We identified 151 patients who received echocardiograms and also underwent trastuzumab and/or doxorubicin therapy. The cohort was predominantly black (n = 70, 46.4%), followed by white (n = 41, 27.2%), Hispanic (n = 33, 21.9%), and other (n = 7, 4.6%). The other category included 5 Asians and 2 listed as “others” in the electronic medical record.
Socio-demographics
Baseline socio-demographics were similar between racial groups in terms of age, gender distribution, and medical insurance (Table 1). About half of black patients had private insurance, which is similar to that of whites, Hispanics, and other races (54.3%, 56.1%, 48.5%, 42.9%, respectively, p = 0.76). Black, Hispanic, and other race patients were more likely to live in ZIP codes with lower median annual household income compared to white patients (p < 0.00001) (Fig. 1). Two (4.9%) white patients live in the lowest quartile of ZIP codes by income, compared to 27 (38.6%) black patients, 10 (30.3%) Hispanic patients, and 3 (42.9%) other race patients. In contrast, 23 (56.1%) white patients live in the highest quartile of ZIP codes by income, compared to 10 (14.3%) black patients, 3 (9.1%) Hispanic patients, and 2 (28.6%) other race patients.
Table 1
Baseline demographics and clinical characteristics of patients by race
| Black (N = 70) | White (N = 41) | Hispanic (N = 33) | Other (N = 7) | P-value |
Age at diagnosis (median, [IQR]) | 58 (49, 66) | 58 (52, 65) | 53 (44, 59) | 61 (43, 66) | p = 0.13 |
Gender | | | | | p = 0.27 |
Male | 6 (8.6%) | 9 (22.0%) | 5 (15.2%) | 1 (14.3%) | |
Female | 64 (91.4%) | 32 (78.0%) | 27 (81.8%) | 6 (85.7%) | |
Insurance | | | | | p = 0.76 |
Private insurance | 38 (54.3%) | 23 (56.1%) | 16 (48.5%) | 3 (42.9%) | |
Medicare | 26 (37.1%) | 12 (29.2%) | 10 (30.3%) | 3 (42.9%) | |
Medicaid | 2 (2.9%) | 1 (2.4%) | 2 (6.1%) | 0 (0.0%) | |
No insurance | 4 (5.7%) | 5 (12.2%) | 5 (15.2%) | 1 (14.3%) | |
Income by ZIP code* | | | | | p < 0.00001 |
Quartile 1 | 27 (38.6%) | 2 (4.9%) | 10 (30.3%) | 3 (42.9%) | |
Quartile 2 | 13 (18.6%) | 5 (12.2%) | 14 (42.4%) | 2 (28.6%) | |
Quartile 3 | 20 (28.6%) | 11 (26.8%) | 6 (18.2%) | 0 (0.0%) | |
Quartile 4 | 10 (14.3%) | 23 (56.1%) | 3 (9.1) | 2 (28.6%) | |
Risk factors | | | | | |
HTN | 48 | 22 | 15 | 3 | p = 0.19 |
HLD | 19 | 16 | 11 | 2 | p = 0.62 |
DM | 20 | 10 | 9 | 1 | p = 0.91 |
Smoking | 33 | 18 | 10 | 1 | p = 0.18 |
FH | 20 | 12 | 7 | 2 | p = 0.86 |
Age > 65 | 17 | 11 | 5 | 1 | p = 0.64 |
Number of risk factors (mean) | 2.2 | 2.2 | 1.7 | 1.3 | p = 0.12 |
Cancer type | | | | | p = 0.048 |
Breast cancer | 58 (82.9%) | 24 (58.5%) | 24 (72.7%) | 5 (71.4%) | |
Other cancer** | 12 (17.1%) | 17 (41.5%) | 9 (27.3%) | 2 (28.6%) | |
Cancer stage | | | | | p = 0.93 |
Stage 1 | 6 (8.6%) | 3 (7.3%) | 2 (6.1%) | 1 (14.3%) | |
Stage 2 | 32 (45.7%) | 18 (43.9%) | 18 (54.5%) | 3 (42.9%) | |
Stage 3 | 14 (20.0%) | 9 (22.0%) | 5 (15.2%) | 1 (14.3%) | |
Stage 4 | 18 (2.7%) | 12 (29.3%) | 7 (21.2%) | 2 (28.6%) | |
Chemotherapy | | | | | p = 0.48 |
Doxorubicin | 25 (35.7%) | 22 (53.7%) | 15 (45.5%) | 3 (42.9%) | |
Herceptin | 40 (57.1%) | 15 (36.6%) | 14 (42.4%) | 4 (57.1%) | |
Doxorubicin and herceptin | 5 (7.1%) | 4 (9.8%) | 4 (12.1%) | 0 (0.0%) | |
Ejection fraction | | | | | p = 0.78 |
Decrease*** | 19 (27.1%) | 11 (26.8%) | 6 (18.2%) | 2 (28.6%) | |
No decrease | 51 (72.9%) | 30 (73.2%) | 27 (81.2%) | 5 (71.4%) | |
Current status | | | | | p = 0.60 |
In remission | 21 (30.0%) | 14 (34.1%) | 11 (33.3%) | 3 (42.9%) | |
Not in remission | 40 (57.1%) | 19 (46.3%) | 20 (60.6%) | 3 (42.9%) | |
Deceased | 9 (12.9%) | 7 (17.1%) | 1 (3.03%) | 1 (14.3%) | |
