“You start feeling comfortable, you just start sharing:” A qualitative study of patient distress screening in Black and White patients with endometrial cancer

Abstract

Objectives:

Black patients with endometrial cancer are less likely to express distress and receive referrals for support services compared to White patients. We aim to characterize patient perceptions of the National Comprehensive Cancer Network Distress Thermometer and Problem List (NCCN DT & PL), a common distress screening tool, among Black and White patients with endometrial cancer and determine strategies to improve equity in referral to appropriate support services.

Methods:

We conducted semi-structured interviews with 15 Black and 15 White patients with endometrial cancer who reported varying levels of distress on the NCCN DT & PL. Interviews were audio-recorded, transcribed, evaluated through staged content analysis, and salient themes were compared by patient race.

Results:

The NCCN DT & PL was generally considered understandable, however the word “distress” could be alienating to participants who considered their stress to be less “drastic.” Black participants mentioned fewer negative emotions such as worry and sadness in describing distress and spoke more often of a positive outlook. Additionally, Black participants emphasized the importance of relationship-building with clinicians for open communication on the NCCN DT & PL and clinical encounter. Finally, participants were divided on whether they would alter the way they completed the NCCN DT & PL given more information on cut off scores for referrals, but generally expressed a desire for more direct offers of support services.

Conclusions:

Relationship-building, open communication around emotion, and longitudinal direct offers of support emerged as avenues to reduce inequities in referral to supportive services for patients with endometrial cancer.

Introduction

Distress, “an unpleasant experience [that] may interfere with the ability to cope effectively with cancer, its physical symptoms and its treatment,” is a common reaction following diagnosis and treatment of cancer.[1] Distress is associated with lower quality cancer care, including decreased adherence to recommended treatments, poorer quality of life, fewer follow-up appointments and, in some instances, shorter survival times.[1–8] Given the potential implications of untreated distress, the National Comprehensive Cancer Network Distress Thermometer and Problem List (NCCN DT & PL) has been used as a common screening tool nationwide to quantify distress and associated practical, family, emotional, spiritual, and physical issues in patients with cancer (Figure 1). A score of 4 or greater out of 10 on the NCCN DT has generally been agreed upon as a screening cut off for clinically significant distress and referral to additional services.[2,9–11]

Figure 1:

National Comprehensive Cancer Network Distress Thermometer and Problem List¹

The NCCN DT & PL was initially developed as a distress screening tool in prostate cancer and has subsequently been adopted as a standard of care in screening for distress in a wide range of oncologic conditions, including gynecologic malignancies.[12,13] However, validation studies of the NCCN DT & PL in both general oncologic populations and gynecologic oncology populations have included predominantly White patient samples, or have not examined race and/or ethnicity at all.[9,10,14–18] Our team and others have recently documented differences in patient reported distress on the NCCN DT & PL between non-Hispanic Black (Black) and non-Hispanic White (White) patients with breast or endometrial cancer and subsequent inequities in referral to support services.[19,20] This is particularly meaningful in the context of known large racial disparities in endometrial cancer survival, regardless of stage, grade and histologic subtype.[21–25]

Supportive services including patient navigation, social work, financial counseling, and therapy have been recognized as key components of comprehensive cancer care. Patient navigation services such as financial support, transportation, clinician coordination, and linkage to community resources have been associated with decreased time to definitive diagnosis and treatment especially for patients with a lower socioeconomic status.[26,27] Thus, quickly and effectively recognizing patient distress and needs and linking patients with appropriate services can have a meaningful impact on their care.

This study uses a qualitative approach to explore perceptions of the NCCN DT & PL among Black and White patients with endometrial cancer. The aim of this research is to identify ways to improve distress screening which could subsequently reduce inequities in referral to support services for all patients with endometrial cancer.

Methods

This study included patients receiving care for endometrial cancer at a large academic tertiary care center (Duke University Hospital). All study activities occurred after receiving approval from the Duke University Institutional Review Board (Pro00107490). Qualitative methods are reported in accordance with the consolidated criteria for reporting qualitative studies (COREQ) guidelines.[28] Patients were eligible for inclusion if they were English speakers ≥18 years of age, had a pathologically confirmed diagnosis of endometrial cancer, were seen for care at Duke, self-identified as Black or White, and had received treatment including surgery, chemotherapy, and/or radiation within 12 months of enrollment. A sample of eligible patients was identified through weekly review of clinic rosters. Eligible patients were contacted via telephone prior to clinic appointments. Informed consent was either obtained over the phone at which time a study member would complete a written form on the patient’s behalf or by the patient completing a consent form online. Purposive sampling was used to ensure a race-balanced sample of Black and White participants. We a priori estimated that a sample size of 15 Black and 15 White participants would yield sufficient thematic content and found that we reached thematic saturation after interviewing 30 patients.[29,30] For participant convenience, interviews were conducted in a private clinic room either directly prior to or following a scheduled oncology or radiation clinic appointment. This also mimicked normal clinic flow in which all patients fill out the NCCN DT & PL in the waiting room prior to their appointment. Participants could bring friends or family with them to the interview, if desired. Participants were offered $20 as compensation for their time and participation.

