
==== Front
JCO Precis Oncol
JCO Precis Oncol
po
PO
JCO Precision Oncology
2473-4284
Wolters Kluwer Health

38935898
PO.23.00699
10.1200/PO.23.00699
00152
ORIGINAL REPORTS
Cancer Genetics
Hereditary Cancer Screening and Outcomes at an Urban Safety-Net Hospital
https://orcid.org/0000-0001-8392-1523
Brehany Sydney MD 1
https://orcid.org/0000-0001-7380-1341
Colton Meryl MD 1
Duarte Cassandra MD 1
https://orcid.org/0009-0006-0769-7252
Baliton Michael BS 2
https://orcid.org/0000-0001-6840-9951
McCranie Alec S. BA 2
https://orcid.org/0000-0002-8107-3521
Okuyama Sonia MD 3
1 University of Colorado Cancer Center, Aurora, CO
2 University of Colorado School of Medicine, Aurora, CO
3 Denver Health Hospital Authority, Denver, CO
Sonia Okuyama, MD; e-mail: Sonia.okuyamasasaki@dhha.org.
2024
27 6 2024
27 6 2024
8 e230069915 12 2023
7 3 2024
26 4 2024
© 2024 by American Society of Clinical Oncology
2024
American Society of Clinical Oncology
https://creativecommons.org/licenses/by-nc-nd/4.0/ Creative Commons Attribution Non-Commercial No Derivatives 4.0 License: https://creativecommons.org/licenses/by-nc-nd/4.0/

PURPOSE

Patients with hereditary cancer syndromes (HCS) have a high lifetime risk of developing cancer. Historically underserved populations have lower rates of genetic evaluation. We sought to characterize demographic factors that are associated with undergoing HCS evaluation in an urban safety-net patient population.

METHODS

All patients who met inclusion criteria for this study from 2016 to 2021 at an urban safety-net hospital were included in this analysis. Inclusion criteria were pathologically confirmed breast, ovarian/fallopian tube, colon, pancreatic, and prostate cancers. Patients also qualified for hereditary breast and ovarian cancers or Lynch syndrome on the basis of National Comprehensive Cancer Network guidelines. Institutional review board approval was obtained. Demographic and oncologic data were collected through retrospective chart review. Univariable and multivariable logistic regression models were constructed.

RESULTS

Of the 637 patients included, 40% underwent genetic testing. Variables associated with receiving genetic testing on univariable analysis included patients living at the time of data collection, female sex, Latinx ethnicity, Spanish language, family history of cancer, and referral for genetic testing. Patients identifying as Black, having Medicare, having pancreatic or prostate cancer, having stage IV disease, having Eastern Cooperative Oncology Group (ECOG) prognostic score ≥1, having medium or high Charlson comorbidity index, with current or previous cigarette use, and with previous alcohol use were negatively associated with testing. On multivariable modeling, family history of cancer was positively associated with testing. Patients identifying as Black, having colon or prostate cancer, and having ECOG score of 2 had significantly lower association with genetic testing.

CONCLUSION

Uptake of HCS was lower in patients identifying as Black, those with colon or prostate cancer, and those with an ECOG score of 2. Efforts to increase HCS testing in these patients will be important to advance equitable cancer care.

Factors associated with receipt of hereditary cancer screening in a diverse patient population

OPEN-ACCESSTRUE
==== Body
pmcINTRODUCTION

Hereditary cancer syndromes (HCS) are uncommon conditions; however, individuals with an identified gene mutation may have up to an 80% lifetime risk of developing cancer. The two most common HCS, hereditary breast and ovarian cancer (HBOC) syndrome and Lynch syndrome, affect approximately 1:400 and 1:279 individuals, respectively, with some populations harboring mutations at much higher rates.1,2 Despite this, more than half of at-risk individuals have not undergone genetic testing.3

CONTEXT

Key Objective

To describe the demographic factors associated with receipt of hereditary cancer screening in an urban safety-net cancer patient population.

Knowledge Generated

In a diverse group of patients, our data showed that having a family history of cancer was positively associated with receipt of genetic testing. Patients identifying as Black, having colon or prostate cancer, or having an Eastern Cooperative Oncology Group score of 2 were significantly less likely to receive hereditary cancer syndrome evaluation.

