Abstract
Abstract
Background:
Improving quality of life (QOL) is important in cancer palliative care (PC) patients. “Spiritual pain” (SP) is common in this population, but it is unknown how it affects QOL.
Objective:
To study the associations between SP and QOL in cancer patients in PC.
Design:
Cross-sectional.
Settings/Subjects:
Cancer patients assessed at a PC clinic in Puente Alto, Chile, were enrolled in a longitudinal study to characterize patients' end of life. Inclusion criteria included age ≥18, a primary caregiver, not having delirium, and a Karnofsky performance status (KPS) ≤80.
Measurements:
After consenting patients completed baseline surveys that included demographics, single-item questions to assess SP (0–10), financial distress, spirituality-related variables and questionnaires to assess QOL (0–100), and physical (Global distress score—physical) and psychological distress (Hospital Anxiety and Depression Scale), baseline data analyses to explore associations between SP and QOL were adjusted for potential confounders.
Results:
Two hundred and eight patients were enrolled: mean age was 64, 50% were female, and 67% had SP. In univariate analysis, SP was significantly associated with lower QOL (coefficient [95% confidence interval]: −1.88 [−2.93 to −0.84], p < 0.001). Lower QOL was also associated with being younger, lower KPS, higher physical distress, having anxiety or depression, and decreased religiosity and religious coping. In the multivariate analysis, QOL remained independently associated with SP (−1.25 [−2.35; to −0.15], p < 0.026), religious coping (11.74 [1.09 to 22.38], p < 0.031), and physical distress (−0.52 [−0.89 to −0.16], p < 0.005).
Conclusions:
SP is associated with QOL in cancer patients in PC. SP should be regularly assessed to plan for interventions that could impact QOL. More research is needed.
Background
Improving quality of life (QOL) is a key goal of palliative care (PC) in patients with advanced cancer. According to the World Health Organization (WHO), PC aims to improve the QOL in patients with life-threatening illness through the assessment and treatment of physical, psychological, and spiritual problems. 1 During the last decades, several reports have shown that most of these problems impact QOL in patients with advanced cancer. For example, physical symptoms,2,3 psychological symptoms,4–6 and financial distress7,8 have been associated with worse QOL in this group of patients.
It is recognized that patients with advanced cancer experience spiritual needs 9 and/or spiritual distress.10,11 It is also known that religious coping and spiritual support availability by religious communities or medical systems are associated with better QOL in cancer patients.12–14 Although these relationships are of interest, it would be important to know whether the presence of spiritual distress directly affects overall QOL to better support the relevance of identifying spiritual distress in the clinical practice and promote interventions in this domain that could contribute to improve the QOL of this population.
Evaluation and identification of spiritual problems, such as spiritual distress, have been recommended as part of integrated PC in patients with advanced cancer. 15 “Spiritual pain” (SP) has been defined in the literature as a “pain deep in your soul/being that is not physical.”10,16 SP has been reported with frequencies between 44% and 61% in outpatient cancer patients and has been associated with physical symptoms, psychological distress, financial distress, and spiritual/religious aspects of QOL in this population.10,11,16
However, it is not known whether the presence and intensity of SP influences overall QOL in this group of patients or not. It is also unknown whether spirituality-related factors, such as self-reported religiosity, self-reported spirituality, or importance of religious coping, affect the relationship between SP and overall QOL. Exploring these associations will help us better understand the relationship between spiritual distress and overall QOL and suggest possible mechanisms that could explain this relationship.
The goals of this exploratory study were as follows: (1) to characterize the association between SP and QOL in a group of patients with advanced cancer assessed at an outpatient PC clinic and (2) to assess whether demographic variables and/or other known factors that impact patient QOL affect the relationship between SP and QOL in this group of patients.
Methods
The data to perform this cross-sectional study were obtained from a database that included baseline characteristics of advanced cancer patients who were enrolled in a prospective study that aimed to characterize QOL during end of life in this population. 17 Briefly, advanced cancer patients followed up at a single outpatient PC clinic in Puente Alto, Chile, who were enrolled in this study, were followed up every two weeks between initial assessment and death. Inclusion criteria included being >18 years old, not being diagnosed with delirium, and a Karnosfky performance status (KPS) ≤80, to detect patients with a short survival prognosis, but who were able to have at least two follow-up assessments. After consenting, patients completed a baseline questionnaire, including the EORTC-QLQ-C15 survey to assess QOL.