The interview guide was developed in collaboration with the Duke Cancer Institute Behavioral Health and Survey Research Core (BHSRC) with the intention of performing cognitive interviewing on the understandability of the NCCN DT & PL and eliciting patient perspectives on distress and distress screening in cancer care through open-ended questions (see Appendix A).[31] Cognitive interviewing is an approach that provides contextual meaning to how individuals interpret questions and apply meaning from their lived experiences when answering interview or assessment tool questions.[32] Based on interviewer feedback and review of early transcripts, the interview guide was amended to minimize repetition and add additional probes for emerging themes.

Interviews were conducted over Zoom (Zoom Video Communications, San Jose, CA, 2011) by three trained qualitative researchers. These researchers, MF, SM, and LJF, currently work within our institution’s behavioral health and survey research core with credentialing as a social worker, senior clinical research specialist, and PhD researcher respectively. Interviewers did not take detailed field notes. Participants did not have any relationship with the interviewers prior to the interview. Interviewers were aware of patient name and treatment being received. All three interviewers identify as female in keeping with our patient cohort. Given the potentially sensitive nature of the interview material, every attempt was made for participant-interviewer race concordance as previous research has shown it can increase participant comfort.[33] All fifteen White patients were interviewed by a race concordant interviewer, however, due to scheduling conflicts, only six of fifteen interviews with Black patients were conducted with a race concordant interviewer.

Patient data including demographics, cancer histology, grade, stage, current treatment, current and past distress scores, and current problem list concerns was collected from the electronic medical record and stored in REDCap.[34,35] Participants completed a REDCap survey with additional demographic characteristics including education, marital status, and financial security. Financial security was categorized as high, medium or low using the following prompts: after paying the bills you still have enough money for special things that you want (high); you have enough money to pay the bills, but little spare money to buy extra or special things (medium); you have money to pay the bills, but only because you have cut back on things (low); and you are having difficulty paying the bills, no matter what you do (low).

All interviews were securely audio-recorded and an initial automated transcript was generated through the Zoom platform. Automated transcriptions were edited for accuracy by members of the study team. A staged approach (familiarization, identifying a thematic framework, indexing, summarizing, and interpretation) was used to conduct content analysis of semi-structured interviews. One researcher (HWR) reviewed five initial transcripts and the interview guide and created a draft codebook. The research team met to review the proposed codes and clarify definitions; the entire team then coded one transcript utilizing the draft codebook and subsequently further clarified and defined codes. Data collection and analysis occurred simultaneously. For data analysis two team members (HWR and BS) independently conducted line-by-line coding of the transcripts using NVivo 12 (QSR International, Doncaster, Australia, 2019) and compared each transcript for consistency, further refining code definitions through discussion of any discrepancies (see Appendix B: Coding Tree). Coders recorded a list of cross-cutting reflections in an overview memo. At the completion of transcript coding, the research team met to review and iterate on cross-cutting reflections and prioritize emerging themes. Finally, a consensus was reached on major themes and two researchers (HWR and BS) identified supporting quotations.

Results

A total of 30 patients (15 Black and 15 White) completed the qualitative interview from April-November 2021. Out of 100 patients contacted at least once, twenty-one patients either declined to participate or were contacted three times without response (N=8 White, N=13 Black) and 8 patients were consented but never interviewed due to scheduling conflicts. Interviews lasted on average 40 minutes (28–87 minutes with average interview time by interviewer being similar at 38, 35, and 31 minutes for MF, LJF and SM respectively). Median participant age was 66 years-old, and distress scores on the interview day ranged from 0–10. Most of our sample had high grade histology (63%), were retired (60%), and had greater than a high school education (70%) (See Table 1).

Table 1:

