparisons, there was no difference in risk of death for Caribbean Black women in comparison with US NHB women (HR = 1.01; 95% CI, 0.89-1.13). After adjusting for age, histology, stage at diagnosis, receipt of surgery, period of diagnosis, and poverty level (Table 2, model 4), US NHB women had 31% higher all-cause mortality (HR = 1.31; 95% CI, 1.22-1.40) in comparison with US NHW women, and Caribbean Black women had a 59% higher risk of death (HR = 1.59; 95% CI, 1.42-1.77). Among African-descent groups exclusively, Caribbean Black women had a 22% (HR = 1.22, 95% CI, 1.06-1.39) higher risk of death than US NHB women.

Table 2.

All-cause survival, Cox proportional hazard ratios for all endometrial cancer cases combined: Florida (2005-2018), Martinique (2005-2018), and Guadeloupe (2008-2018)

Prognostic factor Deaths Model 1 Model 2 Model 3 Model 4
No. per total HR (95% CI) P value HR (95% CI) P value HR (95% CI) P value HR (95% CI) P value
Age group, y
 15-44 158/1402 1 (Referent) 1 (Referent) 1 (Referent) 1 (Referent)
 45-54 527/3666 1.32 (1.11-1.58) .002 1.34 (1.12-1.60) .001 1.31 (1.09-1.56) .003 1.37 (1.15-1.64) .001
 55-64 1836/9376 1.99 (1.69-2.34) <.0001 1.94 (1.64-2.28) <.0001 1.96 (1.67-2.31) <.0001 2.04 (1.73-2.40) <.0001
 65-74 2365/8663 3.12 (2.66-3.67) <.0001 2.88 (2.45-3.39) <.0001 2.89 (2.46-3.39) <.0001 2.97 (2.52-3.49) <.0001
 ≥75 2658/5106 7.02 (5.98-8.25) <.0001 6.11 (5.20-7.18) <.0001 5.94 (5.06-6.98) <.0001 5.72 (4.87-6.72) <.0001
Histology
 Endometrioid 4819/22655 1 (Referent) 1 (Referent) 1 (Referent)
 Nonendometrioid 2115/4584 2.48 (2.35-2.62) <.0001 1.62 (1.54-1.72) <.0001 1.74 (1.64-1.84) <.0001
 Other 610/974 4.12 (3.79-4.49) <.0001 2.27 (2.07-2.49) <.0001 1.92 (1.75-2.11) <.0001
FIGO stage
 I 2786/16698 1 (Referent) 1 (Referent)
 II 807/2827 1.83 (1.69-1.98) <.0001 1.80 (1.66-1.95) <.0001
 III 1454/2813 3.40 (3.19-3.63) <.0001 3.30 (3.09-3.52) <.0001
 IV 1496/1847 9.72 (9.08-10.40) <.0001 7.44 (6.92-7.99) <.0001
 Unknown 1001/4028 3.09 (2.85-3.35) <.0001 1.86 (1.70-2.04) <.0001
Surgery
 No 1686/2536 1 (Referent)
 Yes 5767/25474 0.35 (0.32-0.37) <.0001
 Unknown 91/203 0.52 (0.42-0.65) <.0001
Period of diagnosis
 2005-2008 2715/6670 1 (Referent)
 2009-2013 3005/9725 0.93 (0.88-0.99) .014
 2014-2018 1824/11818 0.88 (0.82-0.94) .0001
Poverty level
 Low 2953/11861 1 (Referent)
 Moderate 2706/10109 1.12 (1.06-1.18) <.0001
 High 1801/5951 1.25 (1.17-1.33) <.0001
 Unknown 84/292 0.84 (0.67-1.06) .135
Race/ethnicity
 White
 US NHW 6005/24216 1 (Referent) 1 (Referent) 1 (Referent) 1 (Referent)
 African descent
 US NHB 1163/3140 2.05 (1.92-2.18) <.0001 1.67 (1.57-1.79) <.0001 1.53 (1.43-1.63) <.0001 1.31 (1.22-1.40) <.0001
 Caribbean Black 376/857 2.00 (1.80-2.22) <.0001 1.72 (1.55-1.91) <.0001 1.54 (1.38-1.71) <.0001 1.59 (1.42-1.77) <.0001
African descent groupa
 US NHB 1163/3140 1 (Referent) 1 (Referent) 1 (Referent) 1 (Referent)
 Caribbean Black 376/857 1.01 (0.89-1.13) .915 1.08 (0.96-1.22) .207 1.04 (0.91-1.18) .580 1.22 (1.06-1.39) .004
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Abbreviations: EC, endometrial cancer; FIGO, Fédération Internationale de Gynécologie et d'Obstétrique; HR, hazard ratio; NHB, non-Hispanic Black; NHW, non-Hispanic White.

a Hazard ratios obtained from separate models with only the given groups.

