Abstract
Objective:
Patient–oncologist therapeutic alliance is a foundation of quality cancer care, although there is limited research demonstrating its relationship with patient outcomes. We investigated the relationship between therapeutic alliance and patient quality of life with a secondary goal of determining whether the association varied by patients’ baseline level of psychological distress.
Methods:
Cross-sectional analysis of baseline data from a randomized clinical trial of 672 patients with advanced cancer participating in a primary palliative care intervention trial. Patients completed baseline self-reported measures of therapeutic alliance (The Human Connection Scale, range: 16–64), overall quality of life (Functional Assessment of Cancer Therapy—Palliative Care, range: 0–184), and psychological distress (Hospital Anxiety and Depression Scale, range: 0–42). First, we determined the relationship between therapeutic alliance and quality of life using multivariable regression adjusting for confounders. We then examined if psychological distress was an effect modifier in this relationship by adding interaction effects of depression and anxiety symptoms on therapeutic alliance into the regression model.
Results:
Patients reported high levels of therapeutic alliance (56.4 ± 7.4) and moderate quality of life (130.3 ± 25.5). Stronger therapeutic alliance was associated with better quality of life after adjusting for other confounding factors (β = 3.7, 95% confidence interval = 2.1, 5.3, p < 0.01). The relationship between therapeutic alliance and quality of life was generally consistent regardless of psychological distress.
Conclusions:
Collaborative, trusting relationships between patients with advanced cancer and their oncologists are associated with better patient quality of life. Future research should investigate the causal, longitudinal nature of these relationships.
Keywords: advanced cancer, affect, cancer, distress, oncology, palliative care, quality of life, therapeutic alliance, psycho-oncology
1 |. BACKGROUND
Quality of life is a highly relevant patient outcome in the advanced cancer setting as patients strive to maximize their well-being in the presence of an incurable illness.1 Quality of life encompasses a holistic view of patients’ physical, social, emotional, and functional health and is directly linked to other patient outcomes, including cancer- and treatment-related symptom severity and disability.2 While quality of life depends on several factors, an important factor is the care provided by oncology clinicians. Clinicians directly assess and manage patient’s quality-of-life concerns, and indirectly support patients in self-managing their quality-of-life needs. In addition, the nature of the relationship between patients and oncology clinicians likely impacts the quality of life.3–5
Therapeutic alliance, defined as the collaborative bond between patients and their healthcare providers, is the cornerstone of quality cancer care.6,7 Within cancer care, patients who believe their oncologist listens to them, responds to their concerns, and is trust-worthy and caring, are thought to experience improved medical care than patients without such a bond.8 Having a strong therapeutic alliance may improve patient outcomes, by first enhancing communication between patients and oncologists, and second improving understanding and shared goals and decision-making about patient needs and priorities.9,10 Ultimately, the goal of therapeutic alliance is to enhance patient-centered care and clinical services that improve patient quality of life.11
Research investigating therapeutic alliance in patients with advanced cancer shows inconsistent results with patient outcomes.12 Understanding this relationship is important because if therapeutic alliance is associated with positive patient outcomes, then oncologists should be trained in the behaviors and attitudes that promote therapeutic alliance. Some studies have validated the positive association between therapeutic alliance and patient psychological symptoms, well-being, coping strategies, and treatment adherence.8,9,13 In contrast, a study by Bar-Sela et al.14 demonstrated that a strong therapeutic alliance with nurses—but not oncologists—was significantly associated with patients’ ability to manage their cancer symptom burden. More alarming, another study found that patients with advanced cancer who reported a strong therapeutic alliance were less likely to express their concerns to their oncologist about treatment and disease status.15
Patients experiencing psychological distress, including depressive and anxiety symptoms, may have difficulty building therapeutic alliance due to higher symptom burden16 and difficulty building rapport with oncologists.17 Without support from their oncologists, patients in distress may lack the necessary motivation and self-efficacy to address their quality-of-life concerns and needs.18,19 Therefore, we aimed to clarify the role of therapeutic alliance as it relates to patient psychological distress and quality of life. If positively associated, targeted attention can be given to supporting the aspects of patient–oncologist therapeutic alliance that improve patient outcomes.
Therefore, our aims are to (1) describe the relationship between patient–oncologist therapeutic alliance and patient quality of life among a cohort of patients with advanced cancer and (2) determine if psychological distress modifies the effect of therapeutic alliance on quality of life. We hypothesized that higher therapeutic alliance is significantly related to higher quality of life and that this association would be weaker for patients with high levels of psychological distress compared to patients with low levels of distress.
