Jpn J Clin Oncol 2014;44(8)705– 710 doi:10.1093/jjco/hyu070 Advance Access Publication 27 May 2014
Original Articles
The Behavior of Turkish Cancer Patients in Fasting During the Holy Month of Ramadan Faruk Tas*, Senem Karabulut, Rumeysa Ciftci, Ibrahim Yildiz, Serkan Keskin, Leyla Kilic and Rian Disci
*For reprints and all correspondence: Faruk Tas, Istanbul Universitesi, Onkoloji Enstitusu, Capa, Istanbul 34390, Turkey. E-mail: [email protected] Received March 16, 2014; accepted April 29, 2014
Objective: Fasting during the holy month of Ramadan is one of the major obligations for all adult Muslims. We performed a survey of Turkish Muslim cancer patients to examine the extent of their fasting status and to compare various clinical characteristics of fasting and non-fasting cancer patients during the month of Ramadan. Methods: This study was conducted on 701 adult cancer patients who attended ambulatory patient care units answered the questionnaires. Results: The population comprised 445 women (63.5%), and the median age was 54 years. Before diagnosis of cancer, 93.1% of the patients used fast consists of completely (78.3%) and partial (14.8%). However, 15% of cases were fasting on the day of interview, either partially (7.4%) or completely (7.6%) with equal distributions. Patients who were females, those with good performance status, those without any comorbid disease, who had non-metastatic disease, those with history of surgery, those treated with radiotherapy and those being treated with oral chemotherapeutic agents were more likely to be fasting than others. The fasting ones had more prevalent among patients with lymphoma, urogenital cancer and breast cancer; conversely, the rate of fasting status among patients with lung and gastrointestinal cancer was quite low. Only 20.8% of all patients asked their physician whether it was alright for them to fast and physicians generally had a negative attitude towards fasting (83.2%). Conclusions: Majority of cancer patients are not fasting during the month of Ramadan, and a small part of patients consult this situation to their physician. Key words: cancer patients – fasting – Ramadan – Turkish – Muslim
INTRODUCTION Fasting during the holy month of Ramadan, one of the lunar month of the Islamic calendar, is one of the major obligations for all adult Muslims. It involves refrain from eating, drinking and sexual intercourse to achieve self-control and body purification. Because Muslims fast from sunrise to sunset daily during the month of Ramadan, the length of fasting time varies with the geographical location of the country and the season in which it falls. Therefore, it may vary from 10 to 19 h a day. During this month, usually two meals are eaten per day. The first meal, called iftar, might be taken immediately after sunset. Before dawn, people wake up to have a meal called
sahur to prepare them for fasting. So, lifestyle and circadian rhythms change during Ramadan (1 – 4). The chronically ill patients are also exempted from fasting during among other reasons according to the Islamic rules. Similar to most of the other major chronic diseases, cancer is also progressive, serious, irreversible and primarily dependent on diet and lifestyle factors and is relatively difficult to address effectively with drug treatment. However, Islam forbids fasting if this would be harmful to the individual, practiced oncologists in this world are faced with a difficult and annoying problem. Despite the existence of limitations which adversely affect health and ongoing therapy, some cancer
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Institute of Oncology, University of Istanbul, Istanbul, Turkey
706
Fasting in Turkish cancer patients
PATIENTS AND METHODS STUDY POPULATION AND PROCEDURES This study was conducted on adult (18 years of age or older) patients diagnosed with malignant disease at the Department of Medical Oncology at the Institute of Oncology, University of Istanbul. Patients who were in a preterminal state or too ill to complete the interview were excluded. Patients were asked to complete the questionnaire immediately after their scheduled visits. All potentially eligible patients attending the clinics were chosen and assessed consecutively. Interviews took place during the month of Ramadan of 2012, between 19 July 2012 and 18 August 2012. The questionnaires were handed out to the patients by their physician on arrival at the hospital as outpatients. The majority of the interviews were self-administered, but they were occasionally face to face. It was explained to the patients that all information offered would be treated confidentially, and that refusal to participate in the study would not in any way jeopardize the care and treatment they would receive in the hospital. Informed consent was obtained from all patients, and the study was reviewed by a local ethical committee. It was carried out in compliance with the rules of good clinical practice and the ethical principles of Declaration of Helsinki. DEFINITION OF FASTING Patients were considered completely fasting (all days), partial fasting (at least 1 day) or non-fasting (never day) for current and former situation. For logistic regression analyses, we used the fasting and non-fasting patients. QUESTIONNAIRE The questionnaire was designed to evaluate the patients’ status of fasting. Patients were asked whether they were fasting on the day of the interview, the regularity of fasting. It consisted
of multiple-choice questions, but the patients were allowed to add further comments. The questionnaire was structured to the details pertaining to fasting among our patients, as well as patient – physician relations. The participating physicians reported the medical characteristics and details of treatment for all patients who were admitted and treated in our clinic during the specified time periods. Medical data included diagnosis, date of diagnosis, stage at diagnosis, performance status, current or previous specific anticancer treatment modalities and current disease status. STATISTICAL ANALYSIS Data analysis was performed using SPSS software (SPSS, Chicago, IL, USA). Fasting person was defined as those who reported fast of at least 1 day. For all statistical analyses, a two-sided P value of 0.05 was considered statistically significant. Comparisons between the distribution of variables in fasting and non-fasting were assessed by x 2 test. Logistic regression analysis was used to analyze potential variables that may have independently influenced the fasting status. The fasting and non-fasting status before and after the diagnosis of the cancer was compared using McNemar’s test. FINAL STUDY POPULATION Of a total of 750 cancer patients who were invited to participate in the study, 701 (93.5%) accepted and answered the questionnaire. Forty-nine patients did not give information on whether or not they fast and therefore they were excluded from the analysis.
