Association between Spirituality, Religiosity, Spiritual Pain, Symptom Distress, and Quality of Life among Latin American Patients with Advanced Cancer: A Multicenter Study

Abstract

Objectives:

The purpose of this multicenter study was to characterize the association between spirituality, religiosity, spiritual pain, symptom distress, coping, and quality of life (QOL) among Latin American advanced cancer patients.

Methods:

Three hundred twenty-five advanced cancer patients from palliative care clinics in Chile, Guatemala, and the United States completed validated assessments: Faith, Importance and Influence, Community, and Address (FICA) (spirituality/religiosity), Edmonton Symptom Assessment Scale-Financial/Spiritual (ESAS-FS), including spiritual pain, Penn State Worry Questionnaire-Abbreviated (PSWQ-A), Center for Epidemiologic Studies Depression Scale (CES-D), Brief-coping strategies (COPE) and Brief religious coping (RCOPE) and RCOPE, respectively, and Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being, Expanded version (FACIT-Sp-Ex).

Results:

Median age: 58 years (range: 19–85); 60% female; and 62% Catholic and 30% Christian, but not Catholic. Three hundred fifteen patients (97%) considered themselves spiritual and 89% religious, with median intensities of 7 (interquartile range [IQR]: 5–10) and 7 (5–9), respectively (0–10 scale, 10 = “very much”). Median importance of spirituality/religiosity was 10 (IQR: 8–10). The frequency and associations between spirituality/religiosity and various items were as follows: helps to cope with illness (98%; r = 0.66303; p < 0.0001), positive effect on physical symptoms (81%; r = 0.42067; p < 0.0001), and emotional symptoms (84%; r = 0.16577; p < 0.0001). One hundred ninety-five patients (60%) reported that their spiritual/religious needs had not been supported by the medical team. Spiritual pain was reported in 162/311 patients (52%), with median intensity of 6 (IQR: 5–8). Spiritual pain was associated with pain (p = 0.0225), depression (p < 0.0001), anxiety (p < 0.0001), worry (p < 0.001), behavioral disengagement (p = 0.0148), FACIT-Sp-Ex score (p = 0.0002), and negative RCOPE (p < 0.0001).

Significance of Results:

Spirituality and religiosity are frequent, intense, and rarely addressed among Latin American patients. Spirituality/religiosity was associated with positive COPE and higher QOL. Spiritual pain was also frequent and associated with physical and psychosocial distress. These patients need increased spiritual/religious support.

Introduction

Spirituality, religiosity, and spiritual pain may influence symptom distress, quality of life (QOL), and coping strategies (COPE) of patients with advanced and terminal illness.^1–3 Spirituality and religiosity also can be used as integrative therapy to promote general well-being and health.^3–6 There is limited research available to define these concepts in Latin American patients with advanced cancer in the palliative care setting. Identifying the ways in which Latinos cope with the distress of advanced illness will improve our understanding of their experiences and may lead to development of interventions to reduce their distress.

Spirituality and religiosity are common and integral in Latino cultural values.^3,5–8 Spiritual and religious beliefs play a significant role in multiple mind-body alternative therapies and healing therapies regularly used by Latinos.^9–14

Spiritual and religious beliefs among Latinos are distinctly related to events of Spanish-Christian colonization of the native persons of Mexico, Central and South America, and the Caribbean. These important events caused a deep impact on the values and spiritual and cultural perspectives of these populations.^4,8,9

Spiritual and religious experiences among Latinos are rooted in important, durable cultural values. For example, personalismo relates to the empathy, warmth, and closeness of one's relationship with others. This concept explains many Latinos' sense of a close and direct relationship with their Creator (commonly embracing the Christian impressions of God), and/or various saints, or another belief system that may provide meaning or purpose in their life.^4,9,14

Another important cultural value among Latinos is familismo, characterized by faithfulness and a durable pledge to family members.^14–16 Spiritual and/or religious beliefs are often entrenched in one's relationship with religious or nonreligious community members and family.^7–9,16

The primary aim of this study was to determine the frequency and intensity of spirituality and religiosity and their association with physical and psychological symptoms, spiritual pain, COPE, and QOL among Latin American patients receiving palliative care for treatment of advanced cancer at three institutions in the United States, Guatemala, and Chile.

Methods

Study procedures

Our study was approved by the Institutional Review Board of the University of Texas MD Anderson Cancer Center and by the ethics committees of Pontificia Universidad Catolica de Chile and Instituto Nacional de Cancerologia de Guatemala. This study was conducted from March 13, 2013, to March 16, 2015. In the United States, the study was conducted at The University of Texas MD Anderson Cancer Center, and at Lyndon B. Johnson General Hospital in Houston, Texas. The principal investigator, co-investigators, and biostatistician were all faculty members at the institution. The research coordinator from MD Anderson's Department of Palliative, Rehabilitation, and Integrative Medicine enrolled patients from the Supportive Care and Palliative Care Outpatient Clinics into the study, performed assessments, and collected data. The research coordinator from our department was fluent in both English and Spanish.

