Abstract
Importance:
Racial bias influences allocation of advanced heart failure therapies, heart transplants and ventricular assist devices (VAD). It is unknown whether gender and racial biases influence the allocation of advanced therapies among women.
Objective:
To determine whether the intersection of patient gender and race influences clinicians’ decision-making during the allocation of advanced heart failure therapies.
Design:
Participants were randomized to clinical vignettes which varied 1:1 by patient race (African-American: White) and 20:3 by gender (women:men), with purposeful target of women vignettes in order to compare with male studies. Participants were interviewed about their decision-making process using the think-aloud technique, and provided supplemental surveys. Interviews were analyzed using grounded theory methodology, and surveys were analyzed with t-tests.
Setting:
International transplant conference
Participants:
U.S. members of an international heart transplant organization
Exposure:
Randomization to clinical vignettes
Main Outcome:
Thematic differences in allocation of advanced therapies by patient race and gender
Results:
Among 46 participants (52% women, 43% racial minority), participants were randomized to the White woman vignette (n=20), African-American woman vignette(n=20), White man vignette(n=3), and African-American man vignette(n=3). Allocation differences centered upon five themes. First, clinicians’ critiqued the appearance of the women more harshly than men as overall impressions. Second, the African-American man was perceived as sicker than other race/gender groups. Third, there was more concern regarding appropriateness of prior care of the African-American woman compared to the White woman. Fourth, there were greater concerns about adequacy of social support of the women. Children were perceived as liabilities for women, particularly the African-American woman. Family dynamics and finances were greater concerns for the African-American woman. Spouses were deemed inadequate support for women. Last, participants recommended VAD over transplant for all race/gender groups. Surveys demonstrated similar final recommendations.
Conclusions and Relevance:
In a national study of healthcare professionals randomized to identical clinical vignettes varying by gender and race, gender and race bias influenced the allocation process particularly among African-American women who were judged more harshly by appearance and adequacy of social support, but not the final recommendations. Bias may contribute to delayed allocation and ultimately inequity in allocation of advanced therapies.
Keywords: Heart transplantation, Racial disparities, Women
INTRODUCTION
Heart failure therapies are inequitably allocated to minority racial groups in the U.S.1,2 Despite African-Americans representing the highest racial risk group for heart failure incidence and mortality,3 African-Americans are less likely to receive defibrillators4,5 and care by a cardiologist compared to Whites.6 Racial disparities are not fully explained by socioeconomic factors,4–6and may be related to bias. Recent works suggest that patient race influences the allocation process for advanced heart failure therapies, heart transplants and ventricular assist devices (VAD).7 Among male vignettes with identical clinical and social histories, White men were favored over African-American men for allocation to heart transplants.7 Variability in clinicians’ assessments of social support and adherence contributed to the racial bias.7
Advanced heart failure therapies are also disparately allocated by gender.2,8 Although women have higher prevalence of heart failure than men,3 women receive less than a quarter of heart transplants and VAD.2,8 This may be related to a higher prevalence of heart failure with preserved ejection fraction in women than in men,3 which is rarely an indication for transplant and not an indication for VAD. However, over 40% of heart failure hospitalizations in White women are attributed to heart failure with reduced ejection fraction,3,9 and African-American women have higher rates of heart failure with reduced ejection fraction than preserved ejection fraction.9 U.S. Women are less likely to receive advanced heart therapies.10,11 The reason for the gender disparity is advanced heart failure therapies is unknown.
Patient race and gender are known to influence clinical decision-making.12,13 With complex decision-making processes such as allocation of advanced heart failure therapies, it is unknown whether the intersection of gender and race influences healthcare professional decision-making. It is unclear how gender and race influence subjective assessments included in evaluation for advanced therapies. Using interviews and supplemental surveys, the decision-making process was examined in a controlled setting with identical clinical vignettes which varied only by gender and race. This study addressed the overriding hypotheses that African-American women would be evaluated more harshly and less likely to be offered heart transplantation than White women or men.
METHODS
Study Design, Sample, and Recruitment
In a simultaneous mixed-methods study performed April 2019, U.S. members of the International Society for Heart and Lung Transplantation (ISHLT) were interviewed at ISHLT scientific sessions and administered supplemental surveys. ISHLT is composed of clinicians, allied health professionals, scientists, and trainees. Eligible members included U.S. based healthcare professionals who engage in clinical decision-making for the allocation of advanced heart failure therapies. Participants were identified through the annual scientific sessions program and ISHLT directory. Participants were purposefully selected for diversity of participant demographics (gender, race, geography, years past training). Snowball sampling was used to meet enrollment goal of 44 participants since this was sufficient to reach 1:1 thematic saturation in a prior study,7 and snowball sampling is an established method of recruiting specific hard-to-reach subgroups.14 Study participants provided verbal informed consent and received monetary incentives worth $10 US dollars for participating. Trained research assistants performed, audio recorded, and collected field notes for all interviews. This study followed the Standards for Reporting Qualitative Research.15 The University of Arizona Institutional Review Board approved this study.
Vignette
Participants were blinded to study objectives until participation was complete. Participants were randomized 1:1 to African-American woman or White woman vignettes in order to compare women vignettes with a prior study including only African-American men and White men.7 On each of the three interview days, two participants were randomized to a male vignette as a data check to compare with prior study of only male vignettes who were slightly taller but had similar body mass index. Gender and race were indicated by photographs, text, and ethnic- or gender- sounding name.16 The four study photographs included an African-American woman, White woman, African-American man, and White man. Within each gender, the hairstyle and physical build were similar. Across all four photographs, clothing was similar, and photos were previously rated similarly for age, attraction, intelligence, health, facial expression, and trustworthiness in a normalization study (Supplemental Table 1 and prior works7). Clinical vignettes were otherwise identical with the exception of sex- based evaluations (normal mammogram for women and normal prostate specific antigen for men, and shorter height Supplemental Table 2). In brief, vignettes described patients with end-stage heart failure with complex history, including multiple relative contraindications for advanced therapies.