2 |. METHODS
This study analyzes baseline data from the Care management by Oncology Nurses to address supportive care needs (CONNECT) cluster randomized trial (NCT02712229). The primary focus of this clinical trial evaluated the effect of a nurse-led primary palliative care intervention on patient and caregiver outcomes. The details of the CONNECT trial design have been published, and no prior paper has addressed this research question.20
Patients were recruited from 17 oncology clinics within the University of Pittsburgh Medical Center Hillman Cancer Center network in Western Pennsylvania. Eligibility criteria included age ≥21 years; metastatic solid tumor; Eastern Cooperative Oncology Group performance status ≤2, indicating that the patient is ambulatory and capable of all self-care; receiving ongoing care from an oncologist participating in the trial; and for whom the oncologist “would not be surprised if the patient died in the next year.”21 Patient exclusion criteria included inability to read and write in English; cognitive impairment or inability to consent to treatment; inability to complete baseline data collection; and hematologic malignancies.
2.1 |. Variables
2.1.1 |. Therapeutic alliance
We assessed patient perceptions of their therapeutic alliance with their primary oncologist using the Human Connection Scale (HCS).9 This scale was originally evaluated amongst a sample of patients with advanced cancer and demonstrated strong internal consistency (Cronbach’s α = 0.90) and concurrent validity with other outcome measures.9 The HCS consists of 16 items with 4-point Likert-type response options assessing patient-perceived levels of therapeutic alliance. For example, items assess patient trust in their doctor, respect for their doctor, and perception of their doctor’s concern with their quality of life. The HCS total score ranges from 16 to 64, with higher scores reflecting stronger patient-oncologist therapeutic alliance. In our sample, the HCS had strong internal consistency (Cronbach’s α = 0.91).
2.1.2 |. Quality of life
We used the Functional Assessment of Chronic Illness Therapy—Palliative Care (FACIT-Pal) to assess patient overall quality of life.22 The 46-item scale includes five domains of quality of life—physical, social, emotional, functional, and palliative care related quality of life that were attained through in-depth interviews with patients with advanced cancer. This measure was validated in a large sample of patients with advanced cancer22 and had high internal consistency in our sample (Cronbach’s α = 0.93). The FACIT-Pal total score ranges from 0 to 184, with higher scores reflecting higher quality of life.
2.1.3 |. Psychological distress
We used the Hospital Anxiety and Depression Scale (HADS) to assess patient psychological distress. Unlike the FACIT-Pal, which assesses general quality of life, the HADS strictly focuses on patient depressive and anxiety symptoms. This scale is frequently used with advanced cancer patient populations.23 Scores for the anxiety and depression subscales range from 0 to 21, with higher scores indicating higher levels of psychological distress. The internal consistency of the depression and anxiety subscales in our sample were Cronbach’s α = 0.78 and α = 0.82, respectively. When indicated in our analytic plan, we used previously developed cut-off scores for patients with cancer on the HADS-depression (≥5) and HADS-anxiety (≥7) subscales to compare patients with high and low levels of psychological distress.24
2.1.4 |. Additional clinical and demographic variables
We accounted for variables that are known to relate to therapeutic alliance and quality of life in our analyses. We considered the following patient self-reported variables as confounders: age, race, ethnicity, time since diagnosis, and current chemotherapy treatment.
2.2 |. Analysis
We describe our sample using descriptive statistics including counts, frequencies, and measures of central tendency. We used Pearson correlations and scatterplots to visually assess the relationships between therapeutic alliance, quality of life, and psychological distress.
We conducted multivariable regression analyses to estimate the relationship between therapeutic alliance and quality of life while adjusting for potential confounding variables. We selected confounding variables a priori that are thought to impact both therapeutic alliance and quality of life: age, race, ethnicity, time since diagnosis, current chemotherapy treatment, and psychological distress.9,25–27 We used linear mixed-effects models with all confounders treated as fixed effects. We rescaled the HCS by a factor of 10 to ensure the interpretability of the regression model results. Therefore, each reported beta coefficient indicates the change in expected value of FACIT-Pal per 10-point increase in the HCS.
