Vol. 60 No.

1 July 2020 Journal of Pain and Symptom Management 37

Original Article

Spiritual Care, Pain Reduction, and Preferred Place of

Death Among Advanced Cancer Patients in Soweto, South
Africa
Mpho Ratshikana-Moloko, MD, MPhil, Oluwatosin Ayeni, MBChB, MSc, Jacob M. Tsitsi, MBChB, FCP(SA),
Michelle L. Wong, MBBCh, FCP(SA), FCCP, FRCP(Lond), Judith S. Jacobson, MBA, DrPh,
Alfred I. Neugut, MD, DrPh, Mfanelo Sobekwa, MBChB, Maureen Joffe, PhD, Keletso Mmoledi, CPN, MPH,
Charmaine L. Blanchard, MBBCh, MPhil, Witness Mapanga, MPH, PhD, Paul Ruff, MBBCh, MMed, FCP(SA),
Herbert Cubasch, MD, Daniel S. O’Neil, MD, MPH, Tracy A. Balboni, MD, MPH, FAAHPM, and Holly G. Prigerson,
PhD
Chris Hani Baragwanath Academic Hospital (M.R.-M., J.M.T., M.S., K.M.), Johannesburg; Centre for Palliative Care (M.R.-M., M.S.,
K.M., C.L.B.), Faculty of Health Sciences, University of Witwatersrand, Johannesburg; Non Communicable Diseases Research
Division (M.R.-M., O.A., M.S., M.J., K.M., C.L.B., W.M., P.R.), Wits Health Consortium (Pty) Ltd, Johannesburg; Department of
Paediatrics (O.A., M.J.), SAMRC/Wits Developmental Pathways to Health Research Unit, Faculty of Health Sciences, University of
Witwatersrand, Johannesburg; Department of Medicine (J.M.T., M.L.W., P.R.), Faculty of Health Sciences, University of
Witwatersrand, Johannesburg; Division of Pulmonology (M.L.W.), Chris Hani Baragwanath Academic Hospital, Johannesburg, South
Africa; Herbert Irving Comprehensive Cancer Center (J.S.J., A.I.N.), College of Physicians and Surgeons, Columbia University, New
York, New York; Department of Medicine (A.I.N.), College of Physicians and Surgeons, Columbia University, New York, New York;
Department of Epidemiology (J.S.J., A.I.N.), Mailman School of Public Health, Columbia University, New York, New York, USA;
South Africa Medical Research Council Common Epithelial Cancers Research Centre (M.J., P.R., H.C.), University of Witwatersrand,
Johannesburg, Gauteng; Division of Medical Oncology (P.R.), Department of Internal Medicine, University of the Witwatersrand
Faculty of Health Sciences, Johannesburg; Department of Surgery (H.C.), Faculty of Health Sciences, University of Witwatersrand,
Johannesburg, South Africa; Sylvester Comprehensive Cancer Center (D.S.O.), University of Miami Miller School of Medicine,
Miami; Dana-Farber/Brigham and Women’s Cancer Center (T.A.B.), Harvard Medical School, Boston, Massachusetts; and Cornell
Center for Research on End-of-Life Care (H.G.P.), Weill Cornell Medicine, New York, New York, USA

Abstract
Context. When religious and spiritual (R/S) care needs of patients with advanced disease are met, their quality of life (QoL)
improves. We studied the association between R/S support and QoL of patients with cancer at the end of life in Soweto, South Africa.

Objectives. To identify R/S needs among patients with advanced cancer receiving palliative care services and to assess
associations of receipt of R/S care with patient QoL and place of death.
Methods. A prospective cohort study conducted from May 1, 2016 to April 30, 2018 at a tertiary hospital in Soweto, South Africa.
Nurses enrolled patients with advanced cancer and referred them to the palliative care multidisciplinary team. Spiritual counselors
assessed and provided spiritual care to patients. We compared sociodemographic, clinical, and R/S factors and QoL of R/S care
recipients and others.
Results. Of 233 deceased participants, 92 (39.5%) had received R/S care. Patients who received R/S care reported less pain (2.82
1.23 vs. 1.93 1.69), used less morphine, and were more likely to die at home than patients who did not (57.5% compared with 33.7%).
On multivariate logistic regression analysis, adjusting for significant confounding influences and baseline African Palliative Care
Association Palliative care Outcome Scale scores, receipt of spiritual care was associated with reduced pain and family worry (odds
ratio 0.33; 95% CI 0.11e0.95 and odds ratio 3.43; 95% CI 1.10e10.70, respectively).