The Inclusion criteria for patients were (1) Latin American (defined as persons who trace their origin or descent to Mexico, Puerto Rico, Cuba, Central and South America countries, and other Spanish cultures) patients with advanced cancer (recurrent or metastatic illness) seen in palliative care and oncology outpatient clinic; (2) patients 18 years of age or older; (3) Karnofsky performance status score of more than 40 at the time of inclusion into study (patients with Karnofsky score less than 40 may have not been able to complete the measures); and (4) normal cognitive status as determined by the interviewer based on the ability to understand the nature of the study and consent process.

The data manager from this department created the protocol-specific database and entered the data. All data monitoring and analysis were performed at MD Anderson Cancer Center.

In Guatemala city, Guatemala, the study was conducted in the outpatient palliative care clinic at the Instituto Nacional de Cancerología (INCAN), the only adult cancer hospital in Guatemala. The research coordinator, who was Spanish speaking, enrolled patients into the study, performed assessments, and collected data.

In Santiago, Chile, the study was conducted at the outpatient palliative care clinic at Sótero del Rio Hospital, linked to the Universidad Católica de Chile. The research coordinator, who was Spanish speaking, enrolled patients into the study, performed assessments, and collected data.

In all three medical centers, the research coordinator first screened the outpatient clinic schedule for Latin American advanced cancer patients according to the rest of the eligibility criteria, and then approached patients to explain the study and obtain consent. The completion of the survey questionnaires took ∼40 minutes. It did not interfere with the regular clinic visit. The research teams were trained according to a standard interview protocol lead by the principal investigator in MD Anderson Cancer Center. To monitor the appropriate collection of data, a continuous and regular communication between the PI and the co-PIs in each country took place along the duration of the study.

Assessment tools for spirituality, religiosity, and spiritual pain

To assess spirituality and religiosity, we used a validated spiritual assessment tool: the FICA (Faith, Importance and Influence, Community, and Address) Spiritual History Tool.^17,18 Patients reported their intensity of spirituality and religiosity using an 11-point scale ranging from 0 (“not at all”) to 10 (“very much”).¹

We also assessed issues related to spirituality/religiosity through additional questions. We used the definition of spiritual pain as “a pain deep in your soul (being) that is not physical”¹⁹ and then asked the patients, “Do you think you are experiencing spiritual pain now and how would you rate your overall spiritual pain?” The intensity of spiritual pain was measured using an 11-point scale ranging from 0 (“none”) to 10 (“worst”). An intensity of 1 or higher was considered positive for the presence of spiritual pain.¹

To evaluate the perception of patients about the impact of spirituality and religiosity on their health, we asked the following questions: “Is spirituality/religiosity a source of strength and comfort to you?,” “Does spirituality/religiosity help you cope with your illness?,” and “Does spirituality/religiosity help your family member/caregiver cope with your illness?” We used an 11-point scale ranging from 0 (“not at all”) to 10 (“a great deal”). Finally, we used a modified questionnaire²⁰ to evaluate patients' variation in religious/spiritual beliefs secondary to their disease diagnosis. This questionnaire assessed 6 items: perceived role of spirituality and religiosity on prognosis (1 item), recalled changes in spirituality (1 item) and religiousness (1 item) from before to after diagnosis, and alienation from places of worship as a result of the diagnosis (3 items).

To evaluate multiple symptoms, we used the Edmonton Symptom Assessment Scale (ESAS)²¹; this tool, used in patients with cancer or chronic illness, measures patients' responses to 10 common symptoms (pain, fatigue, nausea, depression, anxiety, drowsiness, shortness of breath, appetite, sleep problems, and feeling of well-being) within the past 24 hours. Patients use the ESAS to rate the intensity of symptoms on a 0 to 10 scale ranging from 0 (“no symptom”) to 10 (“worst possible symptom”). The ESAS was modified in October 2012 to include evaluation of financial distress and spiritual pain (Edmonton Symptom Assessment Scale-Financial/Spiritual [ESAS-FS]).^22,23 We used Karnofsky Performance Scale to classify patients based on their functional status. The lower the Karnofsky score, the worse the survival for most serious illnesses^24,25

To evaluate COPE, we used the Brief-COPE,²⁶ a shorter version of the COPE (Coping Orientation to Problems Experienced) inventory.²⁷ This tool evaluates patients' engagement in 28 behaviors/activities using a scale ranging from 1 (“I haven't been doing this at all”) to 4 (“I've been doing this a lot”).

We also used the validated Brief religious coping (RCOPE) questionnaire to evaluate positive and negative RCOPE strategies. This tool involves two subscales that include seven positive RCOPE and seven negative RCOPE items. The scale uses a 4-point scale ranging from 0 (“not at all”) to 3 (“a great deal”).²⁸

We used the Cut, Annoyed, Guilt, Eye Opener (CAGE) questionnaire to evaluate risk of chemical coping. This tool is used to screen alcoholism at any period of life, (Have you ever felt that you should Cut down on your drinking?, Have you been Annoyed by people criticizing your drinking?, Have you ever felt bad or Guilty about your drinking?, and Have you ever had a drink to get rid of a hangover (i.e., an Eye-opener)? An abnormal score, defined as two positive answers of the four questions, has been shown to have a prognostic value in the opioid management in patients with cancer, who experience pain.^29,30

Spiritual/religious aspects of QOL were evaluated with the validated tool Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being, Expanded version (FACIT-Sp-Ex).³¹ FACIT-Sp-Ex involves two subscale scores: “Faith” (associated with traditional religiousness dimensions) and “Meaning/Peace” (associated with spirituality dimensions). Higher scores indicate greater importance of spiritual/religious aspects of QOL.