Participant Characteristics

Characteristic	Black Participants N=15	White Participants N=15	Overall N=30
Age, median (IQR)	64 (60, 68)	68 (57, 74)	66 (58, 70)
Initial Visit Distress Scorea, median (IQR)	0.5 (0,8)	5 (1,10)	2 (0,9)
Interview Distress Score, median (IQR)	2 (0,5.5)	2 (0.5,3.5)	2 (0,5)
Interview Problems, median (IQR)	2 (1,3.5)	3 (1,7.5)	2 (1,6.5)
Visit Type, n (%)
Initial Visit	1 (7%)	3 (20%)	4 (13%)
Post-Op	3 (20%)	5 (33%)	8 (27%)
Treatment	6 (40%)	3 (20%)	9 (30%)
Surveillance	5 (33%)	4 (27%)	9 (30%)
Histology, n (%)
Endometrioid Grade 1/2	3 (20%)	9 (60%)	12 (40%)
Endometrioid Grade 3	1 (7%)	1 (7%)	2 (7%)
Papillary Serous	6 (40%)	2 (13%)	8 (27%)
Clear Cell	1 (7%)	0 (0%)	1 (3%)
Adenosarcoma	0 (0%)	1 (7%)	1 (3%)
Carcinosarcoma	4 (27%)	2 (13%)	6 (20%)
Stage, n (%)
I	3 (20%)	9 (60%)	12 (40%)
II	0 (0%)	1 (7%)	1 (3%)
III	7 (47%)	0 (0%)	7 (23%)
IV	3 (20%)	2 (13%)	5 (17%)
N/A (Pre-Op)	2 (13%)	3 (20%)	5 (17%)
Employment, n (%)
Full-time	3 (20%)	4 (27%)	7 (23%)
Part-time	0 (0%)	1 (7%)	1 (3%)
Unemployed	2 (13%)	2 (13%)	4 (13%)
Retired	10 (67%)	8 (53%)	18 (60%)
Marital Status, n (%)
Single	6 (40%)	1 (7%)	7 (23%)
Married	4 (27%)	10 (67%)	14 (47%)
Divorced	1 (7%)	3 (20%)	4 (13%)
Widowed	4 (27%)	1 (7%)	5 (17%)
Education, n (%)
Some High School	1 (7%)	0 (0%)	1 (3%)
Completed High School/GEDb	4 (27%)	4 (27%)	8 (27%)
Trade School/Associate’s Degree	1 (7%)	2 (14%)	3 (10%)
Some College	5 (33%)	2 (13%)	7 (23%)
Bachelor’s Degree	3 (20%)	4 (27%)	7 (23%)
Graduate Degree	1 (7%)	3 (20%)	4 (13%)
Financial Security, n (%)
Low	3 (20%)	0 (0%)	3 (10%)
Medium	5 (33%)	2 (13%)	7 (23%)
High	7 (47%)	13 (87%)	20 (67%)

^aN=13 White and 12 Black due to missing values

^bGED= Graduate Equivalency Degree

Themes from the interview transcriptions were categorized into three main groupings: understanding the distress thermometer, inputs to the distress thermometer, and follow-up to the distress thermometer with multiple subthemes. Participants were characterized as “low distress’ if their distress score on interview was <4.

Understanding and Using the Distress Thermometer

In general, when directed to reflect on and verbalize the instructions on the NCCN DT & PL, participants found the instructions easy to understand (Table 2). There was variability in the way that participants interpreted the word “distress” on the thermometer. Some participants interpreted “distress” as everyday stress, while others felt the word distress indicated a highly emotional state and felt dissociated from the word. That is, for some participants, distress simply meant “having problems [and] trying to cope,” but for others distress was being “in really bad shape.” Those participants who mentioned that distress was associated with being in a worse state mentioned feeling dissociated from this definition stating “well [the word distress] doesn’t bring myself to mind. Distress is when somebody is really in trouble.”

Table 2:

Representative quotations of patients with endometrial cancer on understandability and usability of the NCCN DT & PL

Descriptive Quote	Participant
Understanding instructions
Well it says, please circle the number that best describes how much distress you’ve been experiencing in the last week, including today. I thought about what’s happened to me this week, including today and I circled it.	White; 64-year-old; high distress
It says circle 0 to 10 that best described how much distress you experienced in the last week. So you want me to let you know, from 1 to 10 with zero meaning no distress, which is not my case, to extreme distress, which is closer to my situation.	Black; 62-year-old; high distress
Meaning of distress
[Distress] means is that I’m probably having a crisis, or something like that might need to call 911.	Black; 55-year-old; high distress
Distress to me means I’m really in bad shape. And needing support and help. Where I don’t feel that I’m ever in that spot. So I’ve pretty much. I mean just, just for the sake of filling out the form I sometimes put one or two. If I’m nervous or something like that, but it doesn’t really, to me I’m not really in distress. I’m just having feelings.	White; 73-yearold; low distress
It could be anything […] running the house, food, going to the grocery store, family problems, dealing with partner’s, family health issues. All of these things, emotional problems, uh fears, nervousness, sad.	Black; 60-year-old; high distress
Emphasis on discussion of the NCCN DT & PL
[…] by me sitting here talking to you about this stuff that we have discussed, it has lowered something in my heart […] It’s like a lighter burden […] It’s amazing how being able to discuss can change your feelings and your outlook on things.	Black; 55-year-old; high distress
I think the face to face and talking to somebody. It makes you really think more about stuff because most of stuff I was just going no no no no. I didn’t feel like that. But when you’re talking to somebody, it kind of makes you really think about it a little bit more.	Black, 68-year-old low distress