* ZIP codes were used to group patients into quartiles based on median annual household income, with quartile 1 earnings $0 - $18,900, quartile 2 earnings $19,000–32,800, quartile 3 earnings 32,900–56,000, quartile 4 earnings $57,000–130,300 ** Other cancer types included lymphoma (Hodgkin’s, T-cell, large cell), multiple myeloma, esophageal cancer, gastric cancer, abdominal desmoid cancer, carcinoid tumor, bladder cancer, ovarian cancer, endometrial cancer, leiomyosarcoma, metastatic cancer with an unknown primary *** Decrease in EF defined by symptomatic reduction in EF by at least 5% to less than 55% or an asymptomatic reduction in EF by at least 10% to less than 55% according to Cardiac Review and Evaluation Committee of Trastuzumab-associated Cardiotoxicity |
White patients were more likely to live in ZIP codes with higher median annual household income compared to black, Hispanic, or other races (p < 0.00001). |
2a. Comparing between the racial groups, there is no statistical difference in the number of patients who decrease in EF: 19 [27.1%] blacks, 11 [26.8%] whites, 6 [18.2%] Hispanics, 2 [28.6%] other races, p = 0.78. |
Clinical characteristics
There was no statistical difference between racial groups in cardiotoxicity risk factors, cancer stage at diagnosis, and use of trastuzumab versus doxorubicin (Table 1). Breast cancer was the most common cancer type, with “other types” being very broad, including lymphoma (Hodgkin’s, T-cell, large cell), multiple myeloma, esophageal cancer, gastric cancer, abdominal desmoid cancer, carcinoid tumor, bladder cancer, ovarian cancer, endometrial cancer, leiomyosarcoma, and metastatic cancer with unknown primary. White patients were less likely to have breast cancer in this cohort (24 [58.5%], compared to 58 [82.9%] black patients, 24 [72.7%] Hispanic patients, and 5 [71.4%] other race patients, p = 0.048). There was no statistical difference when comparing racial groups in the number of patients who had drops in EF (19 [27.1%] blacks, 11 [26.8%] whites, 6 [18.2%] Hispanics, 2 [28.6%] other races, p = 0.78) (Fig. 2a). There was no difference in the number of patients whose EF dropped below 40% (p = 0.36). When looking only at female patients, there was still no difference in drop in EF (p = 0.54) (Fig. 2b). The number of patients in remission was also similar between racial groups (p = 0.60).
Referral pattern
A total of 70 (46.4%) patients were referred by oncology clinics to cardio-oncology clinic or general cardiology clinic (50 [71.4%] to cardio-oncology and 20 [28.6%] to general cardiology clinic). When stratified by race, no group was less likely to be referred (33 [47.1%] blacks, 21 [51.2%] whites, 14 [42.4%] Hispanics, 2 [28.6%] others, p = 0.68) (Table 2). The number of oncology appointments attended was similar between groups (p = 0.29). The number of echocardiograms received since starting cardiotoxic chemotherapy was similar between groups (4 for blacks, 4 for whites, 5 for Hispanics, 4 for others, p = 0.62). Among those who were referred to cardio-oncology or cardiology clinic, the median number of appointments attended was 4 (IQR 2–6) and median number of appointments missed or cancelled was 2 (IQR 0–4), with no difference between racial groups (p = 0.88, p = 0.20, respectively). Finally, a total of 6 patients who had a decrease in EF were not referred to cardio-oncology or cardiology clinics at any time. These patients all had either metastatic cancer or were determined to be too frail to tolerate a different chemotherapy regimen and were referred for hospice.