Address correspondence to: Mpho Ratshikana-Moloko, MD, Accepted for publication: January 31, 2020.
MPhil, Centre for Palliative Care, Faculty of Health Sciences,
University of Witwatersrand, 7 York Road, Parktown 2193,
South Africa. E-mail: mpho.ratshikana-moloko@wits.ac.za

2020 American Academy of Hospice and Palliative Medicine. 0885-3924/$ - see front matter
Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jpainsymman.2020.01.019
38 Ratshikana-Moloko et al. Vol. 60 No. 1 July 2020

Conclusion. Patients with cancer have R/S needs. R/S care among our patients appeared to improve their end-of-life experience.
More research is needed to determine the mechanisms by which R/S care may have improved the observed patient outcomes. J Pain
Symptom Manage 2020;60:37e47. 2020 American Academy of Hospice and Palliative Medicine.
Published by Elsevier Inc. All rights reserved.

Key Words
Religion, spirituality, palliative care, cancer patients, pain, place of death

Key Message South Africa faces a heavy burden of communicable

and noncommunicable diseases. Noncommunicable
Prospective cohort study describing religious/spiri-tual
diseases accounted for 61% of deaths in the Western Cape
needs and care among patients with advanced cancer. The 24
results show that patients with cancer have spiritual needs. in 2013. One in six deaths globally is due to cancer, and
Receipt of religious/spiritual care was associated with less cancer diagnoses are expected to increase by 70% in the
pain (odds ratio 0.33; 95% CI 0.11e0.95) and the next 2 decades, especially in low-income and middle-
25
likelihood of dying in the preferred place of death (57.5% income countries. The South African National Policy
compared with 33.7%). Framework and Strategy for Palliative Care (2017e2022)
26
incorporates spirituality into health care. Palliative care
services in south and southern Africa and elsewhere rarely
Introduction address R/S needs, despite available policies, guidelines,
and evidence.
Religion and spirituality (R/S) are important to most
1e4 We therefore examined spiritual needs and reli-
patients facing life-threatening illnesses. Several
studies have found spiritual needs to be common among gious/spiritual (R/S) care received by patients with
patients with serious illnesses, advanced cancer receiving palliative care from Sowe-to,
5e9
including cancer. These and other studies suggest that Johannesburg. We compared baseline and last assessment
5,10,11 before death, QoL outcomes, and preferred location of
patients rely on R/S to cope, and that the
stress and suffering associated with illness frequently death among patients who did and did not receive R/S care
9,12 at end of life. We hy-pothesized that patients who received
generate spiritual needs. Prayer and other R/S
practices are associated with improvements in pain and R/S care would have better QoL (e.g., less pain, more
5,10,11,13,14
quality of life (QoL) and are valued by most belief that life is worthwhile, more peacefulness) and be
6,14e16 more likely to die in their preferred location than those
patients. Failure to identify and
address the R/S needs of patients with cancer may increase who did not.
6,8
distress and suffering. Integration of spir-itual care
17
within the clinical care setting is recommended.
Palliative care encompasses the physical, social, Methods
emotional, and spiritual components of illness man- Setting
agement. Holistic health care must address the spir-itual as The study was conducted at the Gauteng Center for
17,18
well as the physical, psychological, and social aspects. Palliative Care (GCPC), based at Chris Hani Baragwa-
Spirituality refers to the way people find meaning and nath Academic Hospital, a major teaching hospital of the
purpose during traumatic, illness, and life-threatening University of Witwatersrand, Soweto, South Africa.
17 Patients are referred to the palliative care team for
events. According to the African Palliative Care
Association (APCA), religious beliefs, coping, and management. A multidisciplinary team comprising nurses,
19
transcendence are part of spirituality. Finding meaning doctors, social workers, and spiritual coun-selors (SCs)
20 provides comprehensive palliative care services
and purpose in the midst of suffering is important. Most addressing the patients’ physical, psychoso-cial, and
patients prefer to die at home, but very few achieve home spiritual needs in the hospital, at home, and in the
21,22
death. Dying in the preferred place of death (POD) is outpatient clinic.
considered an indicator of high-quality palliative care.
Patients’ families, faith communities, and local Study Design and Participants
communities play a role in caring for sick patients within
23 Between May 2016 and April 2018, we conducted a
their homes. Religious patients prefer to choose where prospective cohort study of patients with advanced cancer
they would like to die, compared with those who are less in Soweto. Eligible patients were older than 18 years;
14
religious and less spiritual. diagnosed with breast, gastrointestinal, or
Vol. 60 No. 1 July 2020 Advanced Cancer Patients in Soweto, South Africa 39

lung carcinoma, or soft tissue sarcoma; judged by a
specialist physician as unlikely to benefit from curative-
intent therapy and to survive beyond six months. Of 598
patients approached, 324 were enrolled, 363 were not
eligible, and 233 had died at time of analysis (Fig. 1). Two
had missing data on duration from enrollment to death,
and two did not have information on receiving R/S care.
Study Measures
Trained nurses conducted the interview in the pa-tient’s
preferred language (English, IsiZulu, Sesotho, IsiXhosa,
or Setswana). At study enrollment, patients reported their
age, gender, marital status, race, and home language, level
of education, employment sta-tus, preferred POD, and R/S
needs. Information on receipt of R/S care and actual POD
were obtained from family caregivers at postmortem.
Clinical
information about the primary tumor, comorbidities, and
HIV status was obtained from the patient’s clinical
records. Nurses evaluated the performance status of
patients using the Eastern Cooperative Oncology Group
27
(ECOG) Performance Scale (PS).
Palliative Care Outcomes
Nurses administered the APCA Palliative care Outcome
Scale (POS), a multidimensional validated tool, consisting
of 10 questions.
28,29
Seven questions address the patient’s
experience during the past three days: 1) pain, 2) other
symptoms (e.g., nausea, cough, and constipation), 3)
feeling worried, 4) feeling that life is worthwhile, 5)
feeling at peace, 6) ability to share feelings with friends
and family, and 7) receipt of enough help and advice to
plan for the future. Three questions ask the family
caregiver about 1) amount of information received about
the patient,