RESULTS The study population comprised 445 women (63.5%) and 256 men (36.5%), in total 701 cases. The median age was 54 years; ranging between 18 and 90 (Table 1). Majority of the patients were females (63.5%) and had a good performance status (0 and 1) (81.6%). Almost half of the patients had nonmetastatic disease (52.5%). Of the subjects, minority (26.1%) had evidence of other concomitant disease in the descending order of frequency of diseases of cardiovascular system (15.1%), metabolic and endocrine system (10.6%) and pulmonary system (4%). The most common diagnosis was breast cancer (32.7) followed by colorectal cancer (17.3%) and lung cancer (10%). FORMERLY AND CURRENT FASTING STATUS Before diagnosis of cancer, only 48 (6.9%) patients did not fast at all during the month of Ramadan, majority of the patients, 653 (93.1%) used fast consists of completely (n ¼ 549, 78.3%) and partial (n ¼ 105, 14.8%) fasting. However, only minority of them, 105 (15%) participants were fasting experience on the day of interview, either partial or complete
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patients are found to obey their religious custom of fasting during Ramadan (1 –4). The number of Muslims worldwide exceeds 1.5 billion, constituting .20% of the population in the world (3). Therefore, Muslims have a significant part of the 10.9 million cancer cases diagnosed yearly worldwide. This situation leads to a serious conclusion: many Muslim cancer patients experience the fasting month of Ramadan, but we do not know which individual elect to fast and influencing factors. Unfortunately, related studies are particularly lacking in other parts of the world (3). Because 4.6% of Muslim population live in Turkey and account for 98.6% of all Turkish population, we, therefore, performed a survey of Turkish Muslim cancer patients to examine the extent of their fasting status and to compare various clinical characteristics of fasting and non-fasting cancer patients during the month of Ramadan.
Jpn J Clin Oncol 2014;44(8)
Table 1. Patient characteristics Characteristics Age (years) median (range)
707
Table 1. Continued n (%)
Characteristics
54 (18–90)
n (%)
Testis cancer
15 (2.1)
,54
361 (51.5)
Esophagus cancer
14 (2.0)
.55
340 (48.5)
GIST
13 (1.9)
Gender
12 (1.7)
256 (36.5)
Melanoma
11 (1.6)
Female
445 (63.5)
Cervical cancer
10 (1.4)
Performance status
Endometrial cancer
8 (1.1)
0
337 (48.1)
Hepatocellular cancer
8 (1.1)
1
235 (33.5)
Pancreas cancer
8 (1.1)
2
101 (14.4)
Bladder cancer
8 (1.1)
3
26 (3.7)
Soft tissue sarcoma
6 (0.9)
4
2 (0.3)
Mesothelioma
6 (0.9)
Prostate cancer
4 (0.6)
Stage of disease Non-metastatic
368 (52.5)
Kaposi sarcoma
4 (0.6)
Metastatic
333 (47.5)
Ewing sarcoma
4 (0.6)
a
Comorbidity
Others
No
518 (73.9)
Yes
183 (26.1)
Cardiovascular system
106 (15.1)
19 (2.7)
a
Hypertension
82 (11.7)
Coronary artery disease
15 (2.1)
Congestive heart failure Metabolic and endocrine system
9 (1.3) 74 (10.6)
Diabetes mellitus
61 (8.7)
Thyroid disorders
13 (1.9)
Pulmonary system
Thymoma (n ¼ 3), osteosarcoma (n ¼ 3), GBM (n ¼ 2), non-GBM brain cancer (n ¼ 2), cholangiocarcinoma (n ¼ 2), tuba cancer (n ¼ 2), vaginal cancer (n ¼ 1), PNET (n ¼ 1) and multiple primary cancers (n ¼ 4) [breast and endometrial cancer (n ¼ 2), breast and pancreatic cancer (n ¼ 1) and colon and non-Hodgkin lymphoma (n ¼ 1)]. CVA, cerebrovascular accident; GIST, gastrointestinal stromal tumor; GBM, glioblastoma multiforme; PNET, primitive neuroectodermal tumor
Table 2. Fasting status of patients Yes, completely n (%)
28 (4.0)
Chronic obstructive pulmonary disease
14 (2.0)
Bronchial asthma
14 (2.0)
Do you fast now?
18 (2.6)
Did you fast formerly?
Others Chronic renal failure
6 (0.9)
CVA
2 (0.3)
Comorbidity
Multiple
No, never n (%)
53 (7.6)
52 (7.4)
596 (85.0)
549 (78.3)
104 (14.8)
48 (6.9)
10 (1.4)
Hepatic cirrhosis
Single
Yes, partially n (%)
145 (20.7) 38 (5.4)
with equal distributions (7.4 and 7.6%, respectively) (P , 0.001) (Table 2). Otherwise, 596 (85%) patients did not fast at all. After diagnosis of cancer, all non-fasting patients included (n ¼ 48, 100%) former non-fasting patients, 94.3% (n ¼ 99) of partial fasting patients and 82% (n ¼ 450) of completely fasting patients.