Cox regression: endometrioid EC

For endometrioid types, in multivariable analysis adjusting only for age (Table 3, model 1), US NHB and Caribbean Black women had an 80% higher risk of all-cause mortality (HR = 1.77 [95% CI, 1.61-1.93]; HR = 1.79 [95% CI, 1.55-2.07], respectively) than US NHW women. When examining intraracial differences, Caribbean Black women did not have a higher risk of death than US NHB women (HR = 1.03; 95% CI, 0.87-1.21) after adjusting for age. After full adjustment (Table 3, model 3), a higher risk of all-cause death was observed for US NHB women (HR = 1.28; 95% CI, 1.16-1.41) and Caribbean Black women (HR = 1.32; 95% CI, 1.14-1.54) in comparison with US NHW women. When comparing African-descent groups only, there was no difference between US NHB and Caribbean Black women (HR = 1.07; 95% CI, 0.88-1.30).

Table 3.

All-cause survival, Cox proportional hazard ratios for endometrioid histologic subtype cases: Florida (2005-2018), Martinique (2005-2018), and Guadeloupe (2008-2018)

Prognostic factor Deaths Model 1 Model 2 Model 3
No. per total HR (95% CI) P value HR (95% CI) P value HR (95% CI) P value
Age group, y
 15-44 117/1251 1 (Referent) 1 (Referent) 1 (Referent)
 45-54 384/3273 1.28 (1.04-1.57) .020 1.31 (1.06-1.61) .012 1.38 (1.12-1.69) .003
 55-64 1169/7789 1.80 (1.49-2.18) <.0001 1.91 (1.58-2.31) <.0001 2.00 (1.65-2.42) <.0001
 65-74 1444/6697 2.89 (2.39-3.49) <.0001 3.00 (2.48-3.62) <.0001 3.11 (2.58-3.76) <.0001
 ≥75 1705/3645 7.24 (6.00-8.74) <.0001 7.16 (5.93-8.64) <.0001 7.04 (5.83-8.50) <.0001
FIGO stage
 I 2247/14855 1 (Referent) 1 (Referent)
 II 504/2125 1.74 (1.58-1.92) <.0001 1.74 (1.58-1.91) <.0001
 III 869/1950 3.42 (3.16-3.70) <.0001 3.37 (3.12-3.65) <.0001
 IV 693/889 12.22 (11.21-13.33) <.0001 8.51 (7.74-9.36) <.0001
 Unknown 506/2836 3.58 (3.24-3.96) <.0001 1.82 (1.61-2.05) <.0001
Surgery
 No 965/1585 1 (Referent)
 Yes 3810/20957 0.30 (0.28-0.33) <.0001
 Unknown 44/113 0.54 (0.40-0.75) .0002
Period of diagnosis
 2005-2008 1962/5535 1 (Referent)
 2009-2013 1929/7884 0.93 (0.87-1.00) .041
 2014-2018 928/9236 0.89 (0.82-0.97) .008
Poverty level
 Low 1923/9716 1 (Referent)
 Moderate 1756/8150 1.20 (1.13-1.28) <.0001
 High 1086/4565 1.35 (1.25-1.47) <.0001
 Unknown 54/224 0.99 (0.75-1.30) .928
Race/ethnicity
 White
 US NHW 4094/20 087 1 (Referent) 1 (Referent) 1 (Referent)
 African descent
 US NHB 530/1987 1.77 (1.61-1.93) <.0001 1.53 (1.40-1.68) <.0001 1.28 (1.16-1.41) <.0001
 Caribbean Black 195/581 1.79 (1.55-2.07) <.0001 1.29 (1.11-1.50) .001 1.32 (1.14-1.54) .0003
African descent groupa
 US NHB 530/1987 1 (Referent) 1 (Referent) 1 (Referent)
 Caribbean Black 195/581 1.03 (0.87-1.21) .755 0.87 (0.73-1.04) .129 1.07 (0.88-1.30) .483
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Abbreviations: FIGO, Fédération Internationale de Gynécologie et d'Obstétrique; HR, hazard ratio; NHB, non-Hispanic Black; NHW, non-Hispanic White.

a Hazard ratios obtained from separate models with only the given groups.