Relevance

Our findings identify subgroups of patients that may benefit from enhanced efforts to engage in hereditary cancer screening to promote equitable cancer care.

There are patient, health care provider, and system barriers to undergoing genetic evaluation. Patient factors include poor understanding of the importance of their family history and not being aware of genetic services available.4 For health care providers, poor family history taking, lack of knowledge of genetic risk factors and genetic services, and inadequate referral coordination have been identified as barriers.4 Additionally, variation in testing criteria guidelines, especially as these change over time, and guidelines failing to capture all affected patients exacerbate difficulties for health care providers to identify patients to refer for adequate care.5-11 Unfortunately, historically underserved populations tend to fare worse. Several studies have shown that racial and ethnic minorities are less likely to receive referrals, undergo genetic counseling, and ultimately receive genetic testing.12-14 Although a physician recommendation to undergo counseling and testing has been identified as a strong predictor of testing completion,12,15,16 McCarthy et al15 found that physicians were less likely to recommend genetic testing to Black patients.

We sought to evaluate the patient demographic and oncologic characteristics that were associated with receipt of genetic testing in our health system with high ethnic diversity. Located in Denver, CO, our institution is an integrated safety-net health system that cares for a diverse patient population, with clinics located in neighborhoods with a high population of low-income individuals and families. Half of the patients served (51%) identify as Hispanic, and one-fifth have a documented need for Spanish interpretation. As the system's mission is to provide care for everyone, regardless of their ability to pay, 81% are either publicly insured or uninsured. Genetic counseling and testing services are available via referral to an outside institution, which adds an extra layer of complexity in accessing genetic services for the patients. We hypothesize that non-White patients and those without insurance will be less likely to receive recommended HCS testing.

METHODS

Study Design

All patients with pathologically confirmed breast, ovarian, fallopian tube, colon, pancreatic, or prostate cancer diagnoses and qualifying for hereditary cancer genetic testing on the basis of National Comprehensive Cancer Network (NCCN) guidelines seen at our urban safety-net hospital from 2016 to 2021 were included in this analysis. NCCN version 1.2022 was used for patients with breast, ovarian, and fallopian tube cancers; version 1.2021 for patients with colon cancer; version 3.2022 for patients with prostate cancer; and version 1.2022 for patients with pancreatic cancer. Institutional review board approval was obtained before any study-related activities. Demographic and oncologic data and hereditary genetic testing outcomes were collected through retrospective chart review using a standardized data collection tool.

Variable Selection

Demographic and clinical variables with known associations with cancer screening, genetic testing, or cancer survival were identified for collection. Demographic variables included age (continuous), sex, race, ethnicity, language, and insurance type. Clinical variables included family history of malignancy, stage at diagnosis, Eastern Cooperative Oncology Group (ECOG) at diagnosis, and Charlson comorbidity index (CCI) at diagnosis. Additionally, as they are known risk factors for development of our selected malignancies,17-22 we collected information on tobacco and alcohol use.

Statistical Analysis

Univariable associations were tested using logistic regression. All variables with an association with P < .1 were included for consideration in the multivariable model. For the multivariable model, we aimed to avoid collinearity by only including variables that increased the Akaike information criterion of the model from two categories with predetermined high concern for correlation. Of race, ethnicity, and language, this only included race and language. Of stage, ECOG, and CCI at diagnosis, this only included ECOG. Variables with no statistical significance (P > .05) in the multivariable model that were not considered confounders of other variables were excluded, including female sex, cigarette use, and alcohol use. The final model included age (continuous), race, language, insurance, type of malignancy, family history of malignancy, and ECOG at diagnosis. All calculations were performed using SAS Studio (Cary, NC).

RESULTS

A total of 637 patients were included in this analysis. Demographic and oncologic characteristics are detailed in Table 1. The majority of patients were biologically female (69%), identified as White (64%), and spoke English (63%). The most common malignancy was breast cancer (58%), and approximately 60% of patients had a documented family history of cancer in the chart. Forty-eight percent of the patients received a referral for genetic testing, and 40% of the total population completed testing. Table 2 shows the patients who received versus who did not receive genetic testing by cancer type.