We followed the main effects model with a stratified analysis to determine if the relationship between HCS and FACIT-Pal was weaker for patients with higher levels of psychological distress. We included all of the previous confounders in the model, except for the HADS, which was now entered into the model as a potential effect modifier. We repeated the same model for patients above and below the respective thresholds of HADS-depression and HADS-anxiety. Finally, we tested interaction terms between (1) HADS-depression and HCS and (2) HADS-anxiety total scores and HCS in the multivariable regression models to formally test whether depression and anxiety were effect modifiers of the relationship between HCS and FACIT-Pal.
3 |. RESULTS
This manuscript includes baseline data from all 672 participants enrolled in the CONNECT trial (Table 1). In this study, patients had a mean age of 69.3 (SD 10.2) years, were balanced by gender (54% female), and were mainly Caucasian (94%) and non-Hispanic (99%). Patients reported a variety of solid tumor types, the most frequent of which were lung (36%), breast (13%), colon (10%), and pancreatic (10%) cancer. Nearly half (44%) of patients were within a year of their first cancer diagnosis while 20% of patients were diagnosed ≥5 years ago. Nearly half of patients (45.3%) had been receiving care from their oncologist for a year or longer. Most patients (69%) were receiving chemotherapy treatment at baseline.
TABLE 1.
Patient baseline characteristics, therapeutic alliance (HCS), quality of life (FACIT-Pal), psychological distress (HADS) (N = 672)
| Patient characteristics | n (%) | |
|---|---|---|
|
| ||
| Age, years (mean ± standard deviation) | 69.3 ± 10.2 | |
|
| ||
| Sex | ||
| Male | 312 (46.4) | |
| Female | 360 (53.6) | |
|
| ||
| Race | ||
| Caucasian/White | 632 (94.0) | |
| African American/Black | 33 (4.9) | |
| Asian | 5 (0.7) | |
| Other | 2 (0.3) | |
|
| ||
| Ethnicity | ||
| Latino | 9 (1.3) | |
|
| ||
| Education | ||
| High school degree or less | 335 (49.9) | |
| Some college or 2-year degree | 201 (29.9) | |
| 4-year degree | 88 (13.1) | |
| Master’s degree, professional school, or doctoral degree | 41 (6.1) | |
| Declined to answer | 6 (0.9) | |
|
| ||
| Cancer type | ||
| Bladder | 15 (2.2) | |
| Brain | 3 (0.4) | |
| Breast | 85 (12.6) | |
| Colon | 69 (10.3) | |
| Endometrial | 6 (0.9) | |
| Esophageal | 34 (5.1) | |
| Gallbladder | 2 (0.3) | |
| Gastric | 17 (2.5) | |
| Head and neck | 13 (1.9) | |
| Kidney | 27 (4.0) | |
| Liver | 8 (1.2) | |
| Lung | 243 (36.2) | |
| Melanoma | 9 (1.3) | |
| Ovarian | 22 (3.3) | |
| Pancreatic | 69 (10.3) | |
| Prostate | 29 (4.3) | |
| Rectal | 11 (1.6) | |
| Sarcoma | 6 (0.9) | |
| Urethral | 2 (0.3) | |
| Other | 2 (0.3) | |
|
| ||
| Time since diagnosis | ||
| <1 month | 23 (3.4) | |
| ≥1 month but <6 months | 174 (25.9) | |
| ≥6 months but <1 year | 96 (14.3) | |
| ≥1 year but <2 years | 109 (16.2) | |
| ≥2 years but <5 years | 131 (19.5) | |
| ≥5 years | 136 (20.2) | |
| Declined to answer | 1 (0.1) | |
|
| ||
| How long have you been receiving care from your current oncologist? | ||
| Less than 1 month ago | 42 (6.3) | |
| 1–6 months ago | 208 (31.0) | |
| 6 months to 1 year ago | 114 (17.0) | |
| 1–2 years ago | 118 (17.6) | |
| 2–5 years ago | 119 (17.7) | |
| >5 years ago | 67 (10.0) | |
| Declined to answer | 3 (0.4) | |
|
| ||
| Receiving chemotherapy at study enrollment | 463 (68.9) | |
|
| ||
| Patient-reported outcomesa | ||
| Mean ± SD | Median (range) | |
|
| ||
| Therapeutic alliance (HCS) | ||
| Total score (16–64) | 56.4 ± 7.4 | 58 (19–64) |
|
| ||
| Quality of life (FACIT-Pal) | ||
| Total score (0–184) | 130.3 ± 25.5 | 131 (41–184) |
|
| ||
| Psychological distress (HADS) | ||
| Depression (0–21) | 5.4 ± 3.8 | 5 (0–19) |
|
| ||
| Anxiety (0–21) | 5.8 ± 3.9 | 5 (0–20) |
Abbreviations: FACIT-Pal, Functional Assessment of Chronic Illness Therapy—Palliative Care; HADS, Hospital Anxiety and Depression Scale; HCS, Human Connection Scale.