Interviews
Interviews were conducted using think-aloud method, which elicits verbalization of conscious and unconscious thoughts.17 Think-aloud is an established method of understanding the decision-making process.17 Participants were directed to articulate their thoughts as they read through each section of the vignette during a 30- minute interview. Prompts from the Shafer and Lohse cognitive interviewing guide were used to aide participants in verbalizing their thoughts, such as “Tell me what you are thinking. What thoughts are going through your mind right now?”18 Participants were asked how each section of the vignette influenced their recommendation for advanced heart failure therapies. Upon conclusion of discussing the vignette, participants were asked to share any thoughts that they had not previously shared, provide a final recommendation for the patient in the clinical vignette and reasons for the recommendation. Then participants were asked whether they trusted the patient in the clinical vignette and about how the vignette compared to patient presentations at their respective centers. The entire interview guide was duplicated from a previously published study since the other guide had been rigorously tested and provided opportunity for comparison of studies.7
Survey Instrument
Supplemental surveys were provided to participants after completing interviews. Using Likert Scale (1–10, strongly disagree to strongly agree), participants were asked to rate how each section of the vignette influenced the patient’s suitability for advanced heart failure therapies. Then participants were asked to rate the suitability for each advanced heart failure therapy (heart transplant, bridge to transplant VAD, destination VAD, no advanced therapy) and need for additional testing or consultation. Participants were also asked to provide write-in responses that supported their decisions. Participants’ demographics were also collected. The survey questions were duplicated from a previously published study.7
Statistical Analysis
Thematic analysis of think-aloud interviews was performed using grounded theory while blinded to patient gender and race. Results were then unblinded and categorized according to gender and race. The stepwise process of grounded theory19 included: (A) open coding: identifying tentative themes until reaching saturation (no new ideas)20, (B) identifying a central phenomenon: combining themes to form a central category, (C) axial coding: identifying relationships between themes, (D) selective coding: supporting themes with specific codes; resulting in a model that represents the decision-making process. Rigor was established through credibility and triangulation (validation of interview response with survey response), transferability (debrief with advanced HF cardiologist [NS White woman]), confirmability (including trained interviewers with bachelor’s degrees [EY Asian and White woman, RHY Asian and White man] and 2 independent faculty analysts with doctorate degrees [NP White woman, MH White woman] who performed the entire qualitative analyses with differences arbitrated by an independent qualitative expert [JC White woman] and the primary investigator an advanced HF cardiologist [KB African-American woman]).21 Neither the interviewers nor the analysts had relationships with study participants. An audit trail and codebook were maintained throughout the study.
Participant survey demographics were compared across African-Americans and Whites within each gender using Fisher’s exact test for categorical data. Mean results of the individual survey questions were compared within women vignettes with Wilcoxon test in order to compare to overall findings from qualitative analyses and adjusted for multiple comparisons with false discovery rate procedure.22 For hypothesis generation, a secondary analysis was performed to examine the means and standard error of this study and a prior study conducted by the PI (KB) including 44 participants who were randomized 1:1 to African-American man and White man vignettes interviews and surveys.7 Groups were not statistically compared since some individuals participated in both studies [survey (n=12), study interview and survey (n=6)].
RESULTS
Among U.S. based members of an international heart transplant organization, 46 participants (52% women, 43% racial minority) were randomized to African-American woman (N=20) and White woman clinical vignettes (N=20), and African-American man (N=3) and White man (N=3) clinical vignettes (Table 1). The majority of participants were in the cardiologist (n=31) and cardiothoracic surgeon (n=7) category. Participants represented 10 of the 11 U.S. regions for heart transplant. There were no statistically significant differences in participant demographics within the women and men patient vignettes.
Table 1.
Women Vignettes | Men Vignettes | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
African-American N= 20 (%) | White N= 20 (%) | P value | African-American N= 3 (%) | White N= 3 (%) | P value | |||||
Age Years | 0.11 | >0.99 | ||||||||
Less than 40 years | 5 | (25) | 11 | (55) | 1 | (33) | 1 | (33) | ||
40+ years | 15 | (75) | 9 | (45) | 2 | (67) | 2 | (67) | ||
Gender | 0.20 | >0.99 | ||||||||
Men | 7 | (35) | 11 | (55) | 2 | (67) | 1 | (33) | ||
Women | 13 | (65) | 8 | (40) | 1 | (33) | 2 | (67) | ||
Unknown | . | . | 1 | (5) | ||||||
Ethnicity | 0.52 | >0.99 | ||||||||
Minority | 10 | (50) | 7 | (35) | 1 | (33) | 2 | (67) | ||
Non-Hispanic White | 10 | (50) | 13 | (65) | 2 | (67) | 1 | (33) | ||
Position | >0.99 | 0.40 | ||||||||
Cardiologist or CT surgeon | 17 | (85) | 17 | (85) | 3 | (100) | 1 | (33) | ||
Non-cardiologist | 3 | (15) | 3 | (15) | . | . | 2 | (67) | ||
Years Past Training | 0.51 | >0.99 | ||||||||
Less than 11 years | 11 | (55) | 14 | (70) | 2 | (67) | 2 | (67) | ||
11+ years | 9 | (45) | 6 | (30) | 1 | (33) | 1 | (33) | ||
UNOS Region | 0.92 | 0.40 | ||||||||
1 | 1 | (5) | . | . | . | . | . | . | ||
2 | 3 | (15) | 4 | (20) | . | . | . | . | ||
3 | 1 | (5) | 2 | (10) | . | . | 1 | (33) | ||
4 | 2 | (10) | 1 | (5) | . | . | . | . | ||
5 | 5 | (25) | 2 | (10) | 3 | (100) | 1 | (33) | ||
6 | . | . | . | . | . | . | . | . | ||
7 | 1 | (5) | 2 | (10) | . | . | . | . | ||
8 | 3 | (15) | 3 | (15) | . | . | 1 | (33) | ||
9 | . | . | . | . | . | . | . | . | ||
10 | 3 | (15) | 5 | (25) | . | . | . | . | ||
11 | 1 | (5) | 1 | (5) | . | . | . | . |
CT indicates cardiothoracic; UNOS, United Network for Organ Sharing. CT surgeons were represented by 7 individuals. Non-cardiologists are represented by 2 nurse practitioners, 3 nurse coordinators, 1 social worker, 1 pharmacist, and 1 director of solid organs.