TABLE 1. Number and Percent (%) or Mean and SD of Patients by Demographic and Cancer-Related Variables

Variable	Total (N = 637)	Received Genetic Testing (n = 254)	Didn't Receive Genetic Testing (n = 383)	
Living at the time of collection, No. (%)	506 (81.0)	210 (85.4)	296 (78.1)	
Age at diagnosis, mean (SD)	55.7 (12.7)	48.4 (11.0)	60.5 (11.2)	
Female, No. (%)	438 (68.9)	214 (84.6)	224 (58.5)	
Race, No. (%)				
 White	405 (63.6)	174 (68.5)	231 (60.3)	
 Black	121 (19)	27 (10.6)	94 (24.5)	
 Asian	17 (2.7)	7 (2.8)	10 (2.6)	
 Other	94 (14.8)	46 (18.1)	48 (12.5)	
Latinx ethnicity, No. (%)	309 (49.1)	145 (57.4)	164 (43.4)	
Language, No. (%)				
 English	404 (63.4)	146 (57.5)	258 (67.4)	
 Spanish	200 (31.4)	98 (38.6)	102 (26.6)	
 Other	33 (5.2)	10 (3.9)	23 (6.0)	
Insurance, No. (%)				
 Medicaid	250 (39.3)	110 (43.3)	140 (36.6)	
 Medicare	132 (20.7)	24 (9.5)	108 (28.2)	
 Private	112 (15.6)	51 (20.1)	61 (15.9)	
 Hospital subsidized	143 (22.5)	69 (27.2)	74 (19.3)	
Type of malignancy, No. (%)				
 Ovariana	31 (4.9)	18 (7.1)	13 (3.4)	
 Breast	369 (57.9)	186 (73.2)	183 (47.8)	
 Prostate	125 (19.6)	15 (5.9)	110 (28.7)	
 Colon	68 (10.7)	27 (10.6)	41 (10.7)	
 Pancreatic	44 (6.9)	8 (3.2)	36 (9.4)	
Family history of malignancy, No. (%)	391 (62.5)	179 (72.2)	212 (56.1)	
Stage at diagnosis, No. (%)				
 I	146 (22.9)	67 (26.4)	79 (20.6)	
 II	136 (21.4)	72 (28.4)	64 (16.7)	
 III	159 (25.0)	66 (26.0)	93 (24.3)	
 IV	145 (22.8)	33 (13.0)	112 (29.2)	
 Unknown	51 (8.0)	16 (6.3)	35 (9.1)	
ECOG at diagnosis, No. (%)				
 0	340 (53.4)	168 (66.1)	172 (44.9)	
 1	199 (31.2)	64 (25.2)	135 (35.3)	
 2	33 (5.2)	4 (1.6)	29 (7.6)	
 ≥3	17 (2.7)	3 (1.2)	14 (3.7)	
 Unknown	48 (7.5)	15 (5.9)	33 (8.6)	
Charlson comorbidity index, No. (%)				
 Low (<3)	542 (85.1)	235 (92.5)	307 (80.2)	
 Medium (3-4)	80 (12.6)	17 (6.7)	63 (16.5)	
 High (>4)	15 (2.4)	2 (0.8)	13 (3.4)	
Cigarette use, No. (%)				
 Never	337 (53.1)	160 (63.2)	177 (46.3)	
 Prior	195 (30.7)	66 (26.1)	129 (33.8)	
 Current	103 (16.2)	27 (10.7)	76 (19.9)	
Alcohol use, No. (%)				
 Never	372 (58.3)	159 (62.6)	212 (55.4)	
 Prior	115 (18.0)	37 (14.6)	78 (20.4)	
 Current	151 (23.7)	58 (22.8)	93 (24.3)	
Referred for genetic testing, No. (%)	305 (47.9)	223 (87.8)	82 (21.4)	
Received genetic testing, No. (%)	254 (40.0)			
Abbreviations: ECOG, Eastern Cooperative Oncology Group; SD, standard deviation.

a Four patients with fallopian tube cancer were classified as ovarian for purposes of this analysis.