To evaluate severity of worry, we used the validated Penn State Worry Questionnaire-Abbreviated (PSWQ-A).³² This tool uses a 5-point Likert-type scale ranging from 1 (“not at all typical of me”) to 5 (“very typical of me”). Total scores range from 8 to 40, with higher scores related to more intense worry.

We also evaluated depression with the validated Center for Epidemiologic Studies Depression Scale (CES-D). This tool involves six scales reflecting major dimensions of depression: psychomotor retardation, loss of appetite, depressed mood, feelings of guilt and worthlessness, feelings of helplessness and hopelessness, and sleep disturbance. Total scores range from 0 to 60. A score of 16 or higher on this scale was used as the cutoff point for high depressive symptoms.^33,34

A bilingual researcher (M.D.-G.) translated the English version of the patients' spirituality, religiosity, and spiritual pain assessment tools into Spanish language. The Spanish version was independently back translated into English to establish semantic and linguistic equivalence between the original and the translated version. The rest of the tools (CAGE, Karnofsky, Brief-COPE, Brief RCOPE, ESAS-FS, FACIT-Sp-Ex, PSWQ-A, and CES-D) have been validated in Spanish. All patients in the three study places completed their questionnaires in Spanish.

Statistical analysis

Patient demographic characteristics such as age, sex, country of origin, Karnofsky performance status, marriage status, religion, and education, as well as disease-related variables such as primary diagnosis, were first summarized by using standard descriptive statistics and frequency tabulation. The survey results for symptoms (ESAS), RCOPE, spirituality and religiosity (FICA and additional questions), spiritual pain assessment, QOL (FACIT-Sp-Ex), emotional distress (CES-D), and COPE were summarized by both median and interquartile range (IQR), when appropriate. The continuous variables were compared among data from the three countries (Chile, Guatemala, and the United States) using the Kruskal-Wallis test. Associations between two continuous variables were assessed using Spearman correlation. All computations were carried out with use of SAS 9.3 software (SAS Institute, Inc., Cary, NC).

Results

The total study population consisted of 325 Latin American patients with advanced cancer. The median age of the 325 patients was 58 years (range: 19–85 years); 60% were female; 62% were Catholic, 30% were Christian, but non-Catholic, and 2% had no religious involvement. The most common types of cancer were gastrointestinal (23%), breast (13%), and gynecological (12%). Table 1 shows characteristics of the participants. Multiple symptoms were expressed by participants; they included pain (median: 5; IQR: 2–8); fatigue: 5 (2–8); depression: 3 (0–7); anxiety: 3 (0–6); well-being: 4 (1–6); financial distress: 4 (0–8); and worry: 5 (0–8) (Table 2).

Table 1.

Characteristics of Advanced Cancer Patients

Characteristics	Total (n = 325)	Chile (n = 104)	Guatemala (n = 99)	United States (n = 122)	p a
Age, median (IQR), years	58 (46, 66)	65 (57, 70)	54 (45, 65)	53 (42, 60)	<0.0001
Karnofsky performance status, median (IQR)	70 (60, 80)	70 (60, 80)	80 (70, 90)	70 (60, 80)	0.0072
bCAGE ≥2/4	31 (10%)	24 (23%)	1 (1%)	6 (5%)	<0.0001
Sex
Female	193 (60%)	46 (44%)	70 (70%)	77 (63%)	<0.0001
Male	132 (40%)	58 (56%)	29 (30%)	45 (37%)
Marital status
Married	204 (64%)	68 (65%)	56 (57%)	80 (65.5%)	0.014
Single/never married	40 (12%)	12 (11%)	9 (9%)	19 (15.5%)
Divorced	5 (2%)	3 (3%)	0 (0%)	2 (2%)
Single/lives with partner	25 (8%)	4 (4%)	15 (15%)	6 (5%)
Widowed	23 (7%)	9 (9%)	10 (10%)	4 (3%)
Separated	22 (7%)	8 (8%)	5 (5%)	9 (7%)
Undisclosed	6 (2%)	0 (0%)	4 (4%)	2 (2%)
Religious affiliation
Catholic	200 (61.5%)	84 (81%)	47 (47.5%)	69 (56%)	<0.0001
Christian non-Catholic	98 (30%)	7 (6%)	47 (47.5%)	44 (36%)
Muslim	1 (0.3%)	0 (0%)	0 (0%)	1 (1%)
Native American	1 (0.3%)	0 (0%)	0 (0%)	1 (1%)
Nondenominational	3 (0.9%)	1 (1%)	0 (0%)	2 (2%)
Other	15 (5%)	8 (8%)	2 (2%)	5 (4%)
None	7 (2%)	4 (4%)	3 (3%)	0 (0%)
Education
Advanced degree	4 (1%)	0 (0%)	0 (0%)	4 (3%)	<0.0001
College	17 (5%)	8 (8%)	1 (1%)	8 (7%)
High school/tech school	113 (35%)	65 (62%)	9 (9%)	39 (32%)
Some college/Jr. college	19 (6%)	7 (7%)	0 (0%)	12 (10%)
Less than high school	154 (47%)	24 (23%)	76 (77%)	54 (44%)
Unknown	18 (6%)	0 (0%)	13 (13%)	5 (4%)
Primary cancer diagnosis					<0.0001
Gastrointestinal	71 (22%)	23 (22%)	25 (25%)	23 (19%)
Breast	40 (12%)	12 (12%)	10 (10%)	18 (15%)
Gynecological	39 (12%)	5 (5%)	24 (24%)	10 (8%)
Head and neck	23 (7%)	8 (8%)	7 (7%)	8 (7%)
Prostate	21 (6%)	14 (14%)	6 (6%)	1 (1%)
Lymphoma	19 (6%)	4 (4%)	3 (3%)	12 (10%)
Urinary/renal	20 (6%)	6 (6%)	4 (4%)	10 (8%)
Lung	14 (4%)	4 (4%)	2 (2%)	8 (7%)
Multiple myeloma	9 (3%)	8 (8%)	1 (1%)	0 (0%)
Sarcomas	10 (3%)	4 (4%)	2 (2%)	4 (3%)
Skin	9 (3%)	5 (5%)	4 (4%)	0 (0%)
Central nervous system	5 (2%)	2 (2%)	0 (0%)	0 (0%)
Bone	3 (1%)	1 (1%)	1 (1%)	1 (1%)
Others	42 (13%)	8 (8%)	10 (10%)	27 (22%)