Participants also reflected that discussing the NCCN DT & PL with another person engaged them in deeper thinking about aspects of their lives that cause distress, such as practical or financial concerns, which were less directly related to their cancer diagnosis and treatment. Discussing the thermometer and problem list “makes you really think more” and for some participants even provided a therapeutic intervention in and of itself by creating a “lighter burden” to carry. One participant also mentioned that the list of problems on the tool helped to define the bounds of appropriate topics for discussion in the medical encounter including financial, family, and work concerns, was more expansive than she had previously thought. Participants felt that the NCCN DT & PL should be “handed in-person, and discussed with [patients] as to what it is, and why it’s here, and how it would be used.”

Inputs to the Thermometer

We observed qualitative differences in the aspects of personal life, background, and relationship with the healthcare system that Black and White patients considered when filling out the distress thermometer and problem list (Table 3). In general, participants with higher distress mentioned feelings of sadness, fear, worry or anxiety more often than participants with lower distress. White participants mentioned these negative emotions more often in interviews than Black participants. In our interviews, Black participants often referred to negative feelings as in the past or as something “I got over [and] worked through.” This trend was also replicated in the way participants interpreted the distress thermometer itself. In our data, more White participants framed the distress thermometer in emotional terms, whereas Black participants spoke more often of the thermometer in terms of physical symptoms, for instance, saying “it was asking what kind of pain I was in.”

Table 3:

Representative quotations from participants on their background, attitude, and relationship with the healthcare system informing how they filled out the NCCN DT & PL.

Descriptive Quote	Participant
Experiencing emotions and physical symptoms
Yeah being scared. that’s, that’s been my utmost thought is, I’m scared.	White; 76-year-old; high distress
[When I first got my diagnosis] I was depressed and I was crying and, yeah, you know, my nerves was upset	Black; 55-year-old; high distress
I wasn’t really thinking of any of those things [when filling out the thermometer]. It was more, the distress was more, I felt was more emotional than specific things, physical things.	White; 68-year-old; low distress
I guess if you in pain it says circle […] how bad you’re hurting. If I’m in real bad pain, call 911, probably circle 10 number 10.	Black, 55-year-old, high distress
Grit, determination and maintaining positivity
I didn’t have a lot of concerns […] whatever I’m faced with the day that I wake up, and that’s what I deal with. I try not to be concerned too much about the next day.	Black; 60-year-old; low distress
I’ll be alright. Everybody, I know everybody going through something. But I get, I get past it too. Now I have some good days […] I stopped trying to worry. It will tear you down.	Black; 65-year-old; low distress
I just try to stay positive about everything. I might have a moment here and there where […] I get a little whiny, but mainly I try to stay positive.	White; 57-year-old; low distress
Relationships with Healthcare Providers
I have just reached the point where I just, if I got something to say I’m going to have to say it. Because I’m expecting their help and if I don’t say something that can’t happen.	White; 57 year-old; low distress
Knowing that the caregivers, the providers are good helps with it too. Then the honesty and discussing everything with you and explaining everything, and encouraging you to ask questions if you have them, then I think that helps too.	Black; 67-year-old; low distress
It’s been passed through, you know, down that we have had to, you know, hide stuff, […]sometimes I think people might be afraid to say what’s wrong with them, because they don’t know how the doctor might look at them like “I don’t know if we’re going to be able to help you with that” so they won’t even tell them that they got that kind of problem […] And so that’s how it is they just pick [a doctor] that they feel like they can trust. […] you start feeling comfortable you just start sharing what, just don’t feel comfortable sharing stuff with everybody.	Black; 55-year-old; high distress
All you can do is get your treatments, talk to your doctor, and do the best course of action for yourself. But find someone you are comfortable with. Because if you’re not comfortable with them then you won’t ask questions.	Black; 59-year-old; low distress
I think that knowing the doctor better and everything that I will be more open about, you know, what issues that I have […] So the first day coming in, I don’t know if I would have checked all of this stuff [on the problem list]. […] but then I got in and met [the doctor] and, saw, you know, how we kind of had a good rapport, then I felt comfortable discussing things like that with her.	Black; 55-year-old, low distress
Experiencing Bias
I don’t know why [Black patients report lower distress on the NCCN DT] As far as African American people period, men and women it’s always been a myth, I think, that we’ve been able to stand more pain than anybody else. We have. I mean you know because you know slavery and, and different things that our ancestors went through and passed down through the years that we, I guess we just take pain, better than anybody else.	Black; 55-year-old; high distress
Well, because in general, it’s where I live […] those are basically progressive cities, and I don’t really worry about what the police are going to do to me […] So no that hasn’t, I mean it bothers me when I see the stories. But that’s elsewhere, not here. So it doesn’t affect me, but I hate to see other people treated that way too	Black; 67-year-old; low distress
You have subconscious thoughts and conscious thoughts, and you hope that decisions are made on a blind color basis. And when you hear things, those things also become part of your subconscious. And so you do think about it but you hope that that’s not occurring […] if they’re not giving me the best possible care that I think I need to have then I make different choices.	Black; 62-year-old; high distress