Think-Aloud Interview Results
The allocation decision-making process was found to be defined by a central phenomenon: is the heart sick enough, body well enough, and is there enough social/emotional support to receive advanced therapies? Participants allocated therapies by sequential steps, major themes: (1) forming an overall impression: critiquing appearance of women more harshly, (2) identifying urgency: believing African-American man was sicker, (3) evaluating appropriateness of prior care: believing African-American woman’s care was less appropriate than the White woman, (4) anticipating challenges: believing similar forms of social support were adequate for men and inadequate for women, particularly African-American women, and (5) evaluating trust and making an ultimate recommendation: recommending VAD over transplant for all subgroups (Table 2). Subthemes varied by race and gender of the clinical vignette including positive, negative, and neutral observations (Supplemental Table 3).
Table 2.
Central Phenomenon: Is the heart sick enough? Is the body well enough? Is there enough social/emotional support to make it through the process? | ||
---|---|---|
Themes | Vignette Type | Illustrative Quotations (Participant Race) |
1. Forming an Overall Impression: Critiquing appearance of women more harshly than men | ||
Strong reactions to photos for women based on weight, age, hair, make-up, and facial expression | African-American Woman | I would say that she looks so anxious, that might be off-putting but I have seen, you know, sort of patients in her situation. (Minority woman participant) Whether someone’s…big-boned, naturally a heavy person…eyeballing this lady, she looks like she’s never been petite… (White woman participant) She looks tired. I wonder if there’s a little bit of like muscle wasting. She looks a little scared as well, too… I mean, from my standpoint, looks healthy; appropriate age. I wonder how old she is. African-Americans sometimes can look younger than their stated age, but no, she just…looks like a healthy, scared, maybe chronically-ill woman. (White woman participant) |
White Woman | I would say that she is older, that she probably has been through a lot, and she looks as though she has depth in her eyes and meaning that she’s not demented, spacing out… I also am thinking she didn’t have time to do certain things, like you know—see this is the part I don’t like. You know her hair is not dyed one color, yet she probably would have if she was having better health and had more time and stuff… And this is why I don’t like photos. (White woman participant) | |
2. Identifying Urgency: Believing African-American man was sicker | ||
Greater urgency for the African-American male than the White male | African-American Man | So again, depending on what we can do with intravenous medications in hospital. He might be someone who we could get on a launching pad for a re-transplant. (White man participant) |
White Man | So he’s chronically sick. Chronically, he would qualify for the advanced therapy. But we just have to make sure he’s compliant. (Minority woman participant) | |
3. Evaluating the Appropriateness of Prior Care for Women: Believing African-American woman’s care was less appropriate than the White woman | ||
Greater concern for the African-American woman than the White woman | African-American Woman | She needed to have something done three or four months ago… She needs help, she needs something really soon. (Minority woman participant) I think I’ve shared how disappointed I am that she’s a year late to being presented, that’s probably my most common thought. (White woman participant) |
White Woman | Just making sure she’s on guideline directed medical therapy and if not, why she’s not on guideline directed medical therapy…which is another reason why her heart failure is in the advanced stages. (White participant/gender not provided) | |
4. Anticipating Challenges: Believing similar forms of social support were adequate for men and inadequate for women, particularly African-American women | ||
Concern that children are liabilities for women, particularly for African- American women | African-American Woman | In my experience most people with younger kids, they want to be the strong parent who is there to provide for them, not sick at home or in the hospital and that sort of thing… I mean it’s going be an aspect of her care…an added layer of complexity, for her care. I mean it wouldn’t be prohibitive by any stretch… I absolutely want to help her out but it just going to be another burden for her. (White woman participant) We didn’t really talk about whether she has any anxiety. It’s typical for women to have anxiety, particularly when they’re taking care of a lot of other things in life like teenagers. (White woman participant) |
White Woman | She has two children dependents and they’re not old enough to truly be helpful and actually, they’re a liability in terms of being sick. (White man participant) And if the patient says, “Oh, I have to take care of my kids. Like, there’s no way I can take all this time away from the family to just focus on me getting through a VAD,” then they are really in a pickle. (White woman participant) |
|
Questioning family dynamics for women, particularly African- American women | African-American Woman | This concerns [me] in terms of the support, the 10 and 15-year-old and then just one vehicle. And then in terms of would her spouse be able to take her to appointments and things like that. (Minority woman participant) She has a 10-year-old? This can’t be her kids. I mean, she has a kid at the age of 53. I’m just doing the math. Giving birth at the age of 53 is a little bit late in life. So, she has two young kids at home, whereas hers or not, I don’t know. (White man participant) As long as we actually figure out who is taking care of these kids and who is the caregiver for all three of them, meaning the kids and her, because if she goes for any kind of advanced therapies, a caregiver is needed. (White man participant) Then the question is, “Does she have any support?” If the grandkids are living with grandma, then it sounds like maybe the kids are unavailable, that’s how I would interpret that. (Minority woman participant) |
White Woman | …we just have to make sure that they have a good caregiver plan in place and understand what type of stress that this would bring on so that we have the ability to cope with it. And that they’re not kind of surprised by how much work it is from their standpoint as well after transplantation or VAD. (Minority man participant) …for advanced heart failure treatment, I’d be definitely worried about finances and the burden on the spouse to be a caregiver because right now sounds like she’s a caregiver for her children and then her spouse is working. So, that would be a concern on social support. (White woman participant) |