Values represent n (%) of patients unless otherwise indicated.

^a p-Values: two-sided Pearson chi-square test/Fisher's exact test, level of significance 0.05.

^b Two or more affirmative responses on the CAGE chemical coping questionnaire. (Questions for screening alcoholism, used to evaluate risk of chemical coping).

CAGE, Cut, Annoyed, Guilt, Eye Opener; IQR, interquartile range

Table 2.

Symptoms among Latinos with Advanced Cancer

Symptom (ESAS-FS)a	Total median (IQR)	Chile median (IQR)	Guatemala median (IQR)	United States median (IQR)	p b
Pain	5 (2, 8)	5 (3, 8)	8 (4, 10)	3 (0, 6)	<0.0001
Fatigue	5 (2, 8)	5 (4, 7)	7 (4, 8)	3 (0, 6)	<0.0001
Nausea	0 (0, 5)	0 (0, 4)	3 (0, 7)	0 (0, 3.5)	<0.0001
Depression	3 (0, 7)	5 (0, 7)	5.5 (1, 9)	0 (0, 3)	<0.0001
Anxiety	3 (0, 6)	5 (2, 7)	4 (0, 7)	0 (0, 3)	<0.0001
Drowsiness	3 (0, 6)	5 (0, 6)	4 (1, 7)	0 (0, 5)	<0.0001
Shortness of breath	0 (0, 5)	1 (0, 6)	0 (0, 5.5)	0 (0, 2)	0.0019
Appetite	3 (0, 6)	2 (0, 5)	4.5 (1, 8)	1 (0, 5)	<0.0001
Sleep	3 (0, 6)	4.5 (1, 7)	2 (0, 7)	2 (0, 5)	0.0532
Well-being	4 (1, 6)	5 (2, 6)	3 (1, 6)	3 (0, 6)	0.0485
Financial distress	4 (0, 8)	0 (0, 7)	7 (1, 9)	3 (0, 6.5)	<0.0001
Worry	5 (0, 8)	7 (4, 10)	6 (2, 8)	2.5 (0, 7)	<0.0001

^a ESAS-FS items were assessed on a scale from 0 to 10 (0 = “no symptom”; 10 = “worst possible symptom”).

^b Kruskal-Wallis test.

ESAS-FS, Edmonton Symptom Assessment Scale-Financial/Spiritual.

Among the Latin American cancer patients, 97% considered themselves spiritual and 89% religious, with median intensities of 7 (IQR: 5–10) and 7 (5–9), respectively. The median importance of spirituality/religiosity in the patients' lives (score 0–10; 10 = very important) was 10 (IQR: 8–10). Table 3 shows the intensity of spirituality/religiosity for the patients by country: in all three countries, intensity was high, although the Chilean patients expressed less intensity of importance of spirituality/religiosity. There were only 312 participants who answered the statements regarding the importance of spirituality and religiosity in their lives. There was no disclosure of why the rest did not answer these questions. Among the ones who answered, 138 (44%) agreed or totally agreed that spirituality and religiosity are the same concept, whereas 35 (11%) had neutral opinions about this difference in concepts. Also, 44% considered themselves more spiritual, 44% equally spiritual, and 8% less spiritual than before they were diagnosed as having cancer; 36% of participants considered themselves more religious, 48% equally religious, and 8% less religious than before they were diagnosed as having cancer. Twelve percent of patients expressed that due to the experience of living with cancer, they had changed their place of worship within the same religious group. Eighty-nine percent believed that their spiritual/religious beliefs had helped them to live longer.

Table 3.