Cox regression: nonendometrioid EC

Among nonendometrioid ECs, after adjusting for age (Table 4, model 1), US NHB women had a 50% higher risk of death (HR = 1.51; 95% CI, 1.36-1.67) than US NHW women, and Caribbean Black women had almost 2 times higher risk (HR = 1.99; 95% CI, 1.67-2.36). Intraracial comparisons showed a 34% increased risk of death from all-causes (HR = 1.34; 95% CI, 1.11-1.61) for Caribbean Black women in comparison with US NHB women. In the fully adjusted model (Table 4, model 4), US NHB and Caribbean Black women had a 23% and 79% higher risk of all-cause mortality, respectively, compared with US NHW women (HR = 1.23 [95% CI, 1.10-1.37]; HR = 1.79 [95% CI, 1.48-2.15]). Comparing African-descent groups only, Caribbean Black women with nonendometrioid carcinomas had a 40% (HR = 1.40; 95% CI, 1.13-1.74) higher risk of death than US NHB women.

Table 4.

All-cause survival, Cox proportional hazard ratios for nonendometrioid histologic subtype cases: Florida (2005-2018), Martinique (2005-2018), and Guadeloupe (2008-2018)

Prognostic factor Deaths Model 1 Model 2 Model 3 Model 4
No. per total HR (95% CI) P value HR (95% CI) P value HR (95% CI) P value HR (95% CI) P value
Age group, y
 15-44 21/81 1 (Referent) 1 (Referent) 1 (Referent) 1 (Referent)
 45-54 89/280 1.12 (0.70-1.80) .643 1.15 (0.72-1.86) .556 1.24 (0.77-1.99) .381 1.15 (0.72-1.86) .557
 55-64 533/1345 1.56 (1.01-2.42) .045 1.47 (0.95-2.28) .084 1.80 (1.16-2.79) .008 1.68 (1.08-2.61) .021
 65-74 772/1721 2.01 (1.30-3.10) .002 1.82 (1.18-2.82) .007 2.30 (1.49-3.55) .0002 2.15 (1.39-3.33) .001
 ≥75 700/1157 3.10 (2.01-4.79) <.0001 2.81 (1.82-4.35) <.0001 3.53 (2.28-5.45) <.0001 3.17 (2.05-4.91) <.0001
Histology
 Clear cell 172/424 1 (Referent) 1 (Referent) 1 (Referent)
 Mixed 310/1040 0.76 (0.63-0.91) .004 0.78 (0.65-0.94) .010 0.80 (0.67-0.97) .021
 Carcinosarcoma 802/1371 1.90 (1.61-2.24) <.0001 1.68 (1.42-1.98) <.0001 1.69 (1.43-1.99) <.0001
 Serous 831/1749 1.36 (1.16-1.61) .0002 1.07 (0.91-1.27) .407 1.10 (0.94-1.31) .222
FIGO stage
 I 485/1672 1 (Referent) 1 (Referent)
 II 274/654 1.72 (1.48-2.00) <.0001 1.71 (1.47-1.98) <.0001
 III 534/798 2.97 (2.63-3.37) <.0001 2.89 (2.55-3.27) <.0001
 IV 601/733 6.14 (5.43-6.95) <.0001 5.59 (4.93-6.35) <.0001
 Unknown 221/727 2.64 (2.24-3.12) <.0001 1.86 (1.55-2.25) <.0001
Surgery
 No 333/466 1 (Referent)
 Yes 1761/4081 0.50 (0.44-0.57) <.0001
 Unknown 21/37 0.87 (0.55-1.37) .548
Period of diagnosis
 2005-2008 562/849 1 (Referent)
 2009-2013 856/1515 0.94 (0.85-1.05) .299
 2014-2018 697/2220 0.88 (0.78-0.99) .039
Poverty level
 Low 815/1807 1 (Referent)
 Moderate 731/1614 1.00 (0.91-1.11) .988
 High 550/1123 1.09 (0.97-1.23) .146
 Unknown 19/40 0.77 (0.48-1.21) .256
Race/ethnicity
 White
 US NHW 1468/3394 1 (Referent) 1 (Referent) 1 (Referent) 1 (Referent)
 African descent
 US NHB 506/974 1.51 (1.36-1.67) <.0001 1.38 (1.25-1.53) <.0001 1.32 (1.19-1.46) <.0001 1.23 (1.10-1.37) .0003
 Caribbean Black 141/216 1.99 (1.67-2.36) <.0001 1.69 (1.42-2.01) <.0001 1.78 (1.48-2.13) <.0001 1.79 (1.48-2.15) <.0001
African descent groupa
 US NHB 506/974 1 (Referent) 1 (Referent) 1 (Referent) 1 (Referent)
 Caribbean Black 141/216 1.34 (1.11-1.61) .003 1.27 (1.05-1.54) .014 1.34 (1.09-1.64) .006 1.40 (1.13-1.74) .002
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Abbreviations: FIGO, Fédération Internationale de Gynécologie et d'Obstétrique; HR, hazard ratio; NHB, non-Hispanic Black; NHW, non-Hispanic White.