Participants spoke of grit and determination in processing their diagnosis and treatment: “I had my difficulties, but it’s cleared up, and I’m moving on (Black participant).” Participants additionally spoke of maintaining a positive outlook which was usually associated with less reported distress. We found that these expressions of positive outlook during difficult times were more commonly mentioned by Black participants compared to White participants (See Table 3). Participants in our sample, regardless of race, also drew on faith as an important part of their outlook and attitude. For these participants, belief in God and a greater purpose re-contextualized cancer and treatment for them as part of a larger spiritual journey to still feel “blessed whichever way that the Lord chose to deal with me (Black participant)” or to express that “my leaning on God has been my way to make it through (White participant).” Finally, participants who expressed feelings of resignation and acceptance also reported lower distress. As one White participant put it “anything that’s causing me distress, there’s nothing that can be done about it. So, I would have to say zero [on the thermometer].”

Participants also described their relationship and comfort with their oncologist as an important factor in how they communicated in the healthcare encounter. The NCCN DT & PL is used to introduce sensitive and distressing topics, therefore the clinician-patient relationship impacts completion of the instrument and discussion of these topics during the medical encounter. In general, participants reported feeling empowered to share information on the NCCN DT & PL and during the clinical encounter. Participants also consistently reported that they have a responsibility to be open and honest to get the most out of their care. However, participants still noted that encouragement from clinicians was helpful to internalize that “nothing should be embarrassing (White participant).” Additionally, some Black participants emphasized the importance of building trust and identifying a clinician who could be an ally especially for sensitive issues highlighted on the NCCN DT & PL. As one participant put it, the doctor “needs to be your best friend when you’re going through this because this is a life-or-death situation (Black participant).”

Finally, we directly queried all participants on the effect of racism and discrimination on reported distress as a focus of this work to better understand race differences in report of distress on the distress thermometer. Racism and prejudice were generally not perceived as personal or individual issues by participants, thus most participants did not consider these when determining a number to report on the distress thermometer. However, one Black participant mentioned that during times of acute or well-publicized racially motivated events, “it brought [my distress] up to a ten.” Additionally, some Black participants mentioned that they were aware that they could experience bias in the medical system, but no participants expressed that they felt they had been treated differently or poorly due to racial identity while receiving their cancer care.

Distress Screening Follow-up

There was no consensus among participants on how the NCCN DT & PL was used after they filled it out. A subset of both Black and White participants reported having no sense of what happened to the questionnaire, whereas others reported that they suspected it was likely reviewed as a means of assessing need for additional support (Table 4). When asked if they would change their score on the distress thermometer knowing more about the purpose of the screening, participants were also split. Some would not change their score and felt they had already filled the thermometer out honestly to their situation, “well I tried to be extremely honest with myself when I was filling out the form. So that wouldn’t have changed. That was my truth.” However, some participants indicated that knowing there was a score cut off for the offer of supportive services would have had an impact stating, “if I needed someone to talk to, I will put a four.”

Table 4:

Representative quotations of patients with endometrial cancer on follow-up from distress screening

Descriptive Quote	Participant
Perceived Use of the NCCN DT & PL
I was just filling it out because I was asked to fill it out. […] Maybe something on top where you first start reading that “we’re here to help” kind of thing. Right, so they know when they’re filling it out, that they’re not just checking off some boxes. It really means something	White; 57-year-old, low distress
I kind of thought that, that’s what the purpose was in a way, that it would be a way for people to get help with things they needed help with.	Black; 55-year-old; low distress
Changing Score
There might have been sometimes when I was on the line that whether or not something was a concern or the number, the distress number, that I might would have gone on the side of marking something as a concern.	White; 54-year-old; low distress
I don’t think I would fill it out any different, because […] to me when you’re going through what you’re going through, they offer, they should offer support. I mean you know that would be an option	White; 69-year-old; low distress
Clarity and Direct Support
If you will put on here, “these services are available to you if you, you know, are willing to say yes you need them and want them.” I would think the woman would answer honestly	White; 77-year-old; high distress
I think you would concentrate more on the form if you knew [it was used to determine support services].	White; 74-year old; Low Distress
I think that’s really important [to know about the cut off level of 4], because I have to be honest with you. I’ve gone to see primary care doctors, and they have a little questionnaire similar to this […] I filled it out but you know what I never heard, nobody ever, nobody has ever addressed that. […] if you’re going to ask me these questions, please follow up you know.	White; 76-year-old; high distress
Availability of Support
The main thing is […] make sure they have Counselors […] or people that we can talk to because that’s, that’s one good thing to get it out, you know.	Black,; 55-year-old; high distress