Spirituality and Religiosity of Latin American Advanced Cancer Patients

Questionsa	Total median (IQR)	Chile median (IQR)	Guatemala median (IQR)	United States median (IQR)	p
Do you consider yourself a spiritual person?	7 (5, 10)	6 (5, 8)	8 (6, 10)	8 (5, 10)	<0.0001
Do you consider yourself a religious person?	7 (5, 9)	6 (5, 8)	7 (4, 10)	7 (4, 9)	0.2306
How important is spirituality in your life?	10 (8, 10)	8 (6, 10)	10 (9, 10)	10 (8, 10)	<0.0001
How important is religion in your life?	10 (8, 10)	9 (6, 10)	10 (10, 10)	10 (9, 10)	<0.0001
Is spirituality/religiosity a source of strength and comfort to you?	10 (8, 10)	8 (6, 10)	10 (9, 10)	10 (10, 10)	<0.0001
Does spirituality/religiosity help you cope with your illness?	10 (8, 10)	8 (6, 10)	10 (9, 10)	10 (10, 10)	<0.0001

^a Participants rated items on a scale of 0 to 10 (0 = not at all and 10 = very much, the most important).

The importance of spirituality/religiosity was associated with various other concepts, as follows: helps them to cope with their illness (98%; r = 0.66303; p < 0.0001), is a source of strength and comfort (99%; r = 0.73380; p < 0.0001), has a positive effect on physical symptoms (81%; r = 0.42067; p < 0.0001) and emotional symptoms (84%; r = 0.16577, p < 0.0001), and helps caregivers cope with patients' illnesses (100%; r = 0.39864, p < 0.0001). Importance of spirituality/religiosity also correlated with spiritual well-being/QOL as measured by the FACIT-Sp-Ex tool, especially for the subscales Faith (r = 0.58095, p < 0.0001) and Meaning/Peace (r = 0.20023, p = 0.0004); and with positive RCOPE strategies (r = 0.52438, p < 0.0001). At the same time, the importance of spirituality/religiosity was negatively correlated with high depressive symptoms on the CES-D (r = −0.11754, p = 0.0374) and CAGE positivity (r = −0.18664, p = 0.0010) (Table 4). A multicovariate linear regression evaluating the effects of different variables on the importance of spirituality/religiosity showed significant correlation with CAGE (r = −0.22234, p = 0.0293) and the FACIT-Sp-Ex-Faith subscale (r = 0.38721, p < 0.0001; R² = 0.43).

Table 4.

Correlations among the Importance of Spirituality and the Presence of Spiritual Pain and Coping, Symptoms, and Quality of Life in Latin American Cancer Patients

	Importance of spirituality		Spiritual pain
	Spearman correlation coefficient (r)	p a	Spearman correlation coefficient (r)	p a
Characteristics
Age	−0.09502	0.0928	0.00919	0.8721
CAGEc	−0.18664	0.0010	−0.00813	0.8874
Karnofsky performance status	0.09855	0.0884	0.09855	0.0884
Spirituality/religiosity questionsb
Do you consider yourself a Spiritual person?	0.55096	<0.0001	0.02140	0.7088
Do you consider yourself a religious person?	0.30484	<0.0001	0.10213	0.0740
How important is religion in your life?	0.79892	<0.0001	−0.08768	0.1240
Is spirituality/religiosity a source of strength and comfort to you?	0.73380	<0.0001	−0.11041	0.0529
Does spirituality/religiosity help you cope with your illness?	0.66303	<0.0001	−0.08221	0.1534
Does spirituality/religiosity help your family member/caregiver cope with your illness?	0.39864	<0.0001	−0.11901	0.0378
Spirituality/religiosity has a positive effect on your physical symptoms	0.42067	<0.0001	−0.12267	0.0311
Spirituality/religiosity has a positive effect on your emotional symptoms	0.16577	0.0035	−0.03091	0.5914
ESAS-FSd symptoms
Pain	−0.01786	0.7541	0.13067	0.0225
Fatigue	−0.03354	0.5576	0.21341	0.0002
Nausea	−0.01260	0.8257	0.16483	0.0040
Depression	−0.05394	0.3470	0.33295	<0.0001
Anxiety	−0.07520	0.1881	0.37245	<0.0001
Drowsiness	−0.06987	0.2207	0.19610	0.0006
Shortness of breath	−0.15538	0.0063	0.18763	0.0010
Appetite	−0.08485	0.1360	0.13268	0.0205
Sleep	−0.11688	0.0397	0.17968	0.0016
Well-being	−0.08312	0.1443	0.23937	<0.0001
Financial distress	0.03991	0.4846	0.24681	<0.0001
Worry	−0.14616	0.0102	0.38936	<0.0001
CES-De	−0.11754	0.0374	0.32925	<0.0001
Spiritual well-being/QOL (FACIT-Sp-Ex)f	0.44064	<0.0001	−0.21641	0.0002
Meaning/peace subscale	0.20023	0.0004	−0.18825	0.0010
Faith subscale	0.58095	<0.0001	−0.15392	0.0075
COPE behaviors/activities
Denial	−0.09893	0.0825	0.18687	0.0011
Behavioral disengagement	−0.15799	0.0054	0.13974	0.0148
Venting	−0.20151	0.0004	0.25714	<0.0001
Positive reframing	0.09218	0.1058	−0.15252	0.0077
Religion	0.51003	<0.0001	−0.23765	<0.0001
Self-blame	−0.13088	0.0214	0.17457	0.0023
Humor	0.11449	0.0443	−0.02327	0.6861
Acceptance	−0.02878	0.6143	−0.09707	0.0911
Active coping	−0.01890	0.7407	−0.13618	0.0175
Positive RCOPE strategies	0.52438	<0.0001	−0.15780	0.0057
Negative RCOPE strategies	−0.00661	0.9083	0.27141	<0.0001

^a Spearman correlation. Bold indicates statistical significance at p < 0.05. The questions used to correlate with other items listed in the table were “How important is Spirituality/Religiosity is your life?” Are you having

“Spiritual Pain?”