a Hazard ratios obtained from separate models with only the given groups.

Discussion

In this population-based study, we compared the survival experience for EC among two distinct African-descent populations—US NHB women and Caribbean Black women—who are residing in regions with high-quality health care infrastructure, with that of US NHW women. For endometrioid and nonendometrioid ECs alike, US NHB and Caribbean Black women had an overall higher risk of death in comparison with US NHW women after accounting for sociodemographic and clinical-related characteristics. However, although intraracial comparisons showed similar survival between US NHB and Caribbean Black women for endometrioid tumors, Caribbean Black women had disproportionately poor survival for the more fatal nonendometrioid histologies. In the context of a universal health care system (ie, that of the French Caribbean), these latter findings are surprising and inform future studies examining the prognostic factors implicated in the survival disparity currently observed for this increasingly important cancer in the United States and other countries worldwide.

In line with previous research,4,8,9,11-14,19,20 US NHB women had a survival disadvantage for both endometrioid and nonendometrioid ECs compared with US NHW populations. Possible explanations in previous work have suggested biological, genetics-based differences and socioenvironmental factors. Racial/ethnic disparities in the molecular profile of ECs have been observed with differences in TP53, PIK3CA, and KRAS mutations and Her-2 oncogene expression between Black and White women.18,40-43 Studies evaluating the correlation between genetic admixture and clinicopathologic factors have uncovered an association between increased African ancestry and worsened survival for EC.44,45 In the United States, however, the inequitable distribution of health care quality and access has been a widely supported hypothesis for poor EC outcomes for women of African descent. Black women are comparatively less likely to receive guideline-concordant treatment9,15 and to be treated across every stage at diagnosis.9 With 18% of Black women living below the poverty level,46 limited financial means can lead to difficulties with insurance coverage, problems with transportation for clinical visits, and availability of resources to have an adequate diet and self-care during treatment. In this respect, we were interested in comparing African-descent populations in the United States with those residing in other regions. Martinique and Guadeloupe, as French overseas departments, both benefit from the French government’s universal health insurance plans, which grant access to health care to the entire population,47 and strides have been made in terms of cancer control efforts in these territories to create cooperative programs with mainland France.48 However, we found dissimilar outcomes depending on EC type: similar for endometrioid but worse survival for nonendometrioid EC among Caribbean Black women.

Despite receiving care in an equal-access health care system, there are contributing factors that could play a role in the survival disadvantage seen in the French Caribbean. The increased risk of death could be attributed to the quality of the health care infrastructure. There is currently a shortage of health care professionals, specifically a lack of specialized physicians, including obstetrics and gynecologists.47 As such, there is inadequate access to follow-up care and psychiatry resources, which affect survival outcomes.47 The Caribbean region has some of the lowest rates of clinical trial registrations worldwide,49 thereby limiting access to novel therapies, which may be suggestive of differences in treatment protocols for these more aggressive serous and carcinosarcoma histology types. As overseas small-island entities, Martinique and Guadeloupe are heavily dependent on metropolitan France, and all pharmaceuticals are imported, which, depending on budgetary concerns and availability of specific drugs or treatments, can create further delays in care and affect the quality of care.47 Additionally, there may be slower adoption of technological advances. Martinique, for example, does not yet have access to positron emission tomography–computed tomography devices.50 Moreover, traditional and holistic medicine is an ingrained part of society,51 which may become a barrier to receiving recommended, contemporary medicine oncology care. A trend toward higher preponderance and worse survival outcomes in p53 abnormal tumors have also been found among Caribbean Black women.52 The widespread use of pesticides, specifically chlordecone, in banana plantations has been a recently highly examined exposure in Martinique and Guadeloupe.53 As a possible carcinogen that works as an endocrine disruptor affecting estrogen and progesterone activities, studies have found an association between chlordecone and prostate cancer.53 Therefore, the extent to which this exposure may be involved in other hormone-related cancers, such as EC, and its association with the severity of tumors and clinical outcomes requires further research.