Total patients approached (N = 598)

Total patients enrolled (N = 324) Total patients not eligible (N = 363)

Patient still alive, with no Patients who died and had

information on R/S care at end- information on R/S care at
of-life. Excluded from the end-of-life
analysis N=235 (72.5%)
N=89 (27.5%)

Patients who had no Patients who had information on R/S

information on R/S care at end-of-life:
care at end-of-life: N=233 (99.2%)
N=2 (0.8%)

Patients who Patients who did not

received R/S care at receive R/S care at
end-of-life end-of-life:
N=92 (39.5%) N =141 (60.5%)

Fig. 1. Flowchart of patients who received R/S care at end of life. R/S ¼ religious/spiritual.
40 Ratshikana-Moloko et al.
2) confidence in the family’s ability to care for the pa-
tient, and 3) the family’s feelings of worry. All answers to
the APCA POS questions are given on a zero to five scale.
For this analysis, zero represents the optimal experience
for patient questions one to three and fam-ily question 10
(worry), and five represents the worst experience
(maximum severity).
The average of the scores was computed for each of the
10 variables and presented as a mean, with SDs. Pa-tients
provided a baseline APCA POS at the initial interview and
at follow-up visits. Whenever a patient died, the most
recently completed APCA POS was designated as the last.
Patients who completed at least two APCA POS are
included in the analysis.
Terminal Illness Understanding
To assess illness understanding, the nurses asked a
question from the U.S. coping with cancer studies
30
(CA106370; principal investigator: Prigerson): How do
you describe your current health status? The response
options were relatively healthy; relatively healthy, but
terminally ill; seriously ill, but not termi-nally ill; and
seriously ill and terminally ill.
Place of Death
In exploring the choice of POD, patients were asked: if
you were dying or at the end of life, where would you
most want to be? At postmortem, caregivers were asked
about the location of death. Possible re-sponses to both
questions were at home, in hospital, at nursing home (step-
down facility), in-patient hos-pice, or other.
R/S Variables
The primary outcome was receipt of R/S care at end of
life. At baseline, nurses asked the patients questions
extracted from the Brief Religious Coping Scale tool
(Kenneth Pargament, Bowling Green, OH) about belief in
31
their God(s), seeking closer connection with their
God(s), feeling abandoned by their God(s), feeling
abandoned by their religious communities/priest, feeling
that cancer is a punish-ment from their God(s), and asking
for forgiveness for their sins. Patients were also asked
about the use of traditional healers and traditional
medicine. Response options for all questions were yes, no,
or not sure. Other spiritual questions (Do you feel your life
is worthwhile?, Do you feel at peace?) were part of the
APCA POS described previously. As part of palliative
care provision, all patients were also asked, Would you
like spiritual support? Response op-tions were yes, no, or
not sure.
The number of spiritual need scores were deter-mined
from the questions: Have you been looking for a stronger
connection with God?, Do you feel abandoned by God?,
Do you feel cancer is God’s way
Vol. 60 No. 1 July 2020
of punishment?, Are you asking for forgiveness of sins?,
Do you feel abandoned by the religious commu-
nity/priests? We assigned a score of one for yes to each of
the questions and zero for no. Two questions were from
the APCA POS; In the last three days, have you felt at
peace?, In the last three days have you felt that life is
worthwhile? We categorized the score zero to three and
four to five and assigned one for scores zero to three and
zero for scores four to five. The scores were added out of a
total of seven. We then cate-gorized number of spiritual
needs into three (zero, one to two, and three and greater).
SCs were recruited from the local communities and
trained in pastoral care, palliative care, and spirituality
(assessment, tools, and planning interventions) in
palliative care. Patients identified as needing R/S care
were followed up by SC, who conducted an R/S
assessment, developed an R/S care plan, and followed
patients up. R/S care in this setting included further
inquiry about patients’ R/S practices, listening to pa-tient’s
stories, reflective listening, counseling, and prayer,
facilitating relationship reconciliation (self, sig-nificant
others, and God/s), referral to place of worship and priests,
and scripture reading. Postmor-tem assessment was used
to confirm the receipt of R/S care in the period before
death.
Other outcomes evaluated were congruence of preferred
with actual POD and the final APCA POS. Family
caregivers were called to confirm the patient’s actual
POD. The final APCA POS was the one completed at the
last palliative care visit.
Analysis
Data were entered into a REDCap database main-tained
in the GCPC at Chris Hani Baragwanath Aca-demic
Hospital. We compared characteristics of patients who
received R/S care at end of life with those who did not.
Differences in sociodemographic factors, clinical factors,
illness understanding, and reli-gious factors were
described and reported using Pear-son Chi-squared test
and Fisher’s exact test for categorical variables. To
compare groups, we used means and SDs with t-tests for
normally distributed variables and medians and
interquartile ranges with signed rank tests for other
continuous variables.
To examine associations of final APCA POS with
receipt of R/S care at end of life, we used multivari-able
logistic regression models. We categorized the APCA
POS into zero to three and four to five. In Model 1, we
adjusted for each final APCA POS co-variate, whereas in
Model 2, we adjusted for age, baseline ECOG PS, illness
understanding, duration from enrollment to death, use of
pain medications, and baseline APCA POS. The analyses
were per-formed using Stata, Version 15 (Stata Corp LP,
Col-lege Station, TX).
Vol. 60 No. 1 July 2020 Advanced Cancer Patients in Soweto, South Africa 41