^b Participants rated items on a scale of 0 to 10 (0 = not at all and 10 = very much, the most important).

^c CAGE (Questions for screening alcoholism, used to evaluate risk of chemical coping)

^d ESAS-FS items were assessed on a scale from 0 to 10 (0 = “no symptom” and 10 = “worst possible symptom”).

^e A score of 16 or higher was used as the cutoff point for high depressive symptoms.

^f FACIT-Sp-Ex. Higher scores indicate greater importance of spiritual/religious aspects of QOL.

CES-D, Center for Epidemiologic Studies Depression Scale; COPE, coping strategies; FACIT-Sp-Ex, Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being, Expanded version; QOL, quality of life; RCOPE, religious coping

Interestingly, 60% of the Latin American cancer patients reported that their spiritual/religious needs had not been supported by the medical team. Only 47 (24%) had received pastoral attention inside the hospital, and 45 (23%) had received a clergy visit from the community.

There were only 312 participants who answered the statements regarding the importance of spirituality and religiosity in their lives. There was no disclosure of why the rest did not answer these questions. Among the ones who answered, 162 (52%) reported having spiritual pain (median 6; IQR: 5–8). Also, patients with spiritual pain expressed poorer COPE such as denial (p = 0.0337), behavioral disengagement (p = 0.0106), venting (p < 0.0001), less positive reframing (p < 0.0157), and worse spiritual well-being/QOL (p = 0.0002), including the subscales for Meaning/Peace (p = 0.0027) and Faith (p = 0.0035); all patients reported less positive RCOPE strategies (p < 0.0012) and more negative RCOPE strategies (p < 0.0001) (Table 5). Spiritual pain significantly correlated with worse pain (r = 0.13067, p = 0.0225), fatigue (r = 0.21341, p = 0.0002), depression (r = 0.33295, p < 0.0001), anxiety (r = 0.37245, p < 0.0001), financial distress (r = 0.24681, p < 0.0001), and worry (r = 0.38936, p < 0.0001), and with worse spiritual well-being/QOL (FACIT-Sp-Ex) (r = −0.21641, p = 0.0002) and worse COPE, including negative RCOPE strategies (r = 0.27141, p < 0.0001) (Table 4). A multicovariate linear regression evaluating the effects of different variables on spiritual pain showed significant correlation with anxiety (r = 0.33472, p < 0.0001), negative RCOPE strategies (r = 0.17068, p = 0.0212), and spiritual well-being/QOL (FACIT-Sp-Ex) (r = −0.03660, p = 0.0021; R² = 0.19).

Table 5.

Impact of Spiritual Pain in Latin American Advanced Cancer Patients

	aWith spiritual pain median (IQR)	Without spiritual pain median (IQR)	p b
Spirituality/religiosity questionsc
Do you consider yourself a spiritual person?	7 (5, 9)	7 (5, 10)	0.7925
Do you consider yourself a religious person?	6 (5, 9)	6 (3, 9)	0.1853
How important is spirituality in your life?	10 (8, 10)	10 (9, 10)	0.0746
How important is religion in your life?	10 (8, 10)	10 (9, 10)	0.0226
Is spirituality/religiosity a source of strength and comfort to you?	10 (8, 10)	10 (9, 10)	0.0127
Does spirituality/religiosity help you cope with your illness?	10 (8, 10)	10 (8, 10)	0.0582
Have you ever experienced spiritual pain any time in your life?	7 (5, 10)	0 (0, 6)	<0.0001
Does your spiritual pain make your physical symptoms (pain, fatigue, drowsiness, appetite, or insomnia) worse?	5 (1, 8)	0 (0, 3)	<0.0001
Does your spiritual pain make your emotional symptoms (anxiety and/or depression) worse?	7 (4, 8)	0 (0, 3)	<0.0001
ESAS-FSd symptoms
Pain	6 (3, 8)	5 (1, 8)	0.1390
Fatigue	6 (3, 8)	4 (2, 7)	0.0059
Nausea	1 (0, 5)	0 (0, 4)	0.0125
Depression	5 (2, 7)	0 (0, 5)	<0.0001
Anxiety	5 (0, 7)	0 (0, 4)	<0.0001
Drowsiness	5 (0, 7)	2 (0, 5)	0.0029
Shortness of breath	1 (0, 5)	0 (0, 2)	0.0021
Appetite	4 (0, 7)	2 (0, 6)	0.0211
Sleep	5 (0, 7)	2 (0, 5)	0.0068
Well-being	5 (2, 7)	3 (0, 5)	<0.0001
Financial distress	6 (0, 8)	1 (0, 6)	0.0003
Worry	7 (4, 9)	3 (0, 7)	<0.0001
CES-De	19 (11, 27)	11 (4, 19)	<0.0001
Spiritual well being/QOL (FACIT-Sp-Ex)f	74 (64, 84)	78 (68, 86)	0.0002
Meaning and peace	25 (20, 28)	27 (22, 30)	0.0027
Faith	13 (10, 16)	15 (12, 16)	0.0035
COPE behaviors/activities
Denial	4 (2, 6)	4 (2, 6)	0.0337
Behavioral disengagement	3 (2, 4)	2 (2, 3)	0.0106
Venting	4 (2, 6)	2 (2, 4)	<0.0001
Positive reframing	4 (3, 6)	5 (4, 7)	0.0157
Religion	7 (5, 8)	8 (6, 8)	<0.0001
Self-blame	4 (2, 5)	2 (2, 4)	0.0085
Positive religious COPE	20 (16, 22)	21 (18, 25)	0.0012
Negative religious COPE	12 (10, 15)	10 (7, 13)	0.0001