It is of note that US Black women with EC did not fare worse than other African-descent populations in a similarly developed context. Historically rooted and culturally reinforced, systemic racism in the United States plays a role in social determinants of health, including, but not limited to, engagement with the medical community and resource acquisition (medical and nonmedical), potentially affecting US Black women in a way not experienced by those in Martinique and Guadeloupe. However, in our study, US Black women with nonendometroid EC had superior survival compared with Caribbean Black women before and after considering clinical and sociodemographic factors. For this reason, although African-descent populations are underserved communities in the United States, the extent to which this is an influencing factor in comparison with other countries remains a question. In a Surveillance Epidemiology and End Results–based study, US Black women with EC, and contrary to the patterns seen for breast cancer, were more likely to be treated by a specialist (ie, gynecologic oncologist) at medical school–affiliated, high-volume, larger, urban, National Cancer Institute Cancer Center–status hospitals than were their White counterparts.54 Therefore, although Black women in the United States may experience multidimensional barriers to quality care, an overall strong health infrastructure, which includes a vast number of specialists, clinical trials, health care technology, and the latest treatment advances, may still be an influencing factor in comparison with other regions worldwide. These findings suggest an incomplete understanding of what is driving current EC disparities; specifically, on one hand, the mechanisms by which racial discrimination and bias may lead to differential outcomes, and on the other hand, the need to identify additional prognostic factors that uniformly influence low survival in populations of African descent that are potentially not yet captured in our medical data.

There are several notable strengths and some limitations of our study. First, our study is among the very few to pool data from independent African-descent population registries to examine survival disparities within the same broadly defined racial group. All 3 registries have high-quality data; for example, the Martinique Cancer Registry data have been included in the Cancer Incidence in Five Continents publication of the World Health Organization since 198155 and have been awarded the top grade by the French Registry Evaluation Committee.56 Second, this is a population-based study that uses all cases of EC inclusive of all women of reported Black race irrespective of missing birthplace data, thereby limiting the effects of selection bias on survival estimates.57

In terms of limitations, because there are no available data on race for Martinique and Guadeloupe,58 all cases of EC were included with the assumption that these are majority African-origin populations (about 91% Black and/or mixed Black and only 5% White).24 Therefore, not all women may be of African descent, and survival may consequently be slightly overestimated among Caribbean Black women in our study. Cause of death data are not available in Caribbean registries; therefore, all-cause rather than cause-specific survival was analyzed. We were restricted to analyzing EC histology according to endometrioid and nonendometrioid subtypes based on a higher proportion of cases with unknown grade precluding an assessment of low-grade endometrioid EC versus high-grade endometrioid EC, serous, clear cell, carcinosarcoma, and mixed-cell subtypes. Furthermore, there are no specific treatment-related data such as specific surgical procedures performed, adherence, and completion of guideline-based care, which are prognostic factors in cancer care. Additionally, due to a large amount of incomplete data on receipt of chemotherapy and radiotherapy in the French Caribbean, we were unable to account for the impact that adjuvant treatment may have on the observed survival disparities between US and Caribbean Black women. However, it is unlikely that this would change our relative results; rather, it might change the magnitude of the survival disadvantage. There may be differences in receipt of adjuvant treatment between the United States and French Caribbean, which might be indicative of variability in patient preferences, physician recommendations, comorbidities, proximity to treatment providers, and availability or access to treatment options. Last, the socioeconomic status indicators are standardized metrics within each registry, but low, moderate, and high poverty levels may be less equivalent concepts between the United States and the French Caribbean. However, the regions of Martinique and Guadeloupe were chosen as the focus of this study in part because, similar to the United States, they have a comparable “very high” human development index.59

In summary, this study compares the survival profile of women with EC who are of African descent in the United States versus those in the French Caribbean. We found similar outcomes for endometrioid but disproportionately lower survival for Caribbean Black women with nonendometrioid EC. Although the current survival gap between women of African descent and White women in the United States may extend to other countries abroad, colorblind cancer registry data collection is currently an impediment to examining this, because race, by law, is not allowed to be recorded in some countries.58 Further studies comparing EC survival between the French Caribbean and mainland France populations are warranted.