Types of cancer Breast
229 (32.7)
Colorectal cancer
121 (17.3)
Lung cancer
70 (10.0)
Ovarian cancer
47 (6.7)
Stomach cancer
44 (6.3)
Lymphoma
21 (3.0)
Head and neck
18 (2.6) Continued
VARIABLES AFFECTING FASTING STATUS Table 3 shows the relationship between potential patient, disease and treatment-related variables and the fasting status. The fasting patients were younger than others (P ¼ 0.013), and the females were more in number than males (P , 0.001). Similarly, the patients with non-metastatic cancer (P , 0.001) and good performance status (PS 0 and 1) (P , 0.001) were more common in the fasting group. While the patients with
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Renal cell cancer
Male
708
Fasting in Turkish cancer patients
COOPERATION BETWEEN PATIENTS AND PHYSICIAN Cooperation between patients and their physicians concerning fasting status was weak (Table 6). Only 20.8% of all patients asked their physicians whether it was alright for them to fast and no difference was determined between fasting and nonfasting patients (81.9 versus 78.7%, respectively, P ¼ 0.455). When asked, physicians generally had a negative attitude towards fasting (83.2%). Of the patients whose oncologists discouraged fasting, the effect of physicians’ advice was prominent on the non-fasting patients compared with fasting patients (85.0 versus 59.9%, respectively, P ¼ 0.012).
DISCUSSION One of the most surprising findings was the behavioral change observed in the patients who preferred to not fast after the diagnosis of cancer. While the rate of fasting was 93.1%
Table 3. Comparison of fasting status of patients compared with various clinical parameters Parameter
Fasting n (%)
No fasting n (%)
No. of patients
105 (15.0)
596 (85.0)
,54
64 (61.0)
297 (49.8)
.55
41 (39.0)
299 (50.2)
Male
27 (25.7)
229 (38.4)
Female
78 (74.3)
367 (61.6)
P value
Age 0.013
Gender ,0.001
Stage of disease Non-metastatic
78 (74.3)
290 (48.7)
Metastatic
27 (25.7)
306 (51.3)
0 –1
99 (94.3)
473 (79.4)
2 –4
6 (5.7)
123 (20.6)
No
86 (81.9)
432 (72.5)
Yes
19 (18.1)
164 (27.5)
16 (84.2)
129 (78.7)
3 (15.8)
35 (21.3)
,0.001
Performance status ,0.001
Comorbidity 0.043
Type of comorbidity Single Multiple
0.790
History of surgery Yes
79 (75.2)
384 (64.4)
No
26 (24.8)
212 (35.6)
Yes
49 (46.7)
205 (34.4)
No
56 (53.3)
391 (65.6)
0.031
History of radiotherapy 0.016
History of chemotherapy Yes
66 (62.9)
492 (82.6)
No
39 (37.1)
104 (17.4)
Single agent
34 (51.5)
167 (33.9)
Combination
32 (48.5)
326 (66.1)
Intravenous
35 (53.0)
371 (75.3)
Oral
31 (47.0)
122 (24.7)
,0.001
Type of chemotherapy 0.005
Route of chemotherapy ,0.001
among our patients before the diagnosis of cancer, the corresponding rate was 15% after the diagnosis of the cancer. 83.9% of patients who had been previously fasting currently do not fast. When the reason for which the patients who had been previously fasting stopped to fast was questioned, they reported that they did not fast because according to Islamic rules, they could not fast due to their severe, chronic, progressed and fatal disease. According to Islamic rules, young children up to the age of puberty, the women with menstruation, breast-feeding
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various comorbid diseases were less than others in the fasting group (P ¼ 0.043), we found no effect of the extension of comorbidity on cancer patients (P ¼ 0.79). However, all of the mentioned variables (age, gender, stage, performance status and comorbidity) were not different between fasting and nonfasting patients before diagnosis of cancer. The patients with history of previous or current administration of surgery (P ¼ 0.031) and radiotherapy (P ¼ 0.016) showed a significant correlation with fasting status, more prevalent in the fasting group (Table 3). Contrarily, the patients underwent and/or undergoing chemotherapy were less fasting compared with the patients without chemotherapy (P , 0.001). Furthermore, patients with treated single-agent versus combination chemotherapy (P ¼ 0.005) and particularly those with treated with oral agents versus intravenous and other route of chemotherapy (P , 0.001) had a higher propensity for fasting status (Table 3). Compared with non-fasting patients, the fasting ones had more prevalent among patients with malignant lymphoma (P , 0.001), urogenital cancer (P ¼ 0.002) and breast cancer (P ¼ 0.06) (Table 4). Conversely, the rate of fasting status among patients with lung (P ¼ 0.007) and gastrointestinal cancer (P ¼ 0.004) was quite low. Other tumors consist of gynecologic, head and neck, sarcoma and skin cancer were not associated with fasting status (P . 0.05). Table 5 depicts the final logistic regression model predicting status of fasting. The subsequent multivariate model includes all of the patient, disease and medical variables that were found statistically significant in the univariate analysis. It showed that patients who were females (P ¼ 0.021), those with good performance status (0 and 1) (P ¼ 0.034), those without any comorbid disease (P ¼ 0.011), who had nonmetastatic disease (P ¼ 0.007), those with history of surgery (P ¼ 0.007), those treated with radiotherapy (P ¼ 0.029) and those being treated with oral chemotherapeutic agents (P ¼ 0.002) were more likely to be fasting than other patients.