Each measure is listed along with its possible range of scores.
Patients rated high levels of therapeutic alliance (HCS mean total score 56.4 ± 7.4) and moderate levels of quality of life (FACIT-Pal mean total score: 130.3 ± 25.5) (Table 1). Therapeutic alliance was significantly associated with quality of life (Pearson R = 0.30, p < 0.001) indicating that patients who reported higher levels of therapeutic alliance tended to report higher overall quality of life (Figure 1).
FIGURE 1.
Relationship between therapeutic alliance (HCS) and quality of life (FACIT-Pal) (N = 672). FACIT-Pal, Functional Assessment of Chronic Illness Therapy—Palliative Care; HCS, Human Connection Scale
Table 2 reports the results of our multivariable regression analyses. In the adjusted model, therapeutic alliance remained significantly associated with quality of life (β = 3.7, 95% confidence interval [CI] = 2.1, 5.3, p < 0.01), meaning that a 10-point increase on the HCS was associated with a 3.7-point increase in the FACIT-Pal total score.
TABLE 2.
Adjusted relationships between therapeutic alliance (HCS) and quality of life (FACIT-Pal), overall and stratified by degree of psychological distress (HADS-Depression and HADS-Anxiety)
| Adjusted |
||
|---|---|---|
| B (95% CI) | p Value | |
| Entire cohort (n = 672)a | 3.69 (2.11, 5.27) | <0.01 |
|
| ||
| Stratified (Depression)b | ||
| HADS-D ≥ 5 (n = 369) | 8.40 (5.53, 11.27) | <0.01 |
| HADS-D < 5 (n = 303) | 6.35 (2.68, 10.02) | <0.01 |
|
| ||
| Stratified (Anxiety)b | ||
| HADS-A ≥ 7 (n = 263) | 6.99 (4.09, 9.90) | <0.01 |
| HADS-A < 7 (n = 409) | 6.77 (3.94, 9.60) | <0.01 |
Note: Beta coefficients scaled such that each represents the expected change in FACIT-Pal for an additional 10 points on the Human Connection Scale.Abbreviations: CI, confidence interval; FACIT-Pal, Functional Assessment of Chronic Illness Therapy—Palliative Care; HADS, Hospital Anxiety and Depression Scale.
Including fixed covariates for age, race, ethnicity, HADS-Depression, HADS-Anxiety, time since diagnosis, and current chemotherapy treatment.
Including fixed covariates for age, race, ethnicity, time since diagnosis, and current chemotherapy treatment.
The stratified analysis demonstrated that the relationship between therapeutic alliance and quality of life was generally consistent regardless of psychological distress. There was a positive association between HCS and FACIT-Pal for patients with HADS-depression ≥5 (β = 8.6, 95% CI = 5.8, 11.4, p < .01) and for patients with HADS-depression <5 (β = 5.9, 95% CI = 2.2, 9.6, p < 0.01). Similarly, there was a positive association between HCS and FACIT-Pal for patients with HADS-anxiety ≥7 (β = 7.0, 95% CI = 4.1, 9.9, p < 0.01) and <7 (β = 6.4, 95% CI = 3.6, 9.3, p < 0.01). The magnitude of the effect of HCS on quality of life was slightly greater for patients with higher levels of distress in both models. However, the interaction terms of HADS-depression and HCS and HADS-anxiety and HCS were nonsignificant (p = 0.36 and p = 0.36, respectively), providing little evidence that the relationship between therapeutic alliance and quality of life is modified by psychological distress. Of note, the beta coefficients in the stratified analyses are larger than the beta coefficient in the overall analysis, likely because the HADS subscales were removed as confounders.
Figure 2 illustrates the relationship between HCS and FACIT-Pal stratified by HADS-depression and HADS-anxiety. The slope of regression lines for patients above and below the respective depression and anxiety thresholds are similar.
FIGURE 2.