TABLE 2. Patients Receiving Versus Not Receiving Genetic Testing by Cancer Type

Type of Malignancy	Received Genetic Testing	Did Not Receive Genetic Testing	Percent Receiving Testing, %	
Ovarian	18	13	58.1	
Breast	186	183	50.4	
Prostate	15	110	12.0	
Colon	27	41	39.7	
Pancreatic	8	36	18.2	

Univariable Models

In the univariable model (Fig 1), receipt of genetic testing was positively associated with the following variables: living at the time of data collection (odds ratio [95% CI], 1.636 [1.065 to 2.512]), female sex (3.875 [2.618 to 5.794]), Latinx ethnicity (1.768 [1.281 to 2.440]), Spanish language (1.698 [1.204 to 2.294]), family history of cancer (2.031 [1.440 to 2.865]), and receiving a referral for genetic testing (20.405 [16.870 to 41.331]). Lower rates of genetic testing were associated with patients identifying as Black (0.381 [0.238 to 0.611]); those with Medicare (0.283 [0.170 to 0.470]); those with prostate or pancreatic cancer (0.098 [0.040 to 0.241]) and (0.160 [0.056 to 0.457], respectively); those with stage IV disease (0.347 [0.209 to 0.577]); those with an ECOG status of 1 (0.485 [0.337 to 0.700]), 2 (0.141 [0.049 to 0.410]), or ≥3 (0.219 [0.062 to 0.777]); those with medium (0.201 [0.045 to 0.899]) or high (0.353 [0.201 to 0.618]) CCI; those with previous (0.566 [0.393 to 0.816]) or current (0.393 [0.241 to 0.640]) cigarette use; and those with previous alcohol use (0.633 [0.407 to 0.984]). Variables without association with testing uptake include patients identifying as Asian or other races, languages aside from Spanish, having private or hospital subsidized insurance, diagnosis of colon cancer, and having stage II or III disease.

FIG 1. ORs and 95% CI from univariable models. OR >1 indicates positive association with genetic testing. Black/Asian/Other race compared with White; Spanish/Other language compared with English; insurance compared with Medicaid; cancer type compared with ovarian; stage compared with stage I; ECOG compared with ECOG 0. ECOG, Eastern Cooperative Oncology Group; ORs, odds ratios; ref, reference.

Multivariable Model

In the multivariable model (Fig 2), variables with significantly poorer association with testing uptake include patients identifying as Black (0.496 [0.274 to 0.897]), those with prostate or colon cancer (0.236 [0.081 to 0.693]) and (0.239 [0.082 to 0.699], respectively), and those with an ECOG performance status of 2 (0.222 [0.056 to 0.883]). A documented family history of cancer was the only variable more positively associated with genetic testing uptake (2.177 [1.406 to 3.371]). Notably, type of insurance and language spoken were no longer statistically significant variables.

FIG 2. ORs and 95% CI from the final multivariable model. OR >1 indicates positive association with genetic testing. Black/Asian/Other race compared with white; Spanish/Other language compared with English; insurance compared with Medicaid; cancer type compared with ovarian; ECOG compared with ECOG 0. ECOG, Eastern Cooperative Oncology Group; ORs, odds ratios; ref, reference. aECOG 4 compared with ECOG 0 not estimable in the multivariable model.

DISCUSSION

The results of our analysis highlight a few themes in testing for HCS. First, as has been described in the literature previously, Black patients are less likely to have genetic testing done. As mentioned previously, racial and ethnic minorities have low rates of referral to genetic services. Considering Black patients specifically, Cragun et al13 showed that compared with non-Hispanic White patients, Black patients in their study were 16.6 times less likely to have genetic testing discussed by a health care provider. Another study found that non-Hispanic Black patients were less likely than non-Hispanic White patients to be referred for genetic testing on the basis of family history alone (30.7% v 40.5%), and unfortunately, 39% of Black patients in their study would have met criteria for testing before a personal diagnosis of cancer.14 Even if patients are referred for testing, medical mistrust/distrust may play into whether a patient ultimately decides to go through with testing. When specifically looking at a population undergoing genomic testing, Angelo et al23 showed the prevalence of medical distrust in the Black/African American population was 43%, significantly higher than that of the overall study population (32%). As patients from our institution were included in this study, the likelihood distrust plays a role for our patients is considerable. Another study found that mistrust around tumor genomic profiling in the African American population centered on concerns of cost, insurance discrimination, privacy breaks, clinical utility and test accuracy, and provider communication around uncertain results.24 Currently, our institution's process for HCS involves patients being referred to a tertiary care center across town, certainly leaving room to introduce one or more of those mistrust factors.