Jpn J Clin Oncol 2014;44(8)
Table 4. Analysis of cancer types affecting on fasting Cancer
Rate of fasting (%)
Odds ratio
Total
15.00
1
95% CI
709
Table 6. Collaboration between patients’ fasting status and his/her doctor P value
n (%) Consultation with doctor about fasting
,0.001
Lymphoma
47.62
5.160
2.137–12.458
Urogenital
35.00
3.056
1.545–6.046
0.002
Yes
146 (20.8)
No
555 (79.2)
Breast
20.52
1.466
1.000–2.148
0.06
Head and neck
11.76
0.756
0.171–3.359
0.982
Do not fast
Gynecologic
If yes, what is his/her reaction? 119 (83.2)
0.651
0.290–1.463
0.387
You may fast
8 (5.6)
2.74
0.160
0.038–0.662
0.007
As you want
19 (13.3)
Gastrointestinal
5.08
0.304
0.155–0.593
0.004
Table 5. Influence of factors that were statistically significant patients’ fasting status Variable
Odds ratio
95% CI
P value
Female
2.41
1.14– 5.07
0.021
Male
1
1.10– 12.39
0.034
1.25– 5.83
0.011
1.24– 3.93
0.007
1.28– 4.90
0.007
1.07– 3.28
0.029
1.41– 4.85
0.002
Gender
Performance status 0– 1
3.70
2– 4
1
Comorbidity No
2.71
Yes
1
Stage of disease Non-metastatic
2.20
Metastatic
1
History of surgery Yes
2.50
No
1
History of radiotherapy Yes
1.87
No
1
Route of chemotherapy Oral
2.62
Intravenous and others
1
women, travelers, elderly people and the patients with chronic diseases could not fast during the month of Ramadan (1 – 4). Other important factor that caused the patients to stop fasting was the fear that fasting state would lead to a decrease in the actual performance, preventing the administration of the therapy and leading to the disease progression. Furthermore, these patients stated that fear that their health will worsen in the absence of appropriate and timely administration of the drug. In a study, during the month of Ramadan, severe changes of
homeostatic functions occurred and catabolic conditions with serious weight loss were observed (5). In another study, it was reported that fasting state caused hypohydration and energy loss due to both fasting and the lack of fluid intake, resulting in a decrease of overall performance, especially the exercise performance (6). The fact that the patients who had been completely fasting before the disease more commonly fasted after the disease compared with the patients who had been partially fasting before the disease could be related to the belief that the God will show more mercy to him/her if he/she fasts and that fasting will lead to the deprivation of the cancer cells. In addition, these patients were told that, even in the presence of the disease, leaving the habitudes that they were following for many years was difficult and they would fast as long as they tolerate. It was seen that the young patients more commonly fasted compared with the older patients. Because most common comorbidities were diagnosed in elderly population, the older patients who suffered these diseases should follow a life style change, diet and exercise, which are accepted as indispensable parts of the therapy and these patients could not fast due to above-mentioned reasons. Approximately one-quarter of our patients had comorbid diseases, and one of the most common comorbid diseases was diabetes mellitus. In these patients, it is recommended that eating less and frequent food in multiple meals set forth to prevent the complications of hypoglycemia and hyperglycemia. These patients could not fast because disease regulation is impaired due to increased food intake of two meals, iftar and sahur. It was stated that increased plasma blood glucose levels were observed during the fasting state and was associated with poor control of the diabetes, and combined with other reasons, it led to an impaired lipid profile (7). In terms of types of cancer and its effect on fasting, we found that the patients with lymphoma and urogenital tumor significantly were fasting more commonly, whereas the patients with gastrointestinal tumor and lung cancer were significantly not fasting. The patients with lymphoma and urogenital tumor (most commonly testicular tumor) had a good PS, were young and had curable disease in the off-treatment follow-up, and consequently they could fast. On the other hand, the patients with gastrointestinal system tumor and lung cancer did not fast because they were more symptomatic, had malnutrition and were receiving continuous intravenous
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10.29
Lung
710
Fasting in Turkish cancer patients
fasting state. As a result, the question ‘May I fast?’ posed by a cancer patient is difficult to answer for an oncologist. Most ideally, this decision should be taken by medical oncologist, psychiatrist and local religious official, altogether, and a consensus should be achieved among these groups. Mosque imams can play a major role in advising patients and should be educated on this subject (1 – 3,8). A similar study was conducted on 102 in- and out-patients with solid and hematologic cancer in Egypt that 60% of the patients fasted during the month of Ramadan (3). Using multivariate analysis, the factors that influenced fasting status of the cancer patients during the month of Ramadan in Egypt were determined to be female gender, good PS and being an outpatient. In our patient group, in addition to the these factors that affect the Egyptian patients, the absence of comorbidity, the presence of non-metastatic disease, the previous administration of radiotherapy and surgery and the administration of oral chemotherapy were found to be other significant effective factors in the multivariate analysis. While 46% of the Egyptian cancer patients consulted the doctor about fasting, this rate was as lower as 20.8% in our patient population. The marked differences of these rates in the two countries could have resulted from the differences of social status, behavior and thoughts and, finally, from the ability to give up the traditions. In conclusion, in Turkey as a Muslim country, majority of cancer patients are not fasting during the month of Ramadan and a small part of patients consult this situation to their physician. Oncologists should be aware of Ramadan and determine fasting practices among their Muslim patients to detect potential complications originating from this practice. Both physician and mosque imam can play a major role in advising cancer patients and should be educated on this subject.
Conflict of interest statement None declared.