^a Spiritual pain was scored from 0 to 10 (0 = “none” and 10 = “worst”). Spiritual pain was defined as any response ≥1.

^b Kruskal-Wallis test. Bold indicates statistical significance at p < 0.05.

^c Participants rated items on a scale of 0 to 10 (0 = not at all and 10 = very much, the most important).

^d ESAS-FS items were assessed on a scale from 0 to 10 (0 = “no symptom” and 10 = “worst possible symptom”).

^e A score of 16 or higher was used as the cutoff point for high depressive symptoms.

^f FACIT-Sp-Ex. Higher scores indicate greater importance of spiritual/religious aspects of QOL.

Discussion

Religion and spirituality have a powerful impact on many Latinos. Our study highlights the importance of spirituality and religiosity in the life of Latin American patients with advanced cancer and their impact on these patients' symptoms, COPE, and QOL. The patients in our cohort reported high frequency and intensity of spirituality and religiosity, like the findings reported in the Pew study of 4016 Latinos, 92% of whom considered themselves religious—68% were Roman Catholic and 15% were Evangelical. Also, among this Latino population, only 8% of Latinos did not express being engaged with any religious belief.^35,36 Interestingly, as spirituality has been defined as a broader construct that can include religious and nonreligious forms,^17,37–39 in our study population, more than 40% considered spirituality and religiosity to be the same concept. This finding highpoint the complexity of the meaning and concepts of spirituality by the general population. As clinicians we have to be aware of this complexity in the concepts of spirituality because it might have an impact in communication and provision of spiritual care in patients and caregivers from different cultural backgrounds.^17,38–40 Latinos are inclined to have a profound relationship with their conception of Higher Power/God and religious beliefs. In a previous study in our outpatient palliative care clinic,¹ almost all the patients with advanced cancer evaluated (n = 100) considered themselves highly spiritual and religious, and spirituality and religiosity had a positive effect in coping with their illness and with their physical and emotional symptoms. Likewise, Peselow et al.⁴¹ noted that with a higher level of spiritual/religious practices, patients might experience less depression. These spiritual practices provided to patients a system of purpose with better perspective on their situation, self-esteem, hope, and adaptation, as well as solider relationships.⁴²

Another interesting finding is the inverse relationship between the importance of spirituality and the presence of CAGE positivity. High spirituality/religiosity has been identified to have a regulatory control function and be a protective factor of risk behaviors, including alcohol use.⁴³ In a sample of 5179 adolescents and young adults 15–24 years of age in post-mandatory education in Switzerland, Chen et al.⁴⁴ noted that the presence of spiritual beliefs was associated to a decreased risk of tobacco smoking, alcohol misuse, and cannabis use.

It is important to recognize that involvement in religious services has been associated with decreased social isolation and decreased feelings of anger, and these allow patients to better cope with their illness.^45,46 We need more research to explore the relationship between participation in religious services and coping, symptom distress, and medical decisions in Latin American patients with advanced cancer.

As noted, interestingly, in all three countries, the frequency and intensity of spirituality and religiosity were high, although the Chilean population expressed less intensity for the importance of spirituality/religiosity. This might be explained, in part, by Chileans' reduced involvement in religious practices during the past few decades.^47,48 Pérez-Cruz et al.⁴⁸ reported that in a Chilean population of cancer patients, 73% considered themselves spiritual and only 69% religious. More studies are needed in various Latin American countries to explore the existing changes in spiritual and religious beliefs among these populations and how these beliefs affect how people cope with adverse situations/illness.

A very important finding in our study is that a high percentage (60%) of Latino advanced cancer patients reported that their spiritual/religious needs had not been supported by the medical team, and less than 25% received pastoral attention inside the hospital or had received a clergy visit from the community. Spiritual support strongly impacts the care of patients with advanced and terminal illnesses. Balboni et al.,⁴⁹ in a cohort of patients with advanced cancer at the end of life, reported that when the patients not only received spiritual support from their religious communities but also received spiritual care from the medical team, these patients had fewer aggressive interventions at the end of life, were less likely to die in an intensive care unit, and used more hospice services.

Many health care providers recognize the importance of spirituality, beliefs, to help and provide spiritual care to patients suffering with spiritual needs/distress; unfortunately there are several barriers that do not allow them to provide compassionate and quality spiritual care to patients and caregivers, including lack of spiritual care education, time restrictions due to clinical load, uneasiness in discussing spiritual/religious beliefs and exploring their spiritual needs, and cultural differences. Health care providers need spiritual care education; thus far, there is a deficiency of such training accessible globally. Also, the support from health care administrators and key stakeholders, and the promotion of spiritual leadership are important to establish global spiritual care within an institution.^40,50,51 More research is needed in Latin American settings to better understand these relationships.