Table 2
Clinical characteristics of patients regarding access to care
All Patients | Black (N = 70) | White (N = 41) | Hispanic (N = 33) | Other (N = 7) | P-value |
Referred to cardiology clinic | 33 (47.1%) | 21 (51.2%) | 14 (42.4%) | 2 (28.6%) | p = 0.68 |
Number of oncology appointments attended (median [IQR]) | 24 (12, 32) | 17 (13, 24) | 21 (15, 28) | 16 (13, 17) | p = 0.29 |
Number of echocardiograms (median [IQR]) | 4 (3, 7) | 4 (2, 6) | 5 (3, 7) | 4 (3, 5) | p = 0.62 |
Referred Patients | Black (N = 33) | White (N = 21) | Hispanic (N = 14) | Other (N = 2) | P-value |
Number of cardio-oncology or cardiology appointments attended (median [IQR]) | 4 (2, 6) | 5 (2, 9) | 4 (4, 5) | 4 (3, 5) | p = 0.88 |
Number of cardio-oncology or cardiology appointments missed or cancelled (median [IQR]) | 1 (0, 3) | 3 (1, 5) | 2 (1, 4) | 1 (0, 2) | p = 0.20 |
Number of echocardiograms in referred patients (median [IQR]) | 6 (4, 8) | 5 (2, 7) | 6 (5, 7) | 5 (4, 6) | p = 0.76 |
IQR = interquartile range |
In unadjusted univariate analysis, patients were more likely to be referred if they lived in ZIP codes with median household income quartiles 2–3, were hypertensive, had breast cancer, or received trastuzumab for chemotherapy (Table 3). A logistic regression model used race, age, gender, insurance, income quartile by home ZIP code, cardiomyopathy risk factors (HTN, HLD, DM, smoking, FH, age > 65), cancer type, cancer stage, and chemotherapy to look at association to referral rate. This model found that increased referral rate was best explained by income quartile by ZIP code (p = 0.004), hypertension as cardiomyopathy risk factors (p = 0.0001), and cancer type (p = 0.04). Compared to patients in income quartile 1 as reference, quartile 3 patients were 6.77 times more likely to be referred (CI 1.83–25.10, p = 0.004). Quartile 2 and 4 patients were not statistically more likely to be referred, however the confidence interval pattern does trend towards increased referral as well (OR 3.06, CI 0.90–10.46, p = 0.07; OR 3.89, CI 0.97–15.59, p = 0.055; respectively) (Fig. 3). Patients who were hypertensive were more likely to be referred (OR 6.85, CI 2.68–17.52, p = 0.0001). Patients with non-breast cancers were less likely to be referred (OR 0.20, CI 0.04–0.97, p = 0.04). Other cardiomyopathy risk factors such as hyperlipidemia, diabetes, smoking, and family history were not associated with increased referral rate. Race, age, gender, insurance, cancer stage, and type of chemotherapy were not associated with increased referral rate.