References 1. Tazi I. Ramadan and cancer. J Clin Oncol 2008;26:5485. 2. Panju ZI. Patients who fast in Ramadan need better advice. BMJ 2012;345:e4754. 3. Zeeneldin AA, Taha FM. Fasting among Muslim cancer patients during the holy month of Ramadan. Ann Saudi Med 2012;32:243– 9. 4. Shehab A, Abdulle A, El Issa A, Al Suwaidi J, Nagelkerke N. Favorable changes in lipid profile: the effect of fasting after Ramadan. PLoS ONE 2012;7:e47615. 5. Iraki L, Bogdan A, Hakkou F, Amrani N, Abkari A, Touitou Y. Ramadan diet restrictions modify the circadian time structure in humans: a study on plasma gastrin, insulin, glucose, and calcium and gastric PH. J Clin Endocrinol Metab 1997;82:1261 –73. 6. Sarraf-Zadegan N, Atashi M, Naderi GA, et al. The effect of fasting in Ramadan on values and interrelations between biochemical, coagulation and hematological factors. Ann Saudi Med 2000;20:377–81. 7. Ziaee V, Razaei M, Ahmadinejad Z, et al. The changes of metabolic profile and weight during Ramadan fasting. Singapore Med J 2006;47:409–14. 8. Iqbal F. What should doctors do about fasting during Ramadan? BMJ 2012;345:e5629.
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chemotherapy. Likewise, it was seen that the patients who have previously undergone surgery and radiotherapy more commonly fast compared with the patients who have not. It may be explained by the fact that these patients were earlystage patients, without disease or who have been followed-up without therapy. These data support the finding that the patients with early disease significantly more commonly fasted compared with the patients with metastatic disease. In order to evaluate the correlation between chemotherapy and fasting status, the first of three parameters examined was the fact that the patients who did not receive chemotherapy significantly more commonly fasted compared with those who received chemotherapy. The patients who did not receive chemotherapy were in the follow-up period. These patients had very early stage who had never received an adjuvant therapy or those with good PS and non-metastatic disease who had received adjuvant therapy. The second parameter was the type of the chemotherapy. The patients treated with single-agent chemotherapy more commonly fasted compared with those treated with multiple-agent chemotherapy because the former showed better PS and earlier stage of disease compared with latter patients. In addition, the patients treated with multiple agents had more problems of compliance, had more difficulty to tolerate the therapy and had more commonly toxicity, and thereby, these cases had decreased tolerance against long-term fasting and they could not fast. The last parameter examined for the chemotherapy was the administration route of the chemotherapy. It was seen that the patients who received oral chemotherapy could fast for more days compared with those who received intravenous chemotherapy because these patients could receive their therapy during the two time intervals between sahur and iftar and they could fast. When the contents of the oral therapies taken by these patients, the drugs taken were adjuvant drugs with relatively less toxicity given during the early-stage diseases, rather than oral therapies taken by the patients with metastatic disease and these drugs were mostly hormonal. Another surprising finding is that there is a poor cooperation between the patient and the doctor about fasting, and that 83.2% of the recommendations given by the doctor was in favor of non-fasting. It was found that this recommendation did not have an effect on fasting state of the patient, and the patients who respected to the recommendations of the doctor showed significantly non-fasting state. It was seen that this recommendation was done especially to the patients with a high tumor burden with a high likelihood of tumor lysis syndrome, to the patients who were using nephrotoxic drugs among the chemotherapeutics and to the patients who were using the drugs that commonly lead to the events such as vomiting and diarrhea. This is because that the combination of these drugs and the dehydration due to fasting increases the risk for renal failure (5,6). Another factor that concerns the doctor is the likelihood that the preventive effects of the therapy disappear because the patient discontinues or decreases the curative therapy thinking that it prevents the
Original Articles
The Behavior of Turkish Cancer Patients in Fasting During the Holy Month of Ramadan Faruk Tas*, Senem Karabulut, Rumeysa Ciftci, Ibrahim Yildiz, Serkan Keskin, Leyla Kilic and Rian Disci
*For reprints and all correspondence: Faruk Tas, Istanbul Universitesi, Onkoloji Enstitusu, Capa, Istanbul 34390, Turkey. E-mail: [email protected] Received March 16, 2014; accepted April 29, 2014
Objective: Fasting during the holy month of Ramadan is one of the major obligations for all adult Muslims. We performed a survey of Turkish Muslim cancer patients to examine the extent of their fasting status and to compare various clinical characteristics of fasting and non-fasting cancer patients during the month of Ramadan. Methods: This study was conducted on 701 adult cancer patients who attended ambulatory patient care units answered the questionnaires. Results: The population comprised 445 women (63.5%), and the median age was 54 years. Before diagnosis of cancer, 93.1% of the patients used fast consists of completely (78.3%) and partial (14.8%). However, 15% of cases were fasting on the day of interview, either partially (7.4%) or completely (7.6%) with equal distributions. Patients who were females, those with good performance status, those without any comorbid disease, who had non-metastatic disease, those with history of surgery, those treated with radiotherapy and those being treated with oral chemotherapeutic agents were more likely to be fasting than others. The fasting ones had more prevalent among patients with lymphoma, urogenital cancer and breast cancer; conversely, the rate of fasting status among patients with lung and gastrointestinal cancer was quite low. Only 20.8% of all patients asked their physician whether it was alright for them to fast and physicians generally had a negative attitude towards fasting (83.2%). Conclusions: Majority of cancer patients are not fasting during the month of Ramadan, and a small part of patients consult this situation to their physician. Key words: cancer patients – fasting – Ramadan – Turkish – Muslim