The study protocol was approved by the Human Results

Research Ethics Committee of the University of Wit-
watersrand (number: M160118; dated February 24, 2016)
and the Institutional Review Board of Columbia
University (Institutional Review Board pro-tocol number:
AAAQ7954; dated March 17, 2016).
Ninety-two patients (39.5%) received R/S care, whereas
141 (60.5%) did not (Table 1). Most patients were black
(90.6%), 73.8% older (50 years and older), and 52.4%
females. The most common cancers were gastrointestinal
or hepatobiliary (40.8%), lung

Table 1
Sociodemographic and Clinical Characteristics of Patients Who Did and Did Not Receive R/S Care
Received R/S Care

Yes No Total

Characteristics N ¼ 92 (%) N ¼ 141 (%) N ¼ 233 P

Age group (yrs) <0.01
Younger than 50 13 (14.1) 48 (34.0) 61 (26.2)
50e69 59 (64.2) 74 (52.5) 133 (57.1)
70 and older 20 (21.7) 19 (13.5) 39 (16.7)
Gender 0.02
Male 35 (38.0) 76 (53.9) 111 (47.6)
Female 57 (62.0) 65 (46.1) 122 (52.4)
Marital status 0.12
Single 23 (25.0) 52 (36.9) 75 (32.2)
Married/partner 40 (43.5) 57 (40.4) 97 (41.6)
Divorced/separated/widowed 29 (31.5) 32 (22.7) 61 (26.2)
Race 0.75
Black 84 (91.3) 127 (90.1) 211 (90.6)
Others 8 (8.7) 14 (9.9) 22 (9.4)
Highest level of education 0.12
No formal education/primary 35 (38.0) 40 (28.4) 75 (32.2)
Completion of high school and 57 (62.0) 101 (71.6) 158 (67.8)
above
Site of primary tumor 0.17
Breast 31 (33.7) 31 (22.0) 62 (26.6)
Lung 25 (27.2) 45 (31.9) 70 (30.0)
GIT/hepatobiliary 35 (38.0) 60 (42.6) 95 (40.8)
a
Others 1 (1.1) 5 (3.5) 6 (2.6)
HIV 0.74
Positive 23 (25.0) 38 (27.0) 61 (26.2)
Negative 69 (75.0) 103 (73.0) 172 (73.8)
ECOG at baseline 0.02
0e2 62 (67.4) 114 (80.9) 176 (75.5)
3e4 30 (32.6) 27 (19.1) 57 (24.5)
Duration from enrollment to
death
Less than one month 26 (28.9) 54 (38.3) 80 (34.6) <0.01
One to three months 22 (24.5) 50 (35.4) 72 (31.2)
Greater than three months to 11 (12.2) 19 (13.5) 30 (13.00
six months
Greater than six months 31 (34.3) 18 (12.8) 49 (21.2)
Median time from enrollment to 83.5 (25e266) 50 (18e97) 57 (21e122) <0.01
death (IQR) in days
Patients’ illness understanding <0.01
Relatively healthy 19 (20.7) 64 (45.4) 83 (35.6)
Relatively healthy but terminally 2 (2.2) 5 (3.5) 7 (3.0)
ill
Seriously ill but not terminally 65 (70.7) 67 (47.5) 132 (56.7)
ill
Seriously and terminally ill 6 (6.5) 5 (3.5) 11 (4.7)
Pain medications according WHO
b
pain ladder
Nonopioids and weak opioids 52 (59.8) 60 (44.4) 112 (50.4) 0.026
Strong opioid 35 (40.2) 75 (55.6) 110 (49.6)
R/S ¼ religious/spiritual; GIT ¼ gastrointestinal; ECOG ¼ Eastern Cooperative Oncology Group; IQR ¼ interquartile range; WHO ¼ World Health Organiza-tion.