|
Concern for the adequacy of finances, slightly more for African- American women | African-American Woman | I think that again the issue becomes the insurance… I don’t necessarily have an opinion as to which one would suit her better. But I know no matter what we do the finance thing is going to be a struggle. (White man participant) You’d want to know that in terms of seeing what can she be eligible for, then try to figure out the next steps too, and does her family have the resources, as we don’t want to bankrupt them either. (Minority woman participant) Most people with heart failure are poor. And, they’re socioeconomically disadvantaged and are on Medicaid or Medicare. (Minority woman participant) |
White Woman | …we’re getting closer and closer to saying that…there would be too much financial toxicity for transplant. (White man participant) …it’s more of an assessment on finance to see if they have the financial stability to be able to handle the burden of advanced therapies. (White woman participant) Medicaid can be tricky depending on what her financial situation is. [This] would not be a problem for a VAD, but when it comes to post transplant medication affordability, it becomes a real problem. And so, we really have to work out what her finances are… (White man participant) |
|
5. Evaluating Trust and Making the Ultimate Recommendation: Recommending VAD over transplant for all subgroups | ||
Offering all groups VAD irrespective of race or gender | African-American Man | I think that overall, he is an appropriate candidate at least for a destination therapy LVAD. Part of the reason I’m leaning towards it as I mentioned is because he is a big O and he’s clearly sliding clinically. I think he needs advance therapy sooner rather than later, and so I’d probably go the route of VADing first. (Minority woman participant) |
White Man | I would lean more towards VAD. His peripheral artery disease could be concerning once he’s on immunosuppression. It could be exacerbated. (White woman participant) | |
African-American Woman | I would say in this case, I’d probably consider LVAD as a bridge, and you’d want to know what nephrology would have to say. But if everyone said, “The kidneys are fine,” I’d go with LVAD as a bridge or a bridge to decision maybe and see if things improve, and if she’ll feel better, and then hopefully she could get transplanted. (Minority woman participant) I’d still do the LVAD. I think it will buy her time… maybe if we could bridge her to some sort of a transplant. (White woman participant) |
|
White Woman | To summarize, I would not put a heart in this patient because of the diabetes and because of the kidney. Second, in order to proceed with an LVAD we need to verify two things: first of all, the support of the husband and get a psych consult whether her depression is under control. And the second thing I’m going to look for is to try and explain to myself why is the hemoglobin so low if she doesn’t have any kind of hemolysis. (White man participant) |
LVAD indicates left ventricular assist device.
1. Forming an Overall Impression: Critiquing Appearance Of Women More Harshly
Vignette photos were not welcomed by all participants. Some participants avoided dwelling on the photo and instead developed clinical assessments from the histories and photos. Others had strong reactions to the photos, particularly the women patients. Negative impressions were focused on the women vignette’s visual appearance, including age, weight, hair, makeup, and facial expression.
“When I see her, I don’t think of her as totally friendly, I see someone who’s a little unkempt to some extent, and yet she’s probably fine and normal. That was my immediate reaction of not wanting the photo. Because I’m now making a decision about whether she is capable of taking care of herself or a machine based on her hair. Maybe there’s value there, but that’s not how we do it. And so, I was upset to see the photos. So anyway, that’s my feeling.” (White woman participant/ White woman patient vignette)
2. Identifying Urgency: Believing African-American Man Was Sicker
Participants believed that the patients had clinical histories that warranted urgent evaluations for heart failure therapies. However, participants believed that the African-American man was sicker than the other vignette categories. Both the White and African-American women were perceived as equally sick.
“His risk of death in the next few months is very high. Again, still can’t decide his eligibility, but it means it may be indicated in an urgent setting for transplantation down the road.” (White man participant/ African-American man patient vignette)
3. Evaluating Appropriateness of Prior Care: Believing African-American Woman’s Care Was Less Appropriate Than The White Woman
Participants were concerned about whether appropriate treatment was provided prior to referral for advanced heart failure therapies. Prior care was perceived to be inadequate for the women vignettes. Concerns for inappropriate care were greater for the African-American woman compared to the White woman vignette.
“It’s a shame that this lady was only diagnosed two years ago. I mean I get angry about that. I mean particularly being a [minority] provider, I see that many patients that are referred to me regardless of their race tend to be referred late from a heart failure standpoint. I find that my minority patients, particularly my African American patients, are referred even later… Many times it’s because their symptoms were going unrecognized by the people that were taking care of them…or their symptoms weren’t believed… They tell me many stories and I’m hoping that this isn’t the case for her but unfortunately if you see it enough times…it starts to dishearten you.” (Minority man participant/ African-American woman patient vignette)
4. Anticipating Challenges: Believing Similar Forms Of Social Support Were Adequate For Men And Inadequate For Women, Particularly African-American Women
Participants were concerned about medical comorbidities such as peripheral arterial disease and chronic kidney disease irrespective of patient vignette category. However, the assessment of social support differed by vignette gender. Participants believed that the women vignettes were the primary caregivers for children and found the spouse as an inadequate form of support; men vignettes were perceived as having more adequate caregiver support. Children were considered liabilities, particularly for the African-American woman vignette. Participants also had more concerns about family dynamics and the adequacy of finances of the African-American woman vignette.