Overall, participants had a positive perception of the NCCN DT & PL stating it was useful and “a good way to find out what is going on with patients,” however both Black and White participants agreed that greater clarity and more direct offers of support would improve the use of the NCCN DT & PL. This was true even among participants who would not have changed their score given more knowledge of the use of and cut off score for the NCCN DT & PL. Some participants suggested incorporating offers of support into the thermometer itself, for instance adding checkboxes to the problem list such as wanting to speak with a psychologist or social worker. A subset of participants cautioned that more direct offers of support would need to be made carefully to avoid alienating people who “aren’t willing to admit that they need help.” Finally, a few participants emphasized that if direct offers of support were made, it would be important to have at least a subset of those resources immediately available on site.

Discussion

This study was designed to qualitatively understand patient perceptions of the NCCN DT & PL and identify opportunities to improve distress screening in endometrial cancer and gynecologic cancers more broadly and reduce disparities in referrals.[19] We found that the NCCN DT & PL was generally understandable, that there were differences in expression of distressing emotions by White and Black participants, and that participants’ relationships with their clinician were impactful to their communication on the NCCN DT & PL and beyond. Additionally, we found that there was confusion among both Black and White participants about the way the NCCN DT & PL was used in practice and room for greater clarity in the offer of support services.

Participants appreciated the mission of the NCCN & DT to help provide comprehensive care and generally found it easy to use. However, while the word distress was explicitly chosen for the NCCN DT & PL because it “sounds ‘normal’” and is “less stigmatizing” than other terms, we found that for participants in our sample, the term could still feel alienating.[13] Participants repeatedly mentioned feeling that distress was “drastic” versus their more routine conception of their own stressors. This meant that some participants with significant stressors such as comorbidities, caregiving responsibilities, or looming treatment decisions did not consider these in reporting distress on the NCCN DT. Therefore, while patients may not identify with the word distress, they may still have significant problem list stressors that could benefit from supportive services.

There were differences between Black and White patients in our sample in the perception of the NCCN DT & PL. White participants expressed negative emotions such as worry, fear, and nervousness more often. This was consistent with our quantitative work in which the only significant difference in number of issues checked on the problem list between Black and White participants was in the domain of “Emotional Problems.”[19] This difference was also evident in the way that White participants emphasized emotions versus physical symptoms in describing how they selected a distress level on the thermometer. Additionally, while many participants spoke of determination to get through their diagnosis and the challenges of treatment, there was a stronger emphasis on maintaining positivity through adversity among Black participants in our sample. These findings are consistent with the body of existing scholarly work characterizing the “strong Black woman,” a societal paradigm birthed from the intersectional experience of oppressive racism and sexism, of a Black woman who maintains control and does not show weakness during times of adversity.[36–39] This “Superwoman” persona includes an “obligation to suppress emotions,” which may partially explain the lower frequency of mention of emotions and emphasis on moving forward and keeping a positive outlook among Black patients in our sample.[36] However, as Beaubeouf-Lafontant cautions, this strong façade can mask true distress and depression and should therefore be assessed with a critical eye toward facilitating open discourse and sharing to achieve optimal health outcomes.[39] As one of our Black participants put it, there’s been a “myth that we’ve been able to stand more pain than anybody else,” but also stated that “by me sitting here talking to you about this stuff that we have discussed, it has lowered something in my heart […] It’s like a lighter burden,” emphasizing that the opportunity to discuss distress was healing. Taking time to clearly introduce the purpose of the NCCN DT & PL, explicitly discuss patient report on the instrument, and encourage open communication of emotion may be helpful in more equitably determining need and desire for support services in the future.

Relationship building between patient and clinician facilitated open communication on the NCCN DT & PL as well as the clinical encounter itself. Nearly all participants spoke of the importance of the clinician-patient relationship, however Black participants placed greater emphasis on the process of building trust to share openly and achieve the best care possible. This may be explained in part by the understanding among some Black participants that being treated differently or poorly by their oncology providers was a real possibility. Worse treatment by healthcare providers has been described by Black breast cancer survivors including lack of receipt of pertinent information from providers and the need for more self-initiative to have questions answered.[40] On the contrary, a positive patient-provider relationship in Black cancer survivors has been associated with significantly better self-reported health and perceived quality of care.[41] Thus, while the NCCN is usually given as a distress screening tool prior to the clinic visit and receives the most emphasis at the initial visit, it may be especially important to revisit distress screening and make repeated, longitudinal, nonjudgmental offers of support as the patient-provider relationship is strengthened.