Relationship between therapeutic alliance (HCS) and quality of life (FACIT-Pal) Stratified by (A) Baseline HADS-Depression and (B) HADS-Anxiety. FACIT-Pal, Functional Assessment of Chronic Illness Therapy—Palliative Care; HADS, Hospital Anxiety and Depression Scale
4 |. DISCUSSION
Our results demonstrate that stronger patient–oncologist therapeutic alliance is associated with moderately better quality of life among patients with advanced cancer. This finding supports our hypothesis that when patients perceive that their oncologist understands their priorities and cooperates with them in managing their care, patients experience positive health outcomes including better quality of life. The association is consistent across levels of depression and anxiety symptoms indicating that patients experiencing psychological distress also have a strong relationship between therapeutic alliance with their oncologist and better quality of life. The results suggest that a large change in therapeutic alliance is needed to improve quality of life, though a lack of published data regarding minimally important differences for either variable make the clinical significance of this association difficult to determine.28 This result provides support to the report by Mack et al.9 that therapeutic alliance is positively associated with several aspects of quality of life in patients with advanced cancer.
This study highlights the importance of therapeutic alliance in the advanced care setting. Patients in this study reported similar levels of therapeutic alliance compared to other studies in advanced cancer populations.9,15 Efforts to enhance therapeutic alliance should target both patients and oncologists as both groups contribute to the overall bond. Recent studies that tested combined patient and oncologist interventions to improve communication and shared decision-making among cancer patients can assist researchers in developing therapeutic alliance interventions.29,30 As oncologists engage in communication skills training, they will gain skills to support patients in improving patient outcomes.31,32 As patients actively participate in their care, oncologists will likely engage in more relationship-building efforts to support their patients’ needs including their quality of life concerns.33 Therapeutic alliance interventions should focus on building trust, recognizing the patient holistically, and encouraging open discussion of patient concerns. Once established, this may improve subsequent patient outcomes including quality of life8 and end-of-life care.9
Contrary to our hypothesis that psychological distress would weaken the relationship between therapeutic alliance and quality of life, patients with higher levels of depressive and anxiety symptoms had a similar, if not stronger, relationship than patients with lower levels. Although patients with higher psychological distress reported lower therapeutic alliance overall, this finding suggests that patients experiencing distress benefit from perceiving their relationship with their oncologist as trusting and collaborative and that this is associated with better quality of life. This may occur because patients experiencing depressive and anxiety symptoms, when they are able to build therapeutic alliance with their oncologist, have considerable opportunity to improve their quality of life that further reinforces their strong, collaborative relationship with their oncologist.34,35 Clinical interventions to support distressed patients connecting with caring, responsive, reliable oncologists may mitigate the poor outcomes among patients with high distress.19,36
There are several potential mechanisms linking strong therapeutic alliance with better quality of life. We proposed that high levels of patient–oncologist therapeutic alliance lead to higher quality of life through means of communication, collaboration, and shared goals and understanding. Patients with a strong therapeutic alliance will (a) work with their oncologists to discuss their concerns, (b) participate as an active member in decisions and options, and (c) develop a shared understanding with the oncologist about priorities for treatment and well-being. Through each of these actions, the patient and oncologist co-create pathways by which they can discuss and manage the patients’ quality-of-life concerns. Patients who report high therapeutic alliance may feel comfortable discussing their quality-of-life goals with their oncologist, who in turn incorporates these concerns into the patients’ clinical care.37 Oncologist behaviors likely contribute to patients’ perceptions of therapeutic alliance and the relationship between therapeutic alliance and quality of life. Oncologists who proactively assess and manage patients’ quality of life likely also engage in behaviors that build therapeutic alliance (e.g., building a holistic understanding of the patient, clarifying patients’ goals, and eliciting patients’ needs).38 Oncologists and patients may exert a mutual influence over each other in which oncologists actively build a therapeutic alliance with patients who are more likely to experience high quality of life.39 Understanding the key oncologist behaviors that support therapeutic alliance and are associated with high quality of life will be particularly helpful in identifying targets for oncologist communication- and skills-training.