“Is the husband willing to help? She’s married, that certainly doesn’t mean that he’s necessarily going to be the person bringing her to appointments or helping… I mean, just making sure that there’s the social support to make sure that she’s successful, and that we’re not hurting her more by doing anything else.” (White woman participant/ African-American woman patient vignette)
“…because she’s African-American, it sounds like her socioeconomic status is not the greatest – one car, she’s working, disability; those sorts of things that make me… think that she’s probably not as socioeconomically stable as other patients. Especially, since she lacked healthcare insurance a couple of times.” (White woman participant/ African-American woman patient vignette)
“I’m just worried about the fact that she’s taking care of little kids. She does have a spouse who will be her caregiver and so she does have support but I mean thus far nothing is a red flag, it’s just concern that those two kids need to be taken care of but she’s in the hospital.” (Minority man participant/African-American woman patient vignette)
5. Evaluating Trust and Making Ultimate Recommendation: Recommending VAD Over Transplant For All Subgroups
Trust was based on interpersonal interactions and patient behavior. Adherence had less of a role in evaluating trust. Adherence was considered a social determinant of health, and participants felt that the women participants deserved the benefit of doubt. Overall, participants supported providing inotropes to patients in order to improve kidney function with the intention of offering VAD. VAD instead of transplant was recommended in vignettes irrespective of race or gender category.
“It’s just really challenging. I mean, you meet a person and they’re under-insured. They have a family, they’re a regular person, right? It’s easier when someone doesn’t have anyone; they’re divorced or they’ve never had kids and…they failed completely on the social side, but she’s got enough soft things that will make it challenging, and in our program, we would say, ‘We’ll take a chance on her for a VAD but not for a heart.’ ”(White man participant/ White woman patient vignette)
Supplemental Survey Results
When comparing results for only women vignettes, final recommendations for each treatment option were similar for the African-American woman and White woman vignettes [heart transplant: 7.53 (Standard error 0.59) African-American versus 6.53 (0.61) White, p=0.56; bridge to transplant VAD: 8.11 (0.58) African-American versus 7.78 (0.57) White, p=0.79; destination therapy: 7.00 (0.77) African-American versus 7.48 (0.63) White, p>0.99; no therapies: 1.40 (0.18) African-Americans versus 1.43 (0.25) Whites, p>0.99; Table 3]. There were no significant differences in participant’s ratings of all clinical and social factors fully adjusted for multiple comparisons (Table 3). In the secondary analysis, survey results were combined from this study (N=46) and a prior study of healthcare professionals who were randomized to either African-American man or White man vignette and completed interviews (N=44, Supplemental Table 4).7 Recommendations for heart transplant trended lower for White Women than other groups. VAD recommendations trended higher for African-American men than other groups. When isolating factors of race/ethnicity and gender, support for advanced therapies trended higher for African-American women than other groups. However, final recommendations were similar across race and gender groups.
Table 3.
Women Vignettes | |||||
---|---|---|---|---|---|
African-American | White |
P value |
|||
Mean | (SE) | Mean | (SE) | ||
TREATMENT RECOMMENDATIONS | |||||
Heart Transplant | 7.53 | (0.59) | 6.53 | (0.61) | 0.56 |
Bridge to Transplant VAD | 8.11 | (0.58) | 7.78 | (0.57) | 0.79 |
Destination VAD | 7.00 | (0.77) | 7.48 | (0.63) | >0.99 |
No Therapies | 1.40 | (0.18) | 1.43 | (0.25) | >0.99 |
FACTORS IMPACTING DECISION | |||||
HPI | 9.45 | (0.23) | 9.33 | (0.21) | 0.79 |
Age | 9.60 | (0.22) | 9.50 | (0.27) | 0.79 |
Race or Ethnicity | 9.35 | (0.48) | 7.29 | (0.88) | 0.23 |
Gender | 9.35 | (0.48) | 7.14 | (0.84) | 0.21 |
Height/Weight/BMI | 8.40 | (0.47) | 8.08 | (0.42) | 0.79 |
Insurance | 8.55 | (0.56) | 7.66 | (0.75) | 0.79 |
Blood Type & PRA | 9.05 | (0.51) | 8.85 | (0.48) | 0.79 |
Cardiac History | 9.75 | (0.14) | 9.85 | (0.11) | 0.85 |
NYHA & Vitals | 9.65 | (0.25) | 9.75 | (0.14) | >0.99 |
Medications | 9.70 | (0.13) | 9.25 | (0.42) | 0.91 |
Other Medical/Surgical History | 8.70 | (0.38) | 8.73 | (0.28) | 0.91 |
Social History | 8.20 | (0.39) | 7.65 | (0.42) | 0.79 |
Adherence | 8.25 | (0.36) | 7.38 | (0.38) | 0.42 |
Cardiac Diagnostic | 9.70 | (0.13) | 9.13 | (0.32) | 0.64 |
Pulmonary Studies | 9.75 | (0.14) | 8.60 | (0.35) | 0.08 |
Laboratory test | 8.95 | (0.32) | 8.53 | (0.36) | 0.79 |
Infectious Disease | 9.90 | (0.07) | 9.35 | (0.26) | 0.42 |
Cancer Screening | 9.80 | (0.14) | 9.05 | (0.48) | 0.45 |
Additional Studies | 8.00 | (0.64) | 7.83 | (0.57) | 0.85 |
Likert scores are 1 to 10, with 10 representing greatest support and 1 least support for offering advanced heart failure therapies. P values have been adjusted for false discovery rate. BMI indicates body mass index; FDR, false determination rate; HPI, history of present illness; NYHA, New York Heart Association; PRA, panel-reactive antibody; SE, standard error; VAD, ventricular assist device.