Overall, there was a mixed level of understanding among our participants of how the NCCN DT & PL was used in practice. Participants generally seemed to favor a direct approach to framing the thermometer and making offers of support services. There is potential for a change in practice to allow patients to directly indicate a desire or need for supportive services instead of screening prior to determine offers. While it is important not to alienate patients who may not be ready to accept support services and to make such offers in a neutral, nonjudgmental manner, there is evidence indicating that clinician referrals are positively correlated with accessing support services in gynecologic cancer patients as well as indicating that beyond just clinician referrals, direct outreach from the referred service itself may also improve uptake.[42,43]

Limitations

This study has several limitations. While we attempted to utilize rigorous qualitative methods due to time limitations, we did not pilot test the interview guide and participants did not check transcripts for accuracy or give feedback on findings. While previous research has shown that distress scores on the NCCN DT are highest at the initial appointment in some populations, in order to conduct this study in a timely manner we recruited patients at various appointments during treatment and early surveillance.[19,44] Patients completed the NCCN DT & PL with an interviewer present on Zoom which could have biased the numbers reported by patients. Additionally, we recruited from one academic gynecologic oncology practice in the Southeast and this population may not be representative of broader geographic regions. Finally, given the demographic make-up of our practice, this study focuses on Black and White patients, however we acknowledge that given the predominantly non-Hispanic White samples used for the development and testing of the NCCN DT & PL future research in other populations of color is warranted.

Conclusions:

While the instructions on the NCCN DT & PL were generally easy to interpret, its purpose was not clear to a significant subset of participants in this study. Participants across the board expressed that more direct offers of support services would be helpful, especially given an understanding that that was the goal of this instrument. However, participants did feel there was value in the form itself for deeper reflection and elicitation of issues that they might not have thought were relevant to their healthcare previously. We found that Black participants emphasized relationship building and were less likely to speak about negative emotions which may contribute to the differences in distress reporting and subsequent disparity in referral to support services we have documented. It therefore may be important to normalize negative emotions as components of distress in the introduction of the NCCN DT & PL and emphasize rapport building around the NCCN DT & PL. While changes to distress screening will require continued evaluation, our work indicates that equity in referral to support services between Black and White patients with endometrial cancer could be improved by treating the NCCN DT & PL as a conversation starter while offering repeated, neutral, nonjudgmental offers of support regardless of patient-reported score on the distress thermometer. Finally, while this paper explores the NCCN DT & PL, we believe that this work motivates critical review of other screening instruments and tools used in clinical practice for differences in patient perceptions and subsequent outcomes from use.

Figure 2.

Histogram of Distress Scores on Interview Day

Highlights.

• Black and White patients with uterine cancer express distress differently.

• The NCCN Distress Thermometer is an understandable and acceptable tool.

• Black patients expressed negative emotions less often than White patients.

• Black patients emphasized trust and relationship building with providers.

• Patients desired direct and repeated offers of supportive services.

Appendix A: Interview Guide

Interview Script

Thank you for agreeing to participate in this research study. We are interested in talking with women who have been recently diagnosed with uterine cancer about how they experience and show distress. Right now we use a survey that can help patients tell the medical team about their concerns or distress. We will ask you some questions about how you use this survey, what you find useful about it, and how we can improve it for other women with uterine cancer.

What do you think of when you see the word distress? What does the word distress mean to you?

What do you think the word distress means to your doctor? Is it different or the same as what it means to you?

You have a paper with you that says National Comprehensive Cancer Network Distress Thermometer. We are going to talk through this survey together. Take a look at the left side of the page that has a cartoon picture of a thermometer. The instructions above the thermometer begin “Instructions: Please circle the number…” Have you found the instructions?

[IF NO] Interviewer can screenshare to clarify which side, may also place sticker on left hand side to help orient patient

Tell me in your own words what the instructions on the left-hand side of the page above the thermometer mean to you?

Now please fill out the thermometer following the instructions we just talked about.

How did you decide what number to put down? What things are you thinking of when you decide a number?

This survey asks your distress in the last 7 days. How do you feel about remembering distress over the past week? Would it be easier to describe your distress if it asked about distress over the last month? The last day? Explain why you prefer one over the other.

Thank you. Now please take a look at the right side of the handout where you see a list of check boxes. There are instructions at the top of this side of the page as well. These instructions begin “Second, please indicate if any…” Do you see these instructions?

[IF NO] Interviewer can screenshare to clarify the side of the handout.

Tell me in your own words what the instructions on right side of this handout mean to you? Does each category name (practical, family, emotional, spiritual, physical) you see there make sense?

What problems on the list are you dealing with right now/have checked off on the list? [Can probe for more detail on issues that patients have indicated]

What, if anything, are we missing on this list of problems?

Look back at the number you wrote in the thermometer on the other side of the page. When you think about the level of distress you put in the thermometer, are there things that contributed to your distress that were not listed in this list of problems?