Data collection
A trained nurse collected baseline patient characteristics, including age, sex, religion, educational level, cancer diagnosis, KPS, alcoholism questionnaire, presence of delirium, physical and psychological distress, and a measure of spiritual distress during the first study interview.11,18,19 The CAGE instrument consists of four questions (cut down, annoyed, guilt, and eye opener) to explore attitudes regarding alcohol consumption, with ≥2 positive responses suggesting alcoholism. 18 The Memorial Delirium Assessment Scale (MDAS) is a previously validated 10-item instrument to assess delirium (0–30) with >13 points suggesting a positive diagnosis. 19 The Edmonton Symptom Assessment System (ESAS) is an instrument, previously validated in Spanish, to assess the mean intensity of 10 common symptoms during the last 24 hours using a numeric rating scale ranging (0–10)20,21 Total physical distress can be estimated with the ESAS using the Global Distress Score—Physical, which represents the sum of ESAS pain, fatigue, nausea, drowsiness, dyspnea, and loss of appetite (0–60). 22 Higher scores indicate higher physical distress.
To assess SP, we used the ESAS-FS, a modified and validated ESAS, which includes two extra questions, one question to assess financial distress and one question to assess SP (“SP is a pain deep in your soul or your being that is not physical; please rate the intensity of your SP in a 0 to 10 scale with 0 having no SP and 10 having the worst SP). 11 We further categorized SP into mild (scores 1–3), moderate (scores 4–6), and severe (scores 7–10). Although several tools and instruments have been used to identify spiritual distress in patients with advanced cancer, very few have been validated and used in Spanish-speaking populations. 23 We decided to assess spiritual distress with the ESAS-FS, because it is a single-item instrument that adds little burden to participants, has been previously used in Spanish-speaking populations, and has been associated with other spirituality-related outcomes in our population, such as decreased meaning in life and increased optimism. 24
To assess psychological symptoms, we used the Hospital Anxiety and Depression Scale (HADS) a 14-item tool that screens for anxiety and depression during the last week, which has been previously validated in Spanish. 25 A score of 8 or higher in either subscale is considered clinically meaningful.
To assess QOL, we used the Spanish version of the EORTC-QLQ-C15-PAL. 26 This is an abbreviated version of the EORTC-QLQ-C30 specially developed for PC, and includes questions that assess symptoms, physical and emotional functioning, and a single-item question to assess global QOL. Both instruments have been validated in Spanish-speaking cancer patients.26,27 We added 6 extra questions from the original 30-item questionnaire to assess role, social, and cognitive functioning. The global QOL item and the responses that assess each of the 5 functioning domains scales are transformed to 0 to 100 scales, with higher scores meaning better QOL or better functioning.
Self reported spirituality and religiosity were assessed by asking the patient “how spiritual do you consider yourself?” and “how religious do you consider yourself?,” respectively. Patient reported their responses with a 4-item Likert scale (nonspiritual/religious, a little bit spiritual/religious, moderately spiritual/religious, or very spiritual/religious). Self-reported religious coping was assessed by asking the patient “how much do your religious beliefs or activities help you to cope with cancer?.” Patient reported their responses using a 5-item Likert scale (“nothing,” “a little bit,” “moderate,” “to a great extent,” and “it is the most important”). These questions have been previously used, but have not been validated in Spanish. 10
Statistical considerations
We summarized our data using standard descriptive statistics. For continuous variables, we reported sample size and mean and standard deviation (SD) for normally distributed variables and median and interquartile range for non-normally distributed variables. For categorical and binary variables, we reported frequency and percentage.
Our main relationship of interest was the association between overall QOL with SP, assessed using Spearman correlation test. To further explore the association between SP and overall QOL and other covariates, including demographic and spirituality-related variables, we performed univariate analysis using linear regression models with SP and QOL as our outcomes. To ease the use of categorical variables in the regression model, we grouped patient responses into binary categories. Self-reported spirituality, religiosity, and religious coping were dichotomized (“nonspiritual/religious” versus “little bit spiritual/religious” versus “moderately spiritual/religious” and “very spiritual/religious”; “nothing” and “a little bit” versus “moderate,” “to a great extent,” and “it is the most important”). Coefficients, with 95% confidence intervals and p-values, were estimated for each covariate.
To explore which variables were independently associated with overall QOL, we created a linear regression model, with QOL as the main outcome, SP as a covariate that was always included, and all covariates that were found to be significantly associated with QOL or with SP in the univariate analysis. To further explore the stability of our model, we performed both stepwise forward and backward selection strategies to identify the variables that could significantly influence the relationship between SP and QOL. SP was always kept in the model. Cuttoffs of 0.05 and 0.1 were used for both strategies to assess the stability of the model. The STATA 13.1 software was used to perform the statistical analyses.