INTRODUCTION Fasting during the holy month of Ramadan, one of the lunar month of the Islamic calendar, is one of the major obligations for all adult Muslims. It involves refrain from eating, drinking and sexual intercourse to achieve self-control and body purification. Because Muslims fast from sunrise to sunset daily during the month of Ramadan, the length of fasting time varies with the geographical location of the country and the season in which it falls. Therefore, it may vary from 10 to 19 h a day. During this month, usually two meals are eaten per day. The first meal, called iftar, might be taken immediately after sunset. Before dawn, people wake up to have a meal called
sahur to prepare them for fasting. So, lifestyle and circadian rhythms change during Ramadan (1 – 4). The chronically ill patients are also exempted from fasting during among other reasons according to the Islamic rules. Similar to most of the other major chronic diseases, cancer is also progressive, serious, irreversible and primarily dependent on diet and lifestyle factors and is relatively difficult to address effectively with drug treatment. However, Islam forbids fasting if this would be harmful to the individual, practiced oncologists in this world are faced with a difficult and annoying problem. Despite the existence of limitations which adversely affect health and ongoing therapy, some cancer
# The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
Downloaded from http://jjco.oxfordjournals.org/ at Robertson Library University of prince Edward Island on March 2, 2015
Institute of Oncology, University of Istanbul, Istanbul, Turkey
706
Fasting in Turkish cancer patients
PATIENTS AND METHODS STUDY POPULATION AND PROCEDURES This study was conducted on adult (18 years of age or older) patients diagnosed with malignant disease at the Department of Medical Oncology at the Institute of Oncology, University of Istanbul. Patients who were in a preterminal state or too ill to complete the interview were excluded. Patients were asked to complete the questionnaire immediately after their scheduled visits. All potentially eligible patients attending the clinics were chosen and assessed consecutively. Interviews took place during the month of Ramadan of 2012, between 19 July 2012 and 18 August 2012. The questionnaires were handed out to the patients by their physician on arrival at the hospital as outpatients. The majority of the interviews were self-administered, but they were occasionally face to face. It was explained to the patients that all information offered would be treated confidentially, and that refusal to participate in the study would not in any way jeopardize the care and treatment they would receive in the hospital. Informed consent was obtained from all patients, and the study was reviewed by a local ethical committee. It was carried out in compliance with the rules of good clinical practice and the ethical principles of Declaration of Helsinki. DEFINITION OF FASTING Patients were considered completely fasting (all days), partial fasting (at least 1 day) or non-fasting (never day) for current and former situation. For logistic regression analyses, we used the fasting and non-fasting patients. QUESTIONNAIRE The questionnaire was designed to evaluate the patients’ status of fasting. Patients were asked whether they were fasting on the day of the interview, the regularity of fasting. It consisted
of multiple-choice questions, but the patients were allowed to add further comments. The questionnaire was structured to the details pertaining to fasting among our patients, as well as patient – physician relations. The participating physicians reported the medical characteristics and details of treatment for all patients who were admitted and treated in our clinic during the specified time periods. Medical data included diagnosis, date of diagnosis, stage at diagnosis, performance status, current or previous specific anticancer treatment modalities and current disease status. STATISTICAL ANALYSIS Data analysis was performed using SPSS software (SPSS, Chicago, IL, USA). Fasting person was defined as those who reported fast of at least 1 day. For all statistical analyses, a two-sided P value of 0.05 was considered statistically significant. Comparisons between the distribution of variables in fasting and non-fasting were assessed by x 2 test. Logistic regression analysis was used to analyze potential variables that may have independently influenced the fasting status. The fasting and non-fasting status before and after the diagnosis of the cancer was compared using McNemar’s test. FINAL STUDY POPULATION Of a total of 750 cancer patients who were invited to participate in the study, 701 (93.5%) accepted and answered the questionnaire. Forty-nine patients did not give information on whether or not they fast and therefore they were excluded from the analysis.
RESULTS The study population comprised 445 women (63.5%) and 256 men (36.5%), in total 701 cases. The median age was 54 years; ranging between 18 and 90 (Table 1). Majority of the patients were females (63.5%) and had a good performance status (0 and 1) (81.6%). Almost half of the patients had nonmetastatic disease (52.5%). Of the subjects, minority (26.1%) had evidence of other concomitant disease in the descending order of frequency of diseases of cardiovascular system (15.1%), metabolic and endocrine system (10.6%) and pulmonary system (4%). The most common diagnosis was breast cancer (32.7) followed by colorectal cancer (17.3%) and lung cancer (10%). FORMERLY AND CURRENT FASTING STATUS Before diagnosis of cancer, only 48 (6.9%) patients did not fast at all during the month of Ramadan, majority of the patients, 653 (93.1%) used fast consists of completely (n ¼ 549, 78.3%) and partial (n ¼ 105, 14.8%) fasting. However, only minority of them, 105 (15%) participants were fasting experience on the day of interview, either partial or complete
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patients are found to obey their religious custom of fasting during Ramadan (1 –4). The number of Muslims worldwide exceeds 1.5 billion, constituting .20% of the population in the world (3). Therefore, Muslims have a significant part of the 10.9 million cancer cases diagnosed yearly worldwide. This situation leads to a serious conclusion: many Muslim cancer patients experience the fasting month of Ramadan, but we do not know which individual elect to fast and influencing factors. Unfortunately, related studies are particularly lacking in other parts of the world (3). Because 4.6% of Muslim population live in Turkey and account for 98.6% of all Turkish population, we, therefore, performed a survey of Turkish Muslim cancer patients to examine the extent of their fasting status and to compare various clinical characteristics of fasting and non-fasting cancer patients during the month of Ramadan.