Based on the bio-psycho-social-spiritual model of care, clinical teams should provide spiritual care to address the spirituality, religious beliefs, and the suffering of patients and their love ones. Patients with spiritual needs and suffering should ideally be referred to a chaplain, who is considered a specialist in spiritual care in the team. In Latin America, there is growing awareness among health care providers about the integration of spiritual care in the daily patient care, the spiritual care education, and the need for participation of a spiritual care specialist (chaplain) in the team; still there is limited presence of chaplains or spiritual care specialist. Also, it is important to mention that The Latin American Association of Palliative Care (ALCP; from the Spanish: Asociacion Latino Americana de Cuidado Paliativo) established the Spirituality Commission, with interdisciplinary palliative care team members from different countries in Latin America, with the main objective to promote and improve the integration of Spiritual Care in the daily clinical practice, through educational programs and research in all settings of care. It is a work in progress from all members of the ALCP to accomplish this objective.

Another important finding in our study was the high prevalence of spiritual pain (52%) and the associated expression of worse physical pain, fatigue, depression, anxiety, financial distress, and worry. At the same time, patients with spiritual pain had worse general and RCOPE strategies and worse spiritual QOL. Pérez-Cruz et al.⁴⁸ reported a higher prevalence (67%) of spiritual pain in Chilean cancer patients, and its presence was associated with worse overall QOL. Similarly, in prior studies performed by our group,^1,22 we reported in advanced cancer patients a 44% prevalence of spiritual pain; these patients also expressed less spirituality and religiosity and had worse physical and emotional distress. Mako et al.¹⁹ found a high frequency of spiritual pain in a sample of 57 hospitalized patients with advanced cancer, who were interviewed by a chaplain. In a report by Alcorn et al.,⁴⁵ 85% of patients with advanced cancer being treated with radiation therapy acknowledged one or more spiritual issues. Among the spiritual issues expressed by these patients, the most frequently reported were “seeking a closer connection with God or one's faith,” 54%; “feeling abandoned by God,” 28%; and “seeking forgiveness (of oneself or others),” 47%. The differences in frequency could be attributed, in part, to different assessment tools for spiritual pain (chaplain vs. self-assessment) and different settings between the studies (inpatient vs. outpatient). Other factors that could affect the differences in frequency of spiritual pain are patients' culture, ethnicity, understanding and meaning of the concept of spiritual pain or distress, spirituality and religiosity, and community church involvement.⁵² More studies are needed to evaluate the meaning and frequency of, and factors associated with, spiritual pain in Latin American patients and other ethnicities.

Spiritual pain is highly prevalent in patients with advanced illness, and knowledge of this prevalence increases the importance of screening all patients for spiritual concerns, even if they have not identified themselves as religious or spiritual persons. Identifying these spiritual needs and issues is the first step in providing appropriate spiritual interventions to our patients in need.^39–41,53 The ESAS-FS can be used as the initial tool to explore the presence of a spiritual/existential crises and to lead toward a complete spiritual screening/assessment and further interventions.²² Additional research will contribute to the validation of this tool's spiritual distress element, especially in the Latin American setting.

This study has several limitations. Due to its cross-sectional design, it is difficult to determine causation among spirituality, religiosity, spiritual pain, and physical and emotional symptoms and QOL. We had three different sites of evaluation, our study being conducted at an outpatient palliative care clinic at a tertiary cancer care center in the United States and at outpatient palliative care clinics in two Latin American countries; hence, our findings may not be generalizable for all Latin American populations with advanced illnesses evaluated by palliative care teams. The tools we used to measure spirituality, religiosity, and spiritual pain were quantitative and unidimensional, and they might not have captured the intricate nature of these concepts in different cultures.

We as a palliative care community need to be mindful of the very strong spiritual and religious needs of Latin American patients who face a life-threatening illness, as well as the needs of their caregivers. By integrating the spiritual domain in our daily practice, we are providing high-quality patient- and family-centered palliative care. All members of the medical team are called to provide spiritual care and to attend to the suffering of this population with specific needs.^{40–48,53,54} Our mission is to continue to share and expand our findings with all disciplines of health care providers caring for patients with advanced cancer through publications, congresses, and educational activities in our own and other institutions to promote spiritual care in this population and other ethnicities.

We conclude that most Latin American patients with advanced cancer consider themselves spiritual and religious. Patients in our multicenter study perceived that spirituality and religiosity helped them cope with their illness and emotional distress and provided them with COPE and higher QOL. Still, patients suffer, and more than 50% of LAAdCa reported that spiritual pain and their spiritual/religious needs were not totally addressed and supported by the medical team.

Funding Information

Dr. M.O.D.-G. is supported, in part, by National Institutes of Health grants R01CA200867 (M.O.D.-G.); R01NR010162-01A1, R01CA122292-01, and R01CA124481-01 (E.B.); and P30CA016672 (used the Biostatistics Resource Group).

Author Disclosure Statement

No competing financial interests exist.