Data protection and confidentiality
The study was approved by the local Ethics Committee (Comité Ético Científico—Facultad de Medicina, Pontificia Universidad Católica de Chile, Protocol Number #13-154). All participants provided signed informed consent. Health information was protected, and data confidentiality was maintained throughout the study. Only trained personnel in maintaining confidentiality and the Primary Investigator had access to study records.
Results
Two hundred and eight advanced cancer patients in PC were enrolled in this prospective study, between February 1, 2016, and January 31, 2017. Mean age was 64, 104 (50%) were female, 131 (63%) had a partner, and most participants were Catholic (124, 60%), with 25 (12%) reporting having no religion or being atheist. Baseline population characteristics are described in Table 1.
Demographics and Baseline Characteristics
ESAS, Edmonton Symptom Assessment System; HADS, Hospital Anxiety and Depression Scale; IQR, interquartile range; MDAS, Memorial Delirium Assessment Scale; QOL, quality of life; SD, standard deviation.
Mean (SD) overall QOL was 65 (29) in a 0 to 100 scale, with better QOL subscales being cognitive and physical QOL and worse QOL subscales included role and social QOL (Table 1). One hundred and forty (67%) patients reported having SP (score ≥1), with 21 (10%) reporting mild SP, 55 (26%) reporting moderate SP, and 64 (31%) reporting severe SP. Spearman correlation between overall QOL with SP was −0.21 (p = 0.002).
One hundred and fifty-one (73%) patients reported that they considered themselves as spiritual (moderately and very spiritual), whereas 144 (69%) patients considered themselves as religious (moderately and very religious). Regarding religious coping, 128 (62%) reported that religion helped them to cope with their disease “to a great extent” or “was the most important thing.” Summary baseline statistics for QOL, and physical, psychological, financial, and spirituality-related variables are described in Table 1. Spearman correlation between patient-reported spirituality and religiosity (four categories each) was 0.44 (p < 0.001), suggesting that there is a moderate association between these two variables. Religious coping was associated with both spirituality (Spearman rho = 0.34, p < 0.001) and religiosity (Spearman rho = 0.44, p < 0.001).
In the univariate analysis of SP with patients' baseline characteristics, we found that SP was associated with being younger and being female. SP was associated with worse overall QOL and with worse scores in each of the QOL subscales. SP was also associated with fatigue, drowsiness, anorexia, dyspnea, depression, anxiety, sleep disturbance, well-being, and overall physical symptom burden. Patients who were depressed and anxious according to the HADS also had higher SP. SP was associated with financial distress, but not with self-reported spirituality, religiosity, or religious coping, considering these variables either as continuous (data not shown) or categorical. Associations between SP and patient characteristics are described in Table 2.
Univariate Analysis between Spiritual Pain and Overall Quality of Life with Patient Baseline Characteristics
Amount of variation in the dependent variable according to one-point increase in the independent variable.
CI, confidence interval.
Bold indicates p < 0.05, statistically significant.
In the univariate analysis of QOL, higher QOL was significantly associated with older age and better performance status. Also, higher QOL was associated with physical symptoms, not having anxiety or depression, and higher self-reported religiosity and religious coping, but not with higher self-reported spirituality. Associations between QOL and patient characteristics are described in Table 2.
In the multivariate analysis, which included all variables that were significantly associated with QOL in the univariate analysis plus gender and financial distress that were associated with SP, the variables that remained independently associated with QOL included SP, religious coping, and physical symptom burden (Table 3). Using both backward and forward strategies and 0.05 and 0.1 cuttoffs, the resulting model included the same three variables, which included SP, physical symptoms, and religious coping (Table 4). Finally, we tested, using likelihood ratio (LR) test, whether the second model was nested under the first, larger model, and it was (LR test chi-square = 3.69, p = 0.595). This test suggests that the more parsimonious model is nested under the larger model.
Multivariate Model Including All Relevant Variables
KPS was considered a continuous variable.
KPS, Karnofsky performance status.
Bold indicates p < 0.05, statistically significant.
Multivariate Model Using Both Stepwise Backward and Forward Selection Strategies for Model Building
The obtained models were the same using both strategies for variable selection and using different cuttoffs (0.05 and 0.1).
Bold indicates p < 0.05, statistically significant.
Discussion
In this study, we report that higher SP is independently associated with lower overall QOL in a group of advanced cancer patients participating at an outpatient PC clinic. Although other articles have explored the associations between spirituality- and QOL-related variables, to our knowledge, this is the first study to demonstrate the direct association between SP and overall QOL in advanced cancer patients in the PC setting. In a previous report by Delgado-Guay et al., the authors found that SP was related to several variables, including spirituality-related QOL measured with the FACIT-Sp-Ex, an instrument that specifically addresses spirituality-related QOL but not overall QOL. 10 Similarly, Schultz et al. recently explored the relationship between spiritual distress, SP, and general distress, domains that did not include QOL. 28 Therefore, this article highlights the relevance of SP in the global patient experience. Besides higher SP, only higher physical symptom burden and positive religious coping remained associated with overall QOL in the multivariate analysis, whereas psychological distress, spirituality, and religiosity were not. Although this study was not powered to study the association between these variables, these findings suggest the relevance of these factors in the QOL in this Latin American population.