DISCUSSION
In a national study of clinicians, both patient gender and race impacted the decision-making process for heart transplant allocation despite patients having identical case presentations. Compared to male patients, female patients were judged more harshly according to their appearance. The African-American man was thought to be sicker than the White man and the women of both races. Social support assessments were more critical when the patient was a woman, particularly African-American. Spouses were often deemed inadequate forms of support when the patient was a woman. Children were considered liabilities when the patient was a woman. Ultimately bridge to transplant VAD was recommended over transplant for patients irrespective of patient race and gender, but differences were found between vignettes that might negatively impact the delivery of care. For the first time, this national study robustly demonstrates how subjective assessments can be influenced by gender and race biases in the allocation of advanced heart failure therapies.
This contemporary study aligns with a historical body of reports and studies, while extending these findings to decision-making in advanced heart failure. In 1991, the Association of American Medical Colleges Council on Ethical and Judicial Affairs identified gender bias as an etiology of variability in provider decision-making and provided a call to action for multiple leading medical organizations.13 Approximately a decade later, a study of physicians revealed reduced likelihood of offering a cardiac catheterization to African-American women compared to White men despite having identical clinical histories.23 A more recent study observed a significant correlation between level of implicit bias and likelihood of a cardiologist recommending a cardiac catheterization to a woman with the same clinical history as a man.24 While gender bias has been increasingly addressed as a public health issue, little progress has been achieved.25
Ultimate recommendations for advanced heart therapies differed from a recent study that favored transplant over VAD in White men compared to African-American men with identical clinical histories.7 In this study which focused on African-American and White women patients, bridge to transplant VAD trended more favorably than transplants for all patients. While the secondary analysis of survey results from the prior study combined with this one revealed no major differences in treatment recommendations for any gender or race group, recommendation differences in the interview conversations are noteworthy. The allocation of advanced heart failure therapies is distinct from cardiac catheterization referral processes, which can be recommended by an individual healthcare professional. Similar to other organ replacement therapies, a multidisciplinary team of healthcare professionals decide who is appropriate for advanced heart therapy. Conversations rather than surveys guide these allocation meetings, and more dominant members may lead the conversations and control the final decision.7 In addition, the differences in concerns by gender and race could contribute to a delay in treatment, which could worsen outcomes.
The differences between reality and bias are important philosophical questions raised by this study. Assumptions raised by healthcare professionals in this study reflect what is observed and valued in society. According to the Family Caregiver Alliance, between 53–68% of caregivers are women.26 In U.S. society, the most valued traits are appearance in women and honesty in men.27 Healthcare professionals were more critical of the idea of a male caregiver and of the appearance of women. It is easy to infer that participants were providing assessments based upon their reality, but the danger lies in applying a stereotype to a population or individual. Stereotypes often yield bias and lead to health inequity.28 These gender and race biases may be the underlying reasons for unequitable allocation of advanced heart failure therapies by gender and race.
There is an urgent need to standardize assessment of subjective criteria for advanced heart therapies. Guidelines provide objective criteria for determining who is ill enough to consider advanced heart therapies.29,30 However, criteria for many of the relative contraindications for advanced therapies are subjective and variable.29,30 More subjective relative contraindications, namely social support and adherence, are sources of potential gender and race biases in the allocation of advanced heart therapies.12,13,31 Part of the reason for subjective assessments rather than objective assessments may be due to limited data.32 A number of different objective measures for social support and adherence exist, but most of the evidence comes from single center studies and other organ replacements.32 Thus, the governing bodies for heart and lung transplantation and social work recommend that standardized psychosocial evaluations be routinely performed among patients being considered for advanced heart therapies, but do not elaborate which measures of social support should be used or the data supporting their use.33 Important areas for future investigation include generating multi-center data on the use of objective social assessments for advanced heart therapy allocation.
Additional steps can be taken to reduce the influence of bias during advanced heart therapy allocation. As demonstrated in this study, healthcare professionals had altruistic plans for each patient, but patient gender and race influenced the decision-making process. Bias reduction training may create a culture of equity for advanced heart failure patients, particularly among individuals with a desire to parallel one’s behavior with one’s belief system.34 Bias training has been effective in reducing implicit bias and changing behavior of health care professionals.35,36 Small systematic changes may also improve health equity.12 Participants in this study identified patient photographs and descriptions of children as potential sources of bias. Steps can be taken to avoid including these data during routine presentations of candidates for advanced therapies. Finally, this study does not address shared decision-making between the patient and healthcare professional; assuring that patients are well educated about their options can assist the health care professional in advocating on their behalf.37
Study Limitations
This study was subject to several limitations. First, the single clinical vignette used does not represent the full spectrum of possible clinical presentations. However, this vignette represented a patient with multiple relative contraindications for advanced heart therapies which uniformly presented a picture of advanced disease while creating uncertainty about appropriateness of advanced therapies. Such a vignette is appropriate for understanding how patient gender and race may influence healthcare professionals’ decisions.38 Second, this study included a small number of participants focused on men vignettes and was not designed to have equal number of men and women vignettes. This limits the power to evaluate significant differences in the supplementary quantitative surveys including the interaction of participant demographics and limits generalizability which is inherent to qualitative design. However this sample was ample for the qualitative analysis, representing more participants than typically used in qualitative studies.21 Sample size was appropriate by thematic saturation analysis. Last, some of the participants previously participated in evaluating decision-making for African-American man and White man patients. They may have suspected the objectives of this study and exhibited Hawthorne effect by providing socially desirable results under observation; however, that would bias results towards the null of no differences in gender and race-based evaluations. No participants were aware of results of the prior study of only men patients.
CONCLUSIONS
In a study of U.S. healthcare professionals, the process of allocating advanced heart failure therapies was influenced by patient gender and race. Women patients were judged more harshly for their appearance and degree of social support than men of both races with identical clinical and social histories, particularly African-American women. Final recommendations in this case supported bridge to transplant VAD over transplant, irrespective of patient gender and race. This study illustrates how bias can impact the allocation of advanced heart failure therapies and possibly contribute to disparate allocation of advanced therapies to women, racial minority women and men. Further investigation and implementation of bias reduction strategies are needed.