Variables significant at P < 0.05 are shown in boldface.

Missing values for covariates were as follows: province of birth (n ¼ 8) and duration from enrollment to death (n ¼ 2).
a
Others ¼ sarcoma.
b
Pain medications: nonopioids (paracetamol, ibuprofen, and diclofenac), weak opioids (tramadol), and strong opioids (morphine).
42 Ratshikana-Moloko et al. Vol. 60 No. 1 July 2020

(30.0%), and breast (26.6%), and 61 patients (26.2%) were
HIV positive. Most patients (176; 75.5%) had ECOG PS
scores of zero to two at enrollment. Older patients and
female patients were more likely than younger or male
patients to have received R/S care. The 11 (4.7%) patients
who acknowledged their serious and terminal illness status
were more likely to have received R/S care than those who
regarded themselves as relatively healthy (70.7% vs.
47.5%; P < 0.01). Median survival time was 57 days
(interquar-tile range 21e122), with patients who received
R/S care more likely to survive longer. Patients who died
within a month were less likely to have received R/S care
(28.9% vs. 38.3%; P < 0.01). Almost all patients (95.3%)
reported pain. Patients who received R/S care were less
likely to receive morphine (40.2% compared with 55.6%;
P ¼ 0.026).
Nearly all patients (97.8%) reported an R/S need and
considered themselves religious or spiritual (94.8%),
believed in God(s) (98.3%), and most were Christians
(85.4%) (Table 2). The most common spiri-tual needs
were seeking a closer connection with their God(s)
(92.6%) and forgiveness for sins (90.8%).
Only 32 (13.7%) acknowledged seeing a traditional healer,
whereas 15 (6.4%) reported using traditional medicines.
Table 3 examines the association between receiving R/S
care and preferred POD. Of the 187 patients with
information on preferred POD and receiving R/S care, 126
(67.3%) patients preferred dying at home, but only 52
(41.3%) achieved a home death. Among patients reporting
home as their preferred POD, pa-tients who received R/S
care were 23 (57.5%) of them who achieved their POD for
home death compared with 29 (33.7%) patients who did
not receive R/S care at end of life (P ¼ 0.012).
One hundred thirty-four patients completed more than
one APCA POS. Of the 134, 44 (32.8%) received R/S care
(Table 4). In comparing baseline and final APCA POS,
patients who received R/S care were more likely to have
less pain (mean 2.82 1.23 vs. 1.93 1.69; P ¼ 0.005) and
less likely to want to share their feelings with their family
(mean 4.43 1.39 vs. 3.77 1.63; P ¼ 0.032). Patients who
did not receive R/S care were more likely to feel that life
was not worth-while (mean 4.59 1.23 vs. 3.68 1.87; P <
0.001) and

Table 2
Association Between Religiousness and Spiritual Care Needs With Receiving R/S Care
Received R/S Care

Yes No Total

Characteristics N ¼ 92 (%) N ¼ 141 (%) N ¼ 233 (%) P

Religion
Christianity 78 (84.8) 121 (85.8) 199 (85.4) 0.28
Traditional/ancestral belief 6 (6.5) 14 (9.9) 20 (8.6)
a
Others 8 (8.7) 6 (4.3) 14 (6.0)
b
R/S (yes) 87 (94.6) 134 (95.0) 221 (94.8) 0.87
b
Believe in God(s) (yes) 89 (96.7) 140 (99.3) 229 (98.3) 0.30
Have been looking for a stronger 85 (95.5) 127 (90.7) 212 (92.6) 0.21
b
connection with God (yes)
Do you feel abandoned by God? 13 (14.6) 14 (10.0) 27 (11.8) 0.29
b
(yes)
Do you feel that cancer is God’s 10 (11.2) 12 (8.6) 22 (9.6) 0.51
b
way of punishment? (yes)
Are you asking for forgiveness of 81 (91.0) 127 (90.7) 208 (90.8) 0.94
b
sins? (yes)
Do you feel abandoned by the 5 (5.6) 2 (1.4) 7 (3.1) 0.11
religious community/priest?
b
(yes)
Number of spiritual needs
0 0 (0.0) 5 (3.6) 5 (2.2) 0.23
1e2 52 (57.8) 82 (58.5) 134 (58.2)
$3 38 (42.2) 53 (37.9) 91 (39.6)
Do you need spiritual care?
No 36 (39.1) 40 (28.4) 76 (32.6) 0.160
Yes 43 (46.8) 71 (50.3) 114 (48.9)
Unknown 13 (14.1) 30 (21.3) 43 (18.5)
Are you seeing a traditional 17 (18.5) 15 (10.6) 32 (13.7) 0.09
b
healer? (yes)
Are you taking traditional 6 (6.5) 9 (6.4) 15 (6.4) 0.97
b
medicine? (yes)
R/S ¼ religious/spiritual.
a
Others (Buddhism, Hinduism, and Islamic).
b
For religiosity variables (yes vs. no and not sure combined).
Vol. 60 No. 1 July 2020 Advanced Cancer Patients in Soweto, South Africa 43