Jpn J Clin Oncol 2014;44(8)
Table 1. Patient characteristics Characteristics Age (years) median (range)
707
Table 1. Continued n (%)
Characteristics
54 (18–90)
n (%)
Testis cancer
15 (2.1)
,54
361 (51.5)
Esophagus cancer
14 (2.0)
.55
340 (48.5)
GIST
13 (1.9)
Gender
12 (1.7)
256 (36.5)
Melanoma
11 (1.6)
Female
445 (63.5)
Cervical cancer
10 (1.4)
Performance status
Endometrial cancer
8 (1.1)
0
337 (48.1)
Hepatocellular cancer
8 (1.1)
1
235 (33.5)
Pancreas cancer
8 (1.1)
2
101 (14.4)
Bladder cancer
8 (1.1)
3
26 (3.7)
Soft tissue sarcoma
6 (0.9)
4
2 (0.3)
Mesothelioma
6 (0.9)
Prostate cancer
4 (0.6)
Stage of disease Non-metastatic
368 (52.5)
Kaposi sarcoma
4 (0.6)
Metastatic
333 (47.5)
Ewing sarcoma
4 (0.6)
a
Comorbidity
Others
No
518 (73.9)
Yes
183 (26.1)
Cardiovascular system
106 (15.1)
19 (2.7)
a
Hypertension
82 (11.7)
Coronary artery disease
15 (2.1)
Congestive heart failure Metabolic and endocrine system
9 (1.3) 74 (10.6)
Diabetes mellitus
61 (8.7)
Thyroid disorders
13 (1.9)
Pulmonary system
Thymoma (n ¼ 3), osteosarcoma (n ¼ 3), GBM (n ¼ 2), non-GBM brain cancer (n ¼ 2), cholangiocarcinoma (n ¼ 2), tuba cancer (n ¼ 2), vaginal cancer (n ¼ 1), PNET (n ¼ 1) and multiple primary cancers (n ¼ 4) [breast and endometrial cancer (n ¼ 2), breast and pancreatic cancer (n ¼ 1) and colon and non-Hodgkin lymphoma (n ¼ 1)]. CVA, cerebrovascular accident; GIST, gastrointestinal stromal tumor; GBM, glioblastoma multiforme; PNET, primitive neuroectodermal tumor
Table 2. Fasting status of patients Yes, completely n (%)
28 (4.0)
Chronic obstructive pulmonary disease
14 (2.0)
Bronchial asthma
14 (2.0)
Do you fast now?
18 (2.6)
Did you fast formerly?
Others Chronic renal failure
6 (0.9)
CVA
2 (0.3)
Comorbidity
Multiple
No, never n (%)
53 (7.6)
52 (7.4)
596 (85.0)
549 (78.3)
104 (14.8)
48 (6.9)
10 (1.4)
Hepatic cirrhosis
Single
Yes, partially n (%)
145 (20.7) 38 (5.4)
with equal distributions (7.4 and 7.6%, respectively) (P , 0.001) (Table 2). Otherwise, 596 (85%) patients did not fast at all. After diagnosis of cancer, all non-fasting patients included (n ¼ 48, 100%) former non-fasting patients, 94.3% (n ¼ 99) of partial fasting patients and 82% (n ¼ 450) of completely fasting patients.
Types of cancer Breast
229 (32.7)
Colorectal cancer
121 (17.3)
Lung cancer
70 (10.0)
Ovarian cancer
47 (6.7)
Stomach cancer
44 (6.3)
Lymphoma
21 (3.0)
Head and neck
18 (2.6) Continued
VARIABLES AFFECTING FASTING STATUS Table 3 shows the relationship between potential patient, disease and treatment-related variables and the fasting status. The fasting patients were younger than others (P ¼ 0.013), and the females were more in number than males (P , 0.001). Similarly, the patients with non-metastatic cancer (P , 0.001) and good performance status (PS 0 and 1) (P , 0.001) were more common in the fasting group. While the patients with
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Renal cell cancer
Male
708
Fasting in Turkish cancer patients
COOPERATION BETWEEN PATIENTS AND PHYSICIAN Cooperation between patients and their physicians concerning fasting status was weak (Table 6). Only 20.8% of all patients asked their physicians whether it was alright for them to fast and no difference was determined between fasting and nonfasting patients (81.9 versus 78.7%, respectively, P ¼ 0.455). When asked, physicians generally had a negative attitude towards fasting (83.2%). Of the patients whose oncologists discouraged fasting, the effect of physicians’ advice was prominent on the non-fasting patients compared with fasting patients (85.0 versus 59.9%, respectively, P ¼ 0.012).