A second theme emerging from our data is that patients with colon or prostate cancer were less likely to undergo genetic testing. Hampel described testing for hereditary colorectal cancer as more complex than HBOC testing. Reasons for this include needing to consider more than one syndrome, phenotypic overlap of possible syndromes, syndromes having more than one causative gene, and involving both tumor and germline sources for adequate testing.25 Differences in testing guidelines also seem to play a role. A comparison of the NCCN guidelines with the American College of Medical Genetics and Genomics (ACMG) guidelines found the greatest difference in proband identification in the colorectal and endometrial guidelines.5 Notably, at the time of that publication, they did not identify guidelines for prostate cancer in the NCCN analogous to those in ACMG,5 highlighting the issue of changing guidelines over time, affecting uptake of testing.

Third, although only significant in the univariable analysis (but trending toward significance on multivariable testing), speaking Spanish was associated with higher receipt of testing, a finding that has not been commonly reported in the literature. In a population of young women with a breast cancer diagnosis, Cragun et al13 found that Spanish-speaking Hispanic patients were almost two times less likely to have genetic testing discussed by a provider, and only 49.6% of Spanish-speaking Hispanic patients received BRCA testing, compared with 64.5% of non-Hispanic White patients. However, the study by Angelo et al,23 which may have included some of this current study's patients, showed the rate of medical distrust in Hispanic patients was less than that in the overall population (26% v 32%). Our institution has a strong reputation for engaging with the Hispanic- and Spanish-speaking community well, which likely contributes to the positive association with testing noted in our study.

Fourth, our analysis showed that patients with an ECOG score of 2 had a negative association with genetic testing. Although we did not have enough patients to draw a true conclusion for ECOG 3+ patients, and the relatively low number of ECOG 2 patients may influence this result, it does raise the question of whether patients may be too ill to travel to the tertiary care center for HCS and/or attention is distracted away from HCS during oncology clinic visits due to acute issue management. As models of genetic testing delivery are evolving to reach more and more patients, we hope to adjust our care delivery so that obtaining HCS is not a burden to patients, but rather centralized more to their primary oncologist's clinic.

Finally, although we had hypothesized that patients without insurance would be less likely to undergo genetic testing and our current care model relies heavily on referrals to a tertiary care center, we did not see a difference on the basis of insurance status in our multivariable model. We hypothesize this is due to our institution's strong history of caring for patients regardless of their ability to pay and working to find creative solutions to maintain a high quality of care for all.

Our study is not without limitations. As noted above, changing guidelines over time has been shown to affect testing. Our inclusion criteria were based on NCCN guidelines at the time of data acquisition; however, the guidelines have since been updated, and as a result, we are likely missing patients who could have been included in this analysis. Additionally, we only collected demographic and oncologic data to associate with HCS uptake; why any patient may have chosen not to have testing done is only speculation at this time. Focus groups of patients may be one way to start elucidating the why behind the results of our study. Finally, we recognize there may be unique factors in play for our institution that may not fully translate to other health systems.

In conclusion, we showed that uptake of HCS was lower in patients identifying as Black, those with colon or prostate cancer, and those with an ECOG score of 2. Tailoring efforts to increase HCS in these patients while maintaining the success seen with our Spanish-speaking patients will be important to advance equitable cancer care for our diverse population.

PRIOR PRESENTATION

AUTHOR CONTRIBUTIONS

Conception and design: Sydney Brehany, Meryl Colton, Sonia Okuyama

Administrative support: Meryl Colton

Collection and assembly of data: All authors

Data analysis and interpretation: Sydney Brehany, Meryl Colton, Cassandra Duarte, Sonia Okuyama

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/po/author-center.

Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).

Presented in part at the 2022 ASCO Annual Meeting, Chicago, IL, June 3, 2022.

Sydney Brehany

Employment: Medtronic, DaVita

Cassandra Duarte

Research Funding: Flatiron Health (Inst)

Michael Baliton

Employment: University of California at San Francisco

No other potential conflicts of interest were reported.
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