Table 3
Associations Between R/S Care and POD
Preferred POD (Hospital) Preferred POD (Home)

Actual POD (Hospital) Actual POD (Home) Actual POD (Hospital) Actual POD (Home)

Characteristics N ¼ 39 (%) N ¼ 25 (%) P N ¼ 74 (%) N ¼ 52 (%) P

Spiritual care at end of life
a a a a
No 14 (58.3 ) 10 (41.7 ) 0.74 57 (66.3 ) 29 (33.7 ) 0.012
a a
Yes 25 (62.5 ) 15 (37.5 ) 17 (42.5a) 23 (57.5a)
a a a b a b
Total 39 (60.9 ) 25 (39.1 ) 74 (58.7 ) 52 (41.3 )
R/S ¼ religious/spiritual; POD ¼ place of death.
Variable significant at P # 0.05 is shown in boldface.
a
Row percentages are shown.
b
Actual POD missing for one person who preferred to die at home.

more likely to need assistance at end of life than at base-
line (mean 3.33 1.96 vs. 4.10 1.64; P ¼ 0.002).
Table 5 presents the multivariable regression models of
the association of final APCA POS with R/S care. In the
unadjusted model, patients who received R/S care reported
less pain (odds ratio [OR] 0.35; 95% CI 0.15e0.84; P ¼
0.01), whereas their families reported more worry (OR
3.27; 95% CI 1.40e7.67; P ¼ 0.001). On multivariate
logistic regression analysis, adjusting for age, gender,
baseline ECOG, illness understanding, duration from
enrollment to death, pain medications and baseline APCA
POS, and receipt of spiritual care was associated with
reduced pain and family worry (OR 0.33; 95% CI
0.11e0.95; P ¼ 0.04 and OR 3.43; 95% CI 1.10e10.70; P
¼ 0.03, respectively).
Discussion
Among patients with advanced cancer at the end of life
in Soweto, South Africa, receiving R/S care was
associated with age, gender, ECOG PS, patient illness
understanding, duration from enrollment to death, use of
pain medication, and reduction of pain score. Adjusting
for these patient differences, receipt of R/S care was
associated with reduced pain, feeling that life is
worthwhile, and, among pa-tients reporting home as their
preferred POD, achieving home death.
These findings indicate that almost all the patients with
advanced cancer at GCPC had R/S needs and
would benefit from R/S screening, assessment, and care to
4,5,6,16,7e9,12,32,33
improve their QoL. Consis-
tent with previous studies, most patients in the pre-sent
5,10,6,33
study considered themselves religious and spiritual,
were seeking a closer connection with their God(s), and
10,11
were asking for forgiveness for their sins. According
6
to Astrow et al., among 727 patients with cancer in the
U.S., 92% were reli-gious, 59% considered themselves
spiritual, and 79% had at least one spiritual need, slightly
lower than our study. A large proportion (92.6%) of pa-
tients in our study expressed a need for a closer
connection with their God(s) and a need for forgive-ness
10
of sins, compared with what Alcorn et al. in the U.S.
found; 53% seeking closer connection with a God/s and
47% seeking forgiveness. Most pa-tients with cancer
appear to regard R/S issues as
important and to want their physicians to address R/S
4,11,14,9,12,34,35
needs. The R/S care that was pro-
vided in our setting was aligned with interventions
17
recommended by Puchalski et al.
Older patients and females in our study, like in other
studies in Greece and sub-Saharan Africa, were more
likely than younger patients and males to receive R/S
care.
35,36
These findings support the notion that as people
36
age, they increasingly value spirituality.
Few patients in our study acknowledged the termi-nal
nature of their illness, perhaps because their doc-tors did
not tell them how serious their illness was, or because they
feared that acknowledging that they were terminal would
indicate a lack of faith, or because they were unaware of
30
how close to death they were. How-ever, patients who
acknowledged being terminally ill were more likely to
receive R/S care, which suggests that prognostic
awareness may improve end-of-life care not just because
of advance care planning and receipt of comfort care, but
because it increases the likelihood that they will get R/S
care.
Being at peace and having no pain at end of life are
2,3,10,13,14
important for patients, and peace and feeling that
2,35
life is worthwhile are aspects of spiritual-ity. Selman et
2
al. reported that palliative care pa-tients in South Africa
and Uganda strongly valued harmonious relationships
with friends and family and with God/s and ancestors.
Patients in our study maintained high levels of peace
throughout the course of their illness, perhaps because
most of them were spiritual and religious, few felt
abandoned by their God(s) or their religious communities/
clergy, and most felt that their R/S needs were being met.
This is despite the fact that almost all patients in our study
had an R/S need. In a meta-analysis pool-ing of 32,000
patients from different countries, pa-tients who felt
abandoned by their God(s) or
44 Ratshikana-Moloko et al. Vol. 60 No. 1 July 2020

Table 4
Changes From Baseline to Last APCA POS Among Patients Who Received and Did Not Receive R/S Care
Received R/S Care