4.1 |. Study limitations
This analysis has several limitations. First, given the cross-sectional nature of the data, we were unable to determine the directionality of the associations between therapeutic alliance and quality of life. It is conceivable that patients experiencing high quality of life may attribute this to their oncologist’s care, creating a sense of trust and comfort with their oncologist or vice versa. Despite this potential relationship, it seems more plausible that the patient-oncologist relationship, characterized as a dynamic, ongoing collaboration, would produce ways to improve patient quality of life rather than patient quality of life positively or negatively impacting the relationship. Longitudinal research is needed to (a) determine how the relationship between these constructs evolves over time, including changes in patients’ disease status which likely impact quality of life, and (b) test the hypothesized mechanisms connecting therapeutic alliance to quality of life. Second, there may be alternative explanations clarifying the positive association between therapeutic alliance and quality of life that relate to unmeasured confounders that jointly impact both variables (endogeneity). This is a common limitation of cross-sectional data and can be addressed in longitudinal research capable of testing causality and mechanisms. Third, our patient population was quite homogeneous and lacked racial/ethnic diversity, which may limit the generalizability of our findings. Additional work is needed to assess therapeutic alliance in more diverse patient populations. Fourth, our data focused on patient perceptions of their therapeutic alliance but lacked clinician factors that likely impact therapeutic alliance, including age, gender- and racial-concordance with patients, and communication style.8,40
4.2 |. Clinical implications
Patients with a strong therapeutic alliance reported better quality of life across varying levels of psychological distress. Oncologists should cultivate a therapeutic alliance with their patients, recognizing that this bond can support the patients’ well-being.
This study underscores the possible benefits of building a caring, trusting relationship between patients with advanced cancer and their oncologists. Future research should consider the longitudinal relationships between these variables to understand how therapeutic alliance, quality of life, psychological distress, and other patient outcomes interact and evolve over time.
ACKNOWLEDGMENTS
The following funding sources supported this study:(Schenker) NCI R01CA197103; (Schenker) Palliative Research Center (PaRC) at the University of Pittsburgh; (UPMC Hillman Cancer Center) P30CA047904; (Thomas) American Cancer Society Mentored Research Scholar Grant MSRG-18-051-51; and (Thomas) National Palliative Care Research Center Career Development Award.
Footnotes
CONFLICT OF INTERESTS
The authors declare that there are no conflict of interests.
ETHICS STATEMENT
All study procedures involving human participants were performed in accordance with the ethical standards of the University of Pittsburgh and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This study received ethical approval from the University of Pittsburgh Institutional Review Board (STUDY19090204). The trial is registered at clinicaltrials.gov (NCT02712229). Informed consent was obtained from all individual participants included in the study.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- 1.DeMartini J, Fenton JJ, Epstein R, et al. Patients’ hopes for advanced cancer treatment. J Pain Symptom Manag. 2019;57(1):57–63. 10.1016/j.jpainsymman.2018.09.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Park SA, Chung SH, Lee Y Factors influencing the quality of life of patients with advanced cancer. Appl Nurs Res. 2017;33:108–112. 10.1016/j.apnr.2016.10.002. [DOI] [PubMed] [Google Scholar]
- 3.Samuel CA, Mbah O, Schaal J, et al. The role of patient-physician relationship on health-related quality of life and pain in cancer patients. Support Care Cancer. 2020;28(6):2615–2626. 10.1007/s00520-019-05070-y. [DOI] [PubMed] [Google Scholar]
- 4.Farin E, Nagl M The patient-physician relationship in patients with breast cancer: influence on changes in quality of life after rehabilitation. Qual Life Res. 2013;22(2):283–294. 10.1007/S11136-012-0151-5. [DOI] [PubMed] [Google Scholar]
- 5.Ernstmann N, Wirtz M, Nitzsche A, et al. Patients’ trust in physician, patient enablement, and health-related quality of life during colon cancer treatment. J Cancer Educ. 2017;32(3):571–579. 10.1007/s13187-017-1166-y. [DOI] [PubMed] [Google Scholar]