Are there problems you put down that you did not think about when you were putting down your distress number in the thermometer?

Prompt:

Did filling out the problems on this side of the page make you want to adjust your distress score at all? Why or why not?

Some women might be experiencing difficult things they don’t feel comfortable talking to their doctor about. What are some things women might experience that might be uncomfortable sharing with their doctor or healthcare team? How could we make women feel more comfortable talking about those topics?

At this clinic we use the results of this survey to help us identify patients that may benefit from additional support and/or resources. If you knew this before filling out the form, how would you fill it out differently (if at all)?

Prompt:

We use a score of 4 on the thermometer to tell us which people might be facing situations that impact their cancer care who we can help with additional support. For example, if someone put a 4 or higher on the thermometer and indicated transportation to and from clinic was an issue, we would try to help them with rides to clinic so that they would not miss clinic appointments. If you knew this before filling out the form, how would you fill it out differently (if at all)?

Is there anything else that you think we should know about this tool and taking care of women with uterine cancer?

Thank you for spending this time with us today to help us better understand how to measure the experience of distress from cancer.

Appendix B: Coding Tree

Node/Sub-node	Description
Communication with Health Care Team
Advocating for self	Comments related to patient as advocate or lack of advocate and/or patient assertiveness to obtain care or information in the clinical encounter OR Explicit deference to physician or other decision makers
Communicating about prognosis and treatment goals	Comments related to patient’s communication with provider about prognosis of disease and goals for treatment.
Context for communicating	Comments related to patient’s background informing healthcare communication style/preferences,
Discussing difficult topics	Comments related to topics that are difficult to broach with healthcare providers. Do not use this code for discussing difficult topics with non-health care providers
Improving Communication	Comments related to how to improve communication with their care provider
Prognosis and Treatment Goals	Comments related to patient’s communication with provider about prognosis of disease and goals for treatment.
Comprehension and Usability
Having adequate time	Comments related to timing of completion of distress tool at appointment
Missing stressors	Comments related to problems missing from problem list or misclassification of a problem on the problem list. Can also include need for clarification or specificity of a problem on the list.
Understanding instructions	Comments related to ease or lack thereof in interpreting the survey and survey directions including terminology around problem list stressors.
Experiences related to or causing distress	Discussion of positive or negative emotions related to health or other life experiences
Caregiving	Comments related to experience caring for others and/or navigating the medical system to care for a family member or close relationship.
Dealing with family	Comments related to how the patient communicates with family and friends including difficult topics. Also includes references to illness and problems in the family that may lead to patient distress without direct caregiving on the part of the patient.
Experiencing emotions	Comments related to mental symptoms and associated distress. Code anxiety, worry, anger depression implied through tone as well as directly stated.
Experiencing pandemic	Comments related to distress or negative emotion related to the COVID-19 pandemic
Experiencing other serious illness	Comments related to experience caring for self or utilizing healthcare for medical problems other than uterine cancer
Experiencing physical symptoms	Comments related to physical symptoms including associated distress. Symptoms could be related to cancer, cancer treatment, or other conditions the patient is experiencing.
Understanding prognosis and treatment	Comments related to patient’s perceived prognosis from disease and goals for treatment. Do not code references to communication with healthcare providers about prognosis and treatment under this code.
Experiencing bias	Comments related to experiences with race and racism with healthcare providers or outside of the healthcare encounter and/or any sequalae.
Potential protective factors
Having faith	Comments related to faith or god in relation to coping with or managing illness/stressors
Having support	Comments related to support or lack thereof derived from family or close relationships.
Navigating health information	Comments related to patient’s familiarity with healthcare and ability to navigate the healthcare system or lack thereof. Do not code patient understanding of prognosis here, code under Understanding prognosis and treatment.
Paying for treatment	Comments related to financial stability or lack thereof and stressors related to finances. May be specifically related to medical cost or the associated costs of cancer treatment such as missing work/lost wages, etc
Having self-efficacy	Comments related to belief or lack thereof in one’s ability to navigate illness, stressors, and/or barriers to care. Must mention action.
Maintaining positivity	Comments related to attitude/outlook and its relation to attitude towards cancer care
Usefulness of DT and PL
Perceiving use of DT in practice	Comments related to how the NCCN DT & PL is used clinically and its impact or lack thereof on clinical care
Changing score	Comments related to changing score whether related to knowing cut off, based on sequencing of filling out problem list or any other comments related to changing score.
Measuring the right timeframe	Comments related to the timeframe of distress measured by the NCCN DT & PL and/or suggested changes to this timeframe.
Interesting	Use this code to note any interesting things that come up while you are coding that may not fit into the existing nodes. Also include annotation to record your thoughts

Data Statement:

De-identified data can be made available upon request with the appropriate data-sharing agreements in place.