Table 3
Referral patterns of patients receiving cardiotoxic chemotherapy agents from oncology clinic to cardio-oncology or cardiology clinic
| Referred (N = 70) | Not Referred (N = 81) | P-value |
Race | | | p = 0.68 |
Black | 33 (47.1%) | 37 (45.7%) | |
White | 21 (30.0%) | 20 (24.7%) | |
Hispanic | 14 (20.0%) | 19 (23.5%) | |
Others | 2 (2.9%) | 5 (6.2%) | |
Age at diagnosis (median, [IQR]) | 61 (51, 68) | 59 (52, 66) | p = 0.55 |
Gender | | | p = 0.73 |
Male | 9 (12.9%) | 12 (14.8%) | |
Female | 61 (87.1%) | 69 (85.2%) | |
Insurance | | | p = 0.18 |
Private insurance | 39 (55.7%) | 41 (50.6%) | |
Medicare | 26 (37.1%) | 25 (30.1%) | |
Medicaid | 2 (2.9%) | 3 (3.7%) | |
No insurance | 3 (4.3%) | 12 (14.8%) | |
Income by ZIP code | | | p = 0.039 |
Quartile 1 | 11 (15.7%) | 28 (34.6%) | |
Quartile 2 | 17 (24.3%) | 18 (22.2%) | |
Quartile 3 | 23 (32.9%) | 15 (18.5%) | |
Quartile 4 | 19 (27.1%) | 20 (51.3%) | |
Risk factors | | | |
HTN | 52 (74.3%) | 36 (44.4%) | p = 0.00001 |
HLD | 25 (35.7%) | 23 (28.4%) | p = 0.34 |
DM | 22 (31.4%) | 18 (22.2%) | p = 0.20 |
Smoking | 27 (38.6%) | 34 (42.0%) | p = 0.67 |
FH | 20 (28.6%) | 20 (24.7%) | p = 0.59 |
Age > 65 | 20 (28.6%) | 15 (18.5%) | p = 0.14 |
Cancer type | | | p = 0.005 |
Breast cancer | 59 (84.3%) | 52 (64.3%) | |
Other cancer | 11 (15.7%) | 29 (35.8%) | |
Cancer stage | | | p = 0.07 |
Stage 1 | 8 (11.4%) | 4 (4.9%) | |
Stage 2 | 38 (54.3%) | 33 (40.7%) | |
Stage 3 | 11 (15.7%) | 18 (22.2%) | |
Stage 4 | 13 (18.6%) | 26 (32.1%) | |
Chemotherapy | | | p = 0.036 |
Doxorubicin | 22 (31.4%) | 42 (51.9%) | |
Herceptin | 40 (57.1%) | 34 (42.0%) | |
Doxorubicin and herceptin | 8 (11.4%) | 5 (6.2%) | |
Table 4
Multivariate analysis of variables associated with increased referral rate of patients receiving cardiotoxic chemotherapy from oncology clinic to cardio-oncology or cardiology clinic
| Odds Ratio | Confidence Interval | P-value |
Race | | | |
Black | | |
White | 1.47 | 0.50–4.32 | 0.48 |
Hispanic | 1.34 | 0.43–4.19 | 0.62 |
Other | 0.42 | 0.05–3.74 | 0.43 |
Age | 0.96 | 0.93–1.00 | 0.08 |
Gender | | | |
Male | Reference | | |
Female | 0.30 | 0.06–1.56 | 0.15 |
Insurance | | | |
Private | Reference | | |
Medicare | 0.52 | 0.16–1.74 | 0.29 |
Medicaid | 0.81 | 0.10–6.32 | 0.84 |
Self | 0.18 | 0.03–1.06 | 0.06 |
Income by ZIP code* | | | |
Quartile 1 | Reference | | |
Quartile 2 | 3.06 | 0.90–10.46 | 0.07 |
Quartile 3 | 6.77 | 1.83–25.10 | 0.004 |
Quartile 4 | 3.89 | 0.97–15.59 | 0.055 |
Risk factors | | | |
HTN | 6.85 | 2.68–17.52 | 0.0001 |
HLD | 1.07 | 0.41–2.81 | 0.90 |
DM | 1.78 | 0.67–4.75 | 0.25 |
Smoking | 1.18 | 0.47–2.99 | 0.73 |
FH | 0.79 | 0.29–2.13 | 0.64 |
Age > 65 | 4.01 | 0.10–16.17 | 0.051 |
Cancer type | | | |
Breast cancer | Reference | | |
Other cancer^ | 0.20 | 0.04–0.97 | 0.04 |
Cancer stage | | | |
Stage 1 | Reference | | |
Stage 2 | 0.53 | 0.12–2.47 | 0.42 |
Stage 3 | 0.27 | 0.05–1.52 | 0.14 |
Stage 4 | 0.50 | 0.09–2.84 | 0.43 |
Chemotherapy | | | |
Doxorubicin | 1.66 | 0.41–6.69 | 0.43 |
Herceptin | 1.66 | 0.35–7.82 | 0.52 |