- 6.Epstein RM, Street RL Jr., Patient-Centered Communication in Cancer Care: Promoting Healing and Reducing Suffering. Bethesda, MD: National Cancer Institute; 2007. https://cancercontrol.cancer.gov/brp/docs/pcc_monograph.pdf. Accessed August 6, 2020. [Google Scholar]
- 7.Rogers AI The cornerstone of medicine: the physician-patient relationship. Am J Gastroenterol. 2007;102(8):1594–1595. 10.1111/j.1572-0241.2007.01160.x. [DOI] [PubMed] [Google Scholar]
- 8.Hillen MA, De Haes HCJM, Smets EMA. Cancer patients’ trust in their physician–a review. Psychooncology. 2011;20(3):227–241. 10.1002/pon.1745. [DOI] [PubMed] [Google Scholar]
- 9.Mack JW, Block SD, Nilsson M, et al. Measuring therapeutic alliance between oncologists and patients with advanced cancer. Cancer. 2009;115(14):3302–3311. 10.1002/cncr.24360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Trice ED, Prigerson HG Communication in end-stage cancer: review of the literature and future research. J Health Commun. 2009;14:95–108. 10.1080/10810730902806786. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Hoerger M, Epstein RM, Winters PC, et al. Values and options in cancer care (VOICE): study design and rationale for a patient-centered communication and decision-making intervention for physicians, patients with advanced cancer, and their caregivers. BMC Cancer. 2013;13:188. 10.1186/1471-2407-13-188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Lelorain S, Brédart A, Dolbeault S, Sultan S A systematic review of the associations between empathy measures and patient outcomes in cancer care. Psychooncology. 2012;21(12):1255–1264. 10.1002/pon.2115. [DOI] [PubMed] [Google Scholar]
- 13.Ma Y, Xu W, Liang Z, et al. Patient-oncologist alliance and psychosocial well-being in Chinese society strongly affect cancer management adherence with cancer of unknown primary. Psychooncology. 2017;26(7):991–998. 10.1002/pon.4245. [DOI] [PubMed] [Google Scholar]
- 14.Bar-Sela G, Yochpaz S, Gruber R, Lulav-Grinwald D, Mitnik I, Koren D The association between the working alliance and sharing concerns by advanced cancer patients. J Clin Oncol. 2015;33(15_suppl):e20553. 10.1200/jco.2015.33.15_suppl.e20553. [DOI] [PubMed] [Google Scholar]
- 15.Freytag J, Street RL, Xing G, et al. The ecology of patient and caregiver participation in consultations involving advanced cancer. Psychooncology. 2018;27(6):1642–1649. 10.1002/pon.4710. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Grotmol KS, Lie HC, Loge JH, et al. Patients with advanced cancer and depression report a significantly higher symptom burden than non-depressed patients. Palliat Support Care. 2019;17(2):143–149. 10.1017/S1478951517001183. [DOI] [PubMed] [Google Scholar]
- 17.Hay CM, Courtney-Brooks M, Lefkowits C, Hagan TL, Edwards RP, Donovan HS Symptom management in women with recurrent ovarian cancer: do patients and clinicians agree on what symptoms are most important? Gynecol Oncol. 2016;143(2):367–370. 10.1016/j.ygyno.2016.08.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.White LL, Cohen MZ, Berger AM, Kupzyk KA, Bierman PJ Self-efficacy for management of symptoms and symptom distress in adults with cancer: an integrative review. Oncol Nurs Forum. 2019;46(1):113–128. 10.1188/19.ONF.113-128. [DOI] [PubMed] [Google Scholar]
- 19.Bisseling E, Cillessen L, Spinhoven P, et al. Development of the therapeutic alliance and its association with internet-based mindfulness-based cognitive therapy for distressed cancer patients: secondary analysis of a multicenter randomized controlled trial. J Med Internet Res. 2019;21(10):e14065. 10.2196/14065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Becker CL, Arnold RM, Park SY, et al. A cluster randomized trial of a primary palliative care intervention (CONNECT) for patients with advanced cancer: protocol and key design considerations. Contemp Clin Trials. 2017;54:98–104. 10.1016/jxct.2017.01.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Moss AH, Lunney JR, Culp S, et al. Prognostic significance of the “surprise” question in cancer patients. J Palliat Med. 2010;13(7):837–840. 10.1089/jpm.2010.0018. [DOI] [PubMed] [Google Scholar]
- 22.Lyons KD, Bakitas M, Hegel MT, Hanscom B, Hull J, Ahles TA Reliability and validity of the Functional Assessment of Chronic Illness Therapy-Palliative care (FACIT-Pal) scale. J Pain Symptom Manage. 2009;37(1):23–32. 10.1016/j.jpainsymman.2007.12.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Zigmond AS, Snaith RP The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67(6):361–370. 10.1111/j.1600-0447.1983.tb09716.x. [DOI] [PubMed] [Google Scholar]