Supplementary Material
Key Points.
Question:
Does bias against a patient’s gender and race influence allocation of advanced heart failure therapies?
Findings:
In a qualitative study of healthcare professionals, there was bias against women compared to men when evaluating appearance and social support, particularly among African-American women. Final recommendations were not different for groups defined by gender or race; all were offered VAD over transplant.
Meaning:
Although gender and race were not associated with allocation of advanced heart failure therapies in this study, bias against women may contribute to delayed allocation and lower allocation of advanced therapies to women nationally.
Acknowledgment
Funding/Support: Dr. Breathett received support from National Heart, Lung, and Blood Institute (NHLBI) K01HL142848 and NHLBI 2R25HL126146-05 Subaward 11692sc; University of Arizona Health Sciences, Strategic Priorities Faculty Initiative Grant, and University of Arizona, Sarver Heart Center, Women of Color Heart Health Education Committee. Dr. Hebdon received support from National Institute of Health (NIH) T32NR013456. Mr. Luy received support from NIH R25HL108837.
Role of the Funder/Sponsor: The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
Footnotes
Conflict of Interest Disclosures: None reported
References
- 1.Breathett K, Allen LA, Helmkamp L, et al. The Affordable Care Act Medicaid Expansion Correlated With Increased Heart Transplant Listings in African-Americans But Not Hispanics or Caucasians. JACC Heart Fail. 2017;5(2):136–147. doi: 10.1016/j.jchf.2016.10.013 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Breathett K, Allen LA, Helmkamp L, et al. Temporal Trends in Contemporary Use of Ventricular Assist Devices by Race and Ethnicity. Circ Heart Fail. 2018;11(8):e005008. doi: 10.1161/CIRCHEARTFAILURE.118.005008 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Benjamin EJ, Muntner P, Alonso A, et al. Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association. Circulation. 2019;139(10):e56–e66. doi: 10.1161/CIR.0000000000000659 [DOI] [PubMed] [Google Scholar]
- 4.Farmer SA, Kirkpatrick JN, Heidenreich PA, Curtis JP, Wang Y, Groeneveld PW. Ethnic and racial disparities in cardiac resynchronization therapy. Heart Rhythm. 2009;6(3):325–331. doi: 10.1016/j.hrthm.2008.12.018 [DOI] [PubMed] [Google Scholar]
- 5.Mezu U, Ch I, Halder I, London B, Saba S. Women and minorities are less likely to receive an implantable cardioverter defibrillator for primary prevention of sudden cardiac death. Europace. 2012;14(3):341–344. doi: 10.1093/europace/eur360 [DOI] [PubMed] [Google Scholar]
- 6.Breathett K, Liu WG, Allen LA, et al. African Americans Are Less Likely to Receive Care by a Cardiologist During an Intensive Care Unit Admission for Heart Failure. JACC Heart Fail. 2018;6(5):413–420. doi: 10.1016/j.jchf.2018.02.015 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Breathett K, Yee E, Pool N, et al. Does Race Influence Decision Making for Advanced Heart Failure Therapies? J Am Heart Assoc. 2019;8(22):e013592. doi: 10.1161/JAHA.119.013592 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Colvin M, Smith JM, Hadley N, et al. OPTN/SRTR 2017 Annual Data Report: Heart. Am J Transplant. 2019;19 Suppl 2:323–403. doi: 10.1111/ajt.15278 [DOI] [PubMed] [Google Scholar]
- 9.Chang PP, Chambless LE, Shahar E, et al. Incidence and survival of hospitalized acute decompensated heart failure in four US communities (from the Atherosclerosis Risk in Communities Study). Am J Cardiol. 2014;113(3):504–510. doi: 10.1016/j.amjcard.2013.10.032 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.DeFilippis EM, Truby LK, Garan AR, et al. Sex-Related Differences in Use and Outcomes of Left Ventricular Assist Devices as Bridge to Transplantation. JACC Heart Fail. 2019;7(3):250–257. doi: 10.1016/j.jchf.2019.01.008 [DOI] [PubMed] [Google Scholar]
- 11.Hsich EM. Sex Differences in Advanced Heart Failure Therapies. Circulation. 2019;139(8):1080–1093. doi: 10.1161/CIRCULATIONAHA.118.037369 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Breathett K, Jones J, Lum HD, et al. Factors Related to Physician Clinical Decision-Making for African-American and Hispanic Patients: a Qualitative Meta-Synthesis. J Racial Ethn Health Disparities. 2018;5(6):1215–1229. doi: 10.1007/s40615-018-0468-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.McMurray RJ, Clarke OW, Barrasso JA, et al. Gender Disparities in Clinical Decision Making. JAMA. 1991;266(4):559–562. doi: 10.1001/jama.1991.03470040123034 [DOI] [PubMed] [Google Scholar]
- 14.Sadler GR, Lee H-C, Seung-Hwan Lim R, Fullerton J. Recruiting hard-to-reach United States population sub-groups via adaptations of snowball sampling strategy. Nurs Health Sci. 2010;12(3):369–374. doi: 10.1111/j.1442-2018.2010.00541.x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.O’Brien BC, Harris IB, Beckman TJ, Reed DA, Cook DA. Standards for Reporting Qualitative Research: A Synthesis of Recommendations. Academic Medicine. 2014;89(9):1245–1251. doi: 10.1097/ACM.0000000000000388 [DOI] [PubMed] [Google Scholar]
- 16.Bertrand M, Mullainathan S. Are Emily and Greg More Employable than Lakisha and Jamal? A Field Experiment on Labor Market Discrimination. National Bureau of Economic Research; 2003. http://www.nber.org/papers/w9873. Accessed December 12, 2016. [Google Scholar]
- 17.Li AC, Kannry JL, Kushniruk A, et al. Integrating usability testing and think-aloud protocol analysis with “near-live” clinical simulations in evaluating clinical decision support. International Journal of Medical Informatics. 2012;81(11):761–772. doi: 10.1016/j.ijmedinf.2012.02.009 [DOI] [PubMed] [Google Scholar]
- 18.Shafer K, Lohse B. How to conduct a cognitive interview: a nutritional education example. http://www.au.af.mil/au/awc/awcgate/usda/cog_interview.pdf.