Yes No

N ¼ 44 N ¼ 90
APCA POS Baseline APCA Final APCA P Baseline APCA Final APCA P

Pain
Mean SD 2.82 1.23 1.93 1.69 0.005 2.93 1.44 2.62 1.73 0.133
Median (IQR) 3 (2e3.5) 2 (0e3) 0.012 3 (2e5) 3 (2e4) 0.137
Other symptoms
Mean SD 1.89 1.66 1.34 1.61 0.142 2.00 1.74 1.83 1.80 0.523
Median (IQR) 2 (0e3) 0 (0e3) 0.196 2 (0e3) 2 (0e3) 0.397
Worried
Mean SD 2.41 1.73 2.36 1.88 0.907 2.49 1.96 2.41 1.90 0.764
Median (IQR) 3 (0.5e4) 3 (0e4) 0.837 3 (0e4) 3 (0e4) 0.928
Able to share feelings
Mean SD 4.43 1.39 3.77 1.63 0.032 3.99 1.92 3.71 1.90 0.331
Median (IQR) 5 (5e5) 4.5 (3e5) 0.007 5 (4e5) 5 (3e5) 0.158
Worthwhile
Mean SD 4.41 1.34 4.02 1.47 0.220 4.59 1.23 3.68 1.87 <0.001
Median (IQR) 5 (5e5) 5 (3e5) 0.166 5 (5e5) 5 (3e5) <0.001
Peace
Mean SD 4.20 1.49 3.93 1.28 0.383 4.02 1.55 3.59 1.72 0.066
Median (IQR) 5 (4e5) 5 (3e5) 0.130 5 (3e5) 4.5 (3e5) 0.054
Assistance
Mean SD 3.23 1.85 3.82 1.85 0.103 3.33 1.96 4.10 1.64 0.002
Median (IQR) 3 (2e5) 5 (3e5) 0.077 3 (4e5) 5 (4e5) 0.004
Family information
Mean SD 4.16 1.19 4.26 1.26 0.741 4.34 1.29 4.32 1.25 0.888
Median (IQR) 5 (3e5) 5 (4e5) 0.523 5 (4e5) 5 (4e5) 0.656
Family confidence
Mean SD 4.67 0.75 4.77 0.68 0.472 4.67 0.99 4.67 1.05 1.000
Median (IQR) 5 (5e5) 5 (5e5) 0.676 5 (5e5) 5 (5e5) 0.852
Family worried
Mean SD 4.05 1.48 4.47 0.88 0.129 3.45 1.79 3.39 1.77 0.811
Median (IQR) 5 (3e5) 5 (4e5) 0.402 4 (3e5) 4 (2.5e5) 0.453

APCA POS ¼ African Palliative Care Association Palliative care Outcome Scale (0e5); R/S ¼ religious/spiritual; IQR ¼ interquartile range.
Variables significant at P < 0.05 are shown in boldface.
Analysis is limited to patients who completed $2 APCA questionnaires.

religious communities felt more depressed and were in
36,37
pain for long periods.
Among patients on pain medication, those who received
R/S care were less likely to be on morphine.
Patients who did not receive R/S care may have had
unresolved R/S needs that exacerbated their pain,
requiring morphine. Spiritual problems may aggra-vate
physical pain and need to be addressed as part