In this study, the frequency of SP was higher than in previous studies that included mainly Caucasian subjects (35% to 67%).10,28 The high frequency of SP, self-reported religiosity (69%), spirituality (73%), and moderate-to-high religious coping (80%) reflect the relevance of religion and spirituality in patients with advanced cancer in this region.
One unexpected finding from this study was that SP was particularly high among younger participants. It is important to note that, although Chile has been historically a religious country with a high proportion of Catholics—similar to other countries in Latin America—it has experienced a continuous process of decrease in religious identification during the last decades, which has been particularly marked among young people. 29 This phenomenon could explain the higher rate of SP we observed in younger individuals, although we were unable to better characterize the role of religiosity, spirituality, and religious coping particularly in this population, due to sampling constraints. We also found that SP was associated with higher physical symptom burden, higher depression and anxiety, and higher financial distress, findings that are similar to what Delgado-Guay, et al. previously reported. 11
Together, these results highlight the complexity and multidimensionality of patients' suffering in the context of advanced cancer, and also support the hypothesis that the presence of SP could increase the expression of symptoms, including all physical, psychological, and financial.
Surprisingly, SP was not associated with self-reported spirituality, religiosity, and religious coping in the univariate analysis. These findings suggest that people who do not self-identify as religious or spiritual, or who report using religion to cope with distress, still experience SP. These results should encourage clinicians to explicitly assess SP and spirituality-related variables, regardless of the religious or spiritual background a person reports.
In this study, we found that QOL was associated with SP, psychological distress, religiosity, and religious coping, although only SP and religious coping remained associated with QOL after adjusting to several covariates, including religiosity and psychological distress. These findings suggest that both SP and religious coping could affect QOL in different ways. This aligns well with the findings of Mako et al., as they described SP as a multidimensional concept in which emotional distress results from rupture in the relationship between the individual and the self, others, and/or the transcendent, that is, God or Nature. 16 It is possible to hypothesize that this relational rupture could impact patients' QOL. For example, loneliness or social isolation, a type of rupture between the self and others, has been associated with poor mental and physical health in both the general and cancer patients.30,31 Therefore, loneliness could be one possible mechanism through which SP affects overall QOL. Another possible explanation could be that SP influences patients' well-being through psychological distress, although our data do not support this hypothesis. A third option could be that SP—such as previously described by Delgado-Guay et al.—could increase the expression of symptoms affecting patients' overall experience. 10 Regarding religious coping, several studies have shown its effect on QOL, such as the Coping with Cancer study and studies in cancer patients receiving radiation therapy or patients with breast cancer.12,13,32 Religious coping could be an indicator of patients' personal and institutional spiritual resources to face SP or existential distress.
This study has several limitations. First, the cross-sectional nature of this analysis allows us to only report associations and not causal mechanisms. Second, this was done at a single site, limiting the generalizability of our findings. However, the fact that this study is exploratory in nature allows us to generate hypothesis that can be further tested in the future in larger populations, in this understudied geographical region. Third, we used a single question item to assess religious coping, religiosity, and spirituality, each one with a predefined set of possible answers, which may be insufficient to assess these complex and multidimensional concepts. Future research regarding the role of religion and spirituality in this population should include multiitem instruments that are able to better capture these constructs. Finally, SP could be explained by different mechanisms that were not studied in this report. Qualitative studies should be performed to better capture how patients experience and understand SP and what are the possible meanings associated with this concept.
In conclusion, overall QOL is independently associated with SP, physical symptom burden, and religious coping in a group of Latin American advanced cancer patients in PC. This study highlights the importance of SP and spiritual-related factors in this population due to its association with overall QOL. These findings call for increasing the attention to the development and assessment of interventions in these domains as they could potentially improve patients' QOL regardless of patient's reported spirituality or religiosity.
Footnotes
Acknowledgments
Pedro Perez-Cruz is supported, in part, by funds awarded by the National Commission for Scientific and Technological Research, Chile (FONDECYT INICIO11130533; REDES1440024).
We would like to thank the Millennium Science Initiative of the Ministry of Economy, Development and Tourism, from Chile, grant “Nuclei for the Study of the Life Course and Vulnerability,” for the institutional support.
Authors Disclosure Statement
No competing financial interests exist.