- 19.Strauss A, Corbin JM. Basics of Qualitative Research: Grounded Theory Procedures and Techniques. Thousand Oaks, CA, US: Sage Publications, Inc; 1990. [Google Scholar]
- 20.Curry LA, Nembhard IM, Bradley EH. Qualitative and mixed methods provide unique contributions to outcomes research. Circulation. 2009;119(10):1442–1452. doi: 10.1161/CIRCULATIONAHA.107.742775 [DOI] [PubMed] [Google Scholar]
- 21.Creswell JW. Qualitative Inquiry and Research Design: Choosing Among Five Approaches. SAGE Publications; 2012. [Google Scholar]
- 22.Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57(1):289–300. [Google Scholar]
- 23.Schulman KA, Berlin JA, Harless W, et al. The effect of race and sex on physicians’ recommendations for cardiac catheterization. N Engl J Med. 1999;340(8):618–626. doi: 10.1056/NEJM199902253400806 [DOI] [PubMed] [Google Scholar]
- 24.Daugherty SL, Blair IV, Havranek EP, et al. Implicit Gender Bias and the Use of Cardiovascular Tests Among Cardiologists. J Am Heart Assoc. 2017;6(12). doi: 10.1161/JAHA.117.006872 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Heise L, Greene ME, Opper N, et al. Gender inequality and restrictive gender norms: framing the challenges to health. The Lancet. 2019;393(10189):2440–2454. doi: 10.1016/S0140-6736(19)30652-X [DOI] [PubMed] [Google Scholar]
- 26.Who Are Family Caregivers? https://www.apa.org. https://www.apa.org/pi/about/publications/caregivers/faq/statistics. Accessed April 20, 2020.
- 27.Parker K, Horowitz JM, Stepler R. 2. Americans see different expectations for men and women. Pew Research Center’s Social & Demographic Trends Project. December 2017. https://www.pewsocialtrends.org/2017/12/05/americans-see-different-expectations-for-men-and-women/. Accessed April 20, 2020. [Google Scholar]
- 28.Smedley B, Stith A, Nelson A. Unequal Treatment: Confronting Racial and Ethnic Disparities in Health Care (with CD). Institute of Medicine; 2003. https://download.nap.edu/openbook.php?isbn=030908265X. Accessed June 2, 2012. [PubMed] [Google Scholar]
- 29.Feldman D, Pamboukian SV, Teuteberg JJ, et al. The 2013 International Society for Heart and Lung Transplantation Guidelines for mechanical circulatory support: Executive summary. The Journal of Heart and Lung Transplantation. 2013;32(2):157–187. doi:wi [DOI] [PubMed] [Google Scholar]
- 30.Mehra MR, Kobashigawa J, Starling R, et al. Listing Criteria for Heart Transplantation: International Society for Heart and Lung Transplantation Guidelines for the Care of Cardiac Transplant Candidates—2006. The Journal of Heart and Lung Transplantation. 2006;25(9):1024–1042. doi: 10.1016/j.healun.2006.06.008 [DOI] [PubMed] [Google Scholar]
- 31.Hart M. Subjective Decisionmaking and Unconscious Discrimination. Ala L Rev. 2004;56:741–792. [Google Scholar]
- 32.Bui QM, Allen LA, LeMond L, Brambatti M, Adler E. Psychosocial Evaluation of Candidates for Heart Transplant and Ventricular Assist Devices: Beyond the Current Consensus. Circ Heart Fail. 2019;12(7):e006058. doi: 10.1161/CIRCHEARTFAILURE.119.006058 [DOI] [PubMed] [Google Scholar]
- 33.Dew MA, DiMartini AF, Dobbels F, et al. The 2018 ISHLT/APM/AST/ICCAC/STSW recommendations for the psychosocial evaluation of adult cardiothoracic transplant candidates and candidates for long-term mechanical circulatory support. J Heart Lung Transplant. 2018;37(7):803–823. doi: 10.1016/j.healun.2018.03.005 [DOI] [PubMed] [Google Scholar]
- 34.Levy N, Harmon-Jones C, Harmon-Jones E. Dissonance and discomfort: Does a simple cognitive inconsistency evoke a negative affective state? Motivation Science. 2018;4(2):95–108. doi: 10.1037/mot0000079 [DOI] [Google Scholar]
- 35.Stone J, Moskowitz GB, Zestcott CA, Wolsiefer KJ. Testing active learning workshops for reducing implicit stereotyping of Hispanics by majority and minority group medical students. Stigma and Health. 2019: 10.1037/sah0000179 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Carnes M, Devine PG, Baier Manwell L, et al. The effect of an intervention to break the gender bias habit for faculty at one institution: a cluster randomized, controlled trial. Acad Med. 2015;90(2):221–230. doi: 10.1097/ACM.0000000000000552 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Alfandre D. Clinical Recommendations in Medical Practice: A Proposed Framework to Reduce Bias and Improve the Quality of Medical Decisions. J Clin Ethics. 2016;27(1):21–27. [PubMed] [Google Scholar]
- 38.Balsa AI, McGuire TG. Prejudice, clinical uncertainty and stereotyping as sources of health disparities. J Health Econ. 2003;22(1):89–116. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.