- 24.Singer S, Kuhnt S, Götze H, et al. Hospital anxiety and depression scale cutoff scores for cancer patients in acute care. Br J Cancer. 2009;100(6):908–912. 10.1038/sj.bjc.6604952. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Gonzales FA, Sangaramoorthy M, Dwyer LA, et al. Patient-clinician interactions and disparities in breast cancer care: the equality in breast cancer care study. J Cancer Surviv. 2019;13(6):968–980. 10.1007/s11764-019-00820-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Maly RC, Frank JC, Marshall GN, DiMatteo MR, Reuben DB Perceived efficacy in patient-physician interactions (PEPPI): validation of an instrument in older persons. J Am Geriatr Soc. 1998;46(7):889–894. [DOI] [PubMed] [Google Scholar]
- 27.Fuertes JN, Mislowack A, Bennett J, et al. The physician-patient working alliance. Patient Educ Counsel. 2007;66(1):29–36. 10.1016/j.pec.2006.09.013. [DOI] [PubMed] [Google Scholar]
- 28.Ringash J, O’Sullivan B, Bezjak A, Redelmeier DA Interpreting clinically significant changes in patient-reported outcomes. Cancer. 2007;110(1):196–202. 10.1002/cncr.22799. [DOI] [PubMed] [Google Scholar]
- 29.Epstein RM, Duberstein PR, Fenton JJ, et al. Effect of a patient-centered communication intervention on oncologist-patient communication, quality of life, and health care utilization in advanced cancer the VOICE randomized clinical trial. JAMA Oncol. 2015;1(5):92–100. 10.1001/jamaoncol.2016.4373. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Henselmans I, Laarhoven HWM, Maarschalkerweerd P, et al. Effect of a skills training for oncologists and a patient communication aid on shared decision making about palliative systemic treatment: a randomized clinical trial. Oncologist. 2020;25(3):e578. 10.1634/theoncologist.2019-0453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Moore PM, Rivera S, Bravo-Soto GA, Olivares C, Lawrie TA Communication skills training for healthcare professionals working with people who have cancer. Cochrane Database Syst Rev. 2018;2018(7):CD003751. 10.1002/14651858.CD003751.pub4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.De Vries AMM, de Roten Y, Meystre C, Passchier J, Despland J-N, Stiefel F Clinician characteristics, communication, and patient outcome in oncology: a systematic review. Psychooncology. 2014;23(4):375–381. 10.1002/pon.3445. [DOI] [PubMed] [Google Scholar]
- 33.Street RL, Krupat E, Bell RA, Kravitz RL, Haidet P Beliefs about control in the physician-patient relationship: effect on communication in medical encounters. J Gen Intern Med. 2003;18(8):609–616. 10.1046/j.1525-1497.2003.20749.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Demark-Wahnefried W, Aziz NM, Rowland JH, Pinto BM Riding the crest of the teachable moment: promoting long-term health after the diagnosis of cancer. J Clin Oncol. 2005;23(24):5814–5830. 10.1200/JCO.2005.01.230. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Bernacki R, Paladino J, Neville BA, et al. Effect of the serious illness care program in outpatient oncology: a cluster randomized clinical trial. JAMA Intern Med. 2019;179(6):751–759. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Applebaum AJ, Duhamel KN, Winkel G, et al. Therapeutic alliance in telephone-administered cognitive-behavioral therapy for hematopoietic stem cell transplant survivors. J Consult Clin Psychol. 2012;80(5):811–816. 10.1037/a0027956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Bar-Sela G, Yochpaz S, Gruber R, Lulav-Grinwald D, Mitnik I, Koren D The association between the strength of the working alliance and sharing concerns by advanced cancer patients: a pilot study. Support Care Cancer. 2016;24(1):319–325. 10.1007/s00520-015-2794-6. [DOI] [PubMed] [Google Scholar]
- 38.Back AL, Arnold RM, Baile WF, Tulsky JA, Fryer-Edwards K Approaching difficult communication tasks in oncology. CA Cancer J Clin. 2005;55(3):164–177. 10.3322/canjclin.55.3.164. [DOI] [PubMed] [Google Scholar]
- 39.Street RL, Gordon H, Haidet P Physicians’ communication and perceptions of patients: is it how they look, how they talk, or is it just the doctor? Soc Sci Med. 2007;65(3):586–598. 10.1016/j.socscimed.2007.03.036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Pollak KI, Arnold RM, Jeffreys A, et al. Oncologist communication about emotion during visits with patients with advanced cancer. Artic J Clin Oncol. 2008;25:5748–5752. 10.1200/JCO.2007.12.4180. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.