Table 5
Multivariate Logistic Regression Models of Associations of Final APCA POS With R/S Care at End of Life
Spiritual Care at End of Life
a b
Model 1 Model 2
Final APCA POS OR (95% CI) P OR (95% CI) P
Pain 0.35 (0.15e0.84) 0.01 0.33 (0.11e0.95) 0.04
Other symptoms 0.85 (0.68e1.05) 0.12 0.85 (0.68e1.05) 0.13
Worried 0.99 (0.81e1.20) 0.89 0.99 (0.82e1.20) 0.91
Able to share feelings 1.02 (0.83e1.25) 0.85 1.01 (0.83e1.24) 0.89
Life worthwhile 1.13 (0.91e1.40) 0.28 1.15 (0.92e1.43) 0.23
Peace 1.15 (0.91e1.47) 0.23 1.15 (0.90e1.47) 0.25
Assistance 0.91 (0.74e1.12) 0.38 0.91 (0.74e1.13) 0.40
Family information 0.96 (0.72e1.29) 0.88 0.97 (0.72e1.31) 0.86
Family confidence 1.13 (0.74e1.75) 0.55 1.21 (0.77e1.90) 0.41
Family worried 3.27 (1.40e7.67) 0.001 3.43 (1.10e10.70) 0.03
APCA POS ¼ African Palliative Care Association Palliative care Outcome Scale; R/S ¼ religious/spiritual; OR ¼ odds ratio.
a
Model 1 (unadjusted).
b
Model 2, adjusting for age, gender, baseline Eastern Cooperative Oncology Group, illness understanding, duration from enrollment to death, pain medications, and baseline
APCA POS.
Vol. 60 No. 1 July 2020 Advanced Cancer Patients in Soweto, South Africa
of pain management. Consistent with other studies, our
study found that patients who received R/S care had less
15,23,38,39
pain than others. Among Afri-can American
40
patients with cancer in Atlanta (U.S.), Bai et al. reported
that spirituality was pro-tective against pain and symptom
38
burden, whereas Yeager et al. reported that African
American pa-tients with cancer used faith and prayer to
control pain and other symptoms. In our study, most
patients who used morphine did not receive R/S care.
Whether R/S care influenced the need for pain medication
in our patients remains a question. Some studies have
36,37
found no association between spir-ituality and pain.
More research to identify spe-cific R/S care associated
with pain alleviation in a broader population is needed.
Previous studies have found receiving R/S care to be
associated with feeling that life was worthwhile.
7,24
Among patients with breast cancer in Southern Thailand,
41
Phenwan et al. reported that being at peace with self and
others and having family support were associated with
2,35
feeling that life is worthwhile, whereas Selman et al.
described a similar concept, Ubuntu (connectedness),
common within the Afri-can culture. At their final APCA
POS, patients who did not receive R/S care were less
likely to feel that life is worthwhile than they did at
baseline, perhaps because they had lost hope and had
failed to seek, and therefore to receive, care for their
spiritual needs. However, patients who received R/S care
were less likely to share their feelings with their fam-ily.
23
According to Murray et al., when comparing pa-tients
from Scotland and Kenya, Kenyan patients were less
likely to communicate their feelings with family as they
considered themselves a burden to their families.
Similarly, patients in our study might have kept things to
themselves to protect their fam-ilies. Further research into
how not sharing feelings with family relates to R/S care
among African pa-tients is required.
Previous studies confirm that most patients prefer to die
21,22
at home, but only a few achieve a home death. Of the
90% who preferred home death in a study in the U.S., only
23
22.5% died at home. Dying in a hospital or a facility has
32
been associated with poor QoL. Dying at home when
home was the preferred POD was associated with
receiving R/S care in our study, perhaps because patients
did not feel abandoned by their religious commu-
nities/clergy. Previous studies confirm that family
members, community, and faith groups provide R/ S care
23
to their patients in their communities. How-ever, not all
patients prefer a home death. Among patients referred to
specialist palliative care clinic in the U.K., 60% preferred
to die in a hospice compared with 37% who preferred
42
home. In the
45
same study, patients who had a previous hospice
admission were more likely than others to prefer to die in
a hospice. Thus, the choice of POD may be influenced by
knowledge and availability of end-of-life facilities. In
South Africa, most patients do not have access to in-
patient hospice units. How-ever, among palliative care
patients in Soweto, R/S care may have helped to make
home care more sup-portive and to attend to patient
preferences for re-maining at home.
Our study has several strengths. It is a prospective
longitudinal study that used validated tools adminis-tered
by trained palliative care nurses. The study also has
limitations. As an observational study, it cannot
demonstrate causality between R/S care and improving
pain and POD. Concepts of R/S were not separated, and
most patients use the terms inter-changeably. Spirituality
among Africans goes beyond what was covered in the
study, for example, some South African patients have
ancestral beliefs and rit-uals, which are not covered in this
study, and will require tools that are tailored for the local
context. The location of the hospital influenced the
popula-tion studied, which is predominantly African and
Christian. These results can thus not be generalized to
other populations.
Conclusions
To the best of our knowledge, this study is the first to
assess the R/S needs and R/S care provided to pa-tients
with advanced cancer who received palliative care in
Soweto, South Africa. We found that most pa-tients
experience R/S needs. Furthermore, those who received
R/S care had less physical pain, used less morphine, and
had higher odds of dying at home where they wished than
those who did not. Future research is needed to confirm
and extend these results beyond the palliative care setting,
and to determine the mechanisms by which R/S care im-
proves the observed patient outcomes.
Disclosures and Acknowledgments
This work was supported by research grants from the
National Cancer Institute of U.S. awarded to Drs.
Jacobson, Joffe, Neugut, and Ruff (R01 CA192627); Drs
Emerson and Ruff (P30 CA013696-41S4) (Suba-ward no.
1: [GG010416-62]); Drs Abate-Shen and Blanchard (P30
CA013696-43S4) (Subaward no. 3: [GG010416-BI]); and
Dr. Prigerson (R35 CA197730; RO1 CA106370); the
South African Medical Research Council/University of the
Witwatersrand Common Epithelial Cancer Research
Centre awarded to Dr. Ruff and a 2018 Conquer Cancer
Foundation Young
46 Ratshikana-Moloko et al.
Investigator Award to Dr. O’Neil; as well as the Bristol-
Myers Squibb Foundation Secure the Future Cancer
Program.
Spiritual Care counselors were supported by a global
grant no. GG1531 from Rotary Club Rosebank, South
Africa, South Africa and Rotary Club Hatfield in United
Kingdom.
The authors declare no conflicts of interest.
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