Population-based studies examining EC in women of African descent, such as this one, are important in documenting the persistent Black-White disparity to maximize efforts to address and diminish widening inequalities. The mechanisms by which this disparity proliferates remain undetermined; however, our findings suggest that emphasis on socioenvironmental factors could translate to an overall improved prognosis in African-descent populations internationally.

Acknowledgments

This collaboration was facilitated by the African-Caribbean Cancer Consortium (AC3) network, of which several collaborators are members.

Contributor Information

Heidy N Medina, Department of Public Health Sciences, University of Miami School of Medicine, Miami, FL 33136, United States; Sylvester Comprehensive Cancer Center, University of Miami School of Medicine, Miami, FL 33136, United States.

Frank J Penedo, Sylvester Comprehensive Cancer Center, University of Miami School of Medicine, Miami, FL 33136, United States; Department of Psychology, College of Arts and Sciences, University of Miami, Miami, FL 33146, United States.

Jacqueline Deloumeaux, Guadeloupe Cancer Registry, University Hospital of Guadeloupe, Les Abymes 97142, Guadeloupe.

Clarisse Joachim, Martinique Cancer Registry, University Hospital of Martinique, Fort de France 97261, Martinique.

Tulay Koru-Sengul, Department of Public Health Sciences, University of Miami School of Medicine, Miami, FL 33136, United States; Sylvester Comprehensive Cancer Center, University of Miami School of Medicine, Miami, FL 33136, United States.

Jonathan Macni, Martinique Cancer Registry, University Hospital of Martinique, Fort de France 97261, Martinique.

Bernard Bhakkan, Guadeloupe Cancer Registry, University Hospital of Guadeloupe, Les Abymes 97142, Guadeloupe.

Jessica Peruvien, Guadeloupe Cancer Registry, University Hospital of Guadeloupe, Les Abymes 97142, Guadeloupe.

Matthew P Schlumbrecht, Sylvester Comprehensive Cancer Center, University of Miami School of Medicine, Miami, FL 33136, United States; Department of Obstetrics and Gynecology, University of Miami School of Medicine, Miami, FL 33136, United States.

Paulo S Pinheiro, Department of Public Health Sciences, University of Miami School of Medicine, Miami, FL 33136, United States; Sylvester Comprehensive Cancer Center, University of Miami School of Medicine, Miami, FL 33136, United States.

Funding

This work was supported by supplemental funding provided by the Sylvester Comprehensive Cancer Center at the University of Miami Miller School of Medicine and by the National Cancer Institute, National Institutes of Health (grant P30CA240139 to P.S.P.). Funding was also received through the Florida Education Fund McKnight Doctoral Fellowship to H.N.M. H.N.M. was also funded by The Ruth L. Kirschstein NRSA Institution Research Training Grant (T32; 5T32CA251064-03) in Cancer Training in Disparities and Equity. The project described was also supported by grant R25CA112383 from the National Cancer Institute.

Conflict of interest

The authors declare no conflicts of interest.

Disclaimer

The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health.

Data availability

The authors confirm that, for approved reasons, some access restrictions apply to the data underlying the findings. These data are confidential public health records with personal identifiers that can only be released for specific use upon approvals from the Florida Department of Health Cancer Registry Program, Florida Department of Health Bureau of Vital Statistics, the Florida Department of Health Institutional Review Board, and authorized officials of the Martinique and Guadeloupe Cancer Registry. These data are never available for public repository, given the confidential information they contain. In the case of the Florida Cancer Data System (FCDS), the data sets are available by request with required approvals from the Florida Department of Health Cancer Registry Program and Florida Department of Health Institutional Review Board. Applications for data request are available from the FCDS webpage (http://fcds.med.miami.edu/inc/datarequest.shtml).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The authors confirm that, for approved reasons, some access restrictions apply to the data underlying the findings. These data are confidential public health records with personal identifiers that can only be released for specific use upon approvals from the Florida Department of Health Cancer Registry Program, Florida Department of Health Bureau of Vital Statistics, the Florida Department of Health Institutional Review Board, and authorized officials of the Martinique and Guadeloupe Cancer Registry. These data are never available for public repository, given the confidential information they contain. In the case of the Florida Cancer Data System (FCDS), the data sets are available by request with required approvals from the Florida Department of Health Cancer Registry Program and Florida Department of Health Institutional Review Board. Applications for data request are available from the FCDS webpage (http://fcds.med.miami.edu/inc/datarequest.shtml).

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