DISCUSSION One of the most surprising findings was the behavioral change observed in the patients who preferred to not fast after the diagnosis of cancer. While the rate of fasting was 93.1%
Table 3. Comparison of fasting status of patients compared with various clinical parameters Parameter
Fasting n (%)
No fasting n (%)
No. of patients
105 (15.0)
596 (85.0)
,54
64 (61.0)
297 (49.8)
.55
41 (39.0)
299 (50.2)
Male
27 (25.7)
229 (38.4)
Female
78 (74.3)
367 (61.6)
P value
Age 0.013
Gender ,0.001
Stage of disease Non-metastatic
78 (74.3)
290 (48.7)
Metastatic
27 (25.7)
306 (51.3)
0 –1
99 (94.3)
473 (79.4)
2 –4
6 (5.7)
123 (20.6)
No
86 (81.9)
432 (72.5)
Yes
19 (18.1)
164 (27.5)
16 (84.2)
129 (78.7)
3 (15.8)
35 (21.3)
,0.001
Performance status ,0.001
Comorbidity 0.043
Type of comorbidity Single Multiple
0.790
History of surgery Yes
79 (75.2)
384 (64.4)
No
26 (24.8)
212 (35.6)
Yes
49 (46.7)
205 (34.4)
No
56 (53.3)
391 (65.6)
0.031
History of radiotherapy 0.016
History of chemotherapy Yes
66 (62.9)
492 (82.6)
No
39 (37.1)
104 (17.4)
Single agent
34 (51.5)
167 (33.9)
Combination
32 (48.5)
326 (66.1)
Intravenous
35 (53.0)
371 (75.3)
Oral
31 (47.0)
122 (24.7)
,0.001
Type of chemotherapy 0.005
Route of chemotherapy ,0.001
among our patients before the diagnosis of cancer, the corresponding rate was 15% after the diagnosis of the cancer. 83.9% of patients who had been previously fasting currently do not fast. When the reason for which the patients who had been previously fasting stopped to fast was questioned, they reported that they did not fast because according to Islamic rules, they could not fast due to their severe, chronic, progressed and fatal disease. According to Islamic rules, young children up to the age of puberty, the women with menstruation, breast-feeding
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various comorbid diseases were less than others in the fasting group (P ¼ 0.043), we found no effect of the extension of comorbidity on cancer patients (P ¼ 0.79). However, all of the mentioned variables (age, gender, stage, performance status and comorbidity) were not different between fasting and nonfasting patients before diagnosis of cancer. The patients with history of previous or current administration of surgery (P ¼ 0.031) and radiotherapy (P ¼ 0.016) showed a significant correlation with fasting status, more prevalent in the fasting group (Table 3). Contrarily, the patients underwent and/or undergoing chemotherapy were less fasting compared with the patients without chemotherapy (P , 0.001). Furthermore, patients with treated single-agent versus combination chemotherapy (P ¼ 0.005) and particularly those with treated with oral agents versus intravenous and other route of chemotherapy (P , 0.001) had a higher propensity for fasting status (Table 3). Compared with non-fasting patients, the fasting ones had more prevalent among patients with malignant lymphoma (P , 0.001), urogenital cancer (P ¼ 0.002) and breast cancer (P ¼ 0.06) (Table 4). Conversely, the rate of fasting status among patients with lung (P ¼ 0.007) and gastrointestinal cancer (P ¼ 0.004) was quite low. Other tumors consist of gynecologic, head and neck, sarcoma and skin cancer were not associated with fasting status (P . 0.05). Table 5 depicts the final logistic regression model predicting status of fasting. The subsequent multivariate model includes all of the patient, disease and medical variables that were found statistically significant in the univariate analysis. It showed that patients who were females (P ¼ 0.021), those with good performance status (0 and 1) (P ¼ 0.034), those without any comorbid disease (P ¼ 0.011), who had nonmetastatic disease (P ¼ 0.007), those with history of surgery (P ¼ 0.007), those treated with radiotherapy (P ¼ 0.029) and those being treated with oral chemotherapeutic agents (P ¼ 0.002) were more likely to be fasting than other patients.
Jpn J Clin Oncol 2014;44(8)
Table 4. Analysis of cancer types affecting on fasting Cancer
Rate of fasting (%)
Odds ratio
Total
15.00
1
95% CI
709
Table 6. Collaboration between patients’ fasting status and his/her doctor P value
n (%) Consultation with doctor about fasting
,0.001
Lymphoma
47.62
5.160
2.137–12.458
Urogenital
35.00
3.056
1.545–6.046
0.002
Yes
146 (20.8)
No
555 (79.2)
Breast
20.52
1.466
1.000–2.148
0.06
Head and neck
11.76
0.756
0.171–3.359
0.982
Do not fast
Gynecologic
If yes, what is his/her reaction? 119 (83.2)
0.651
0.290–1.463
0.387
You may fast
8 (5.6)
2.74
0.160
0.038–0.662
0.007
As you want
19 (13.3)
Gastrointestinal
5.08
0.304
0.155–0.593
0.004
Table 5. Influence of factors that were statistically significant patients’ fasting status Variable
Odds ratio
95% CI
P value
Female
2.41
1.14– 5.07
0.021
Male
1
1.10– 12.39
0.034
1.25– 5.83
0.011
1.24– 3.93
0.007
1.28– 4.90
0.007
1.07– 3.28
0.029
1.41– 4.85
0.002
Gender
Performance status 0– 1
3.70
2– 4
1
Comorbidity No
2.71
Yes
1
Stage of disease Non-metastatic
2.20
Metastatic
1
History of surgery Yes
2.50
No
1
History of radiotherapy Yes
1.87
No
1
Route of chemotherapy Oral
2.62
Intravenous and others
1
women, travelers, elderly people and the patients with chronic diseases could not fast during the month of Ramadan (1 – 4). Other important factor that caused the patients to stop fasting was the fear that fasting state would lead to a decrease in the actual performance, preventing the administration of the therapy and leading to the disease progression. Furthermore, these patients stated that fear that their health will worsen in the absence of appropriate and timely administration of the drug. In a study, during the month of Ramadan, severe changes of
homeostatic functions occurred and catabolic conditions with serious weight loss were observed (5). In another study, it was reported that fasting state caused hypohydration and energy loss due to both fasting and the lack of fluid intake, resulting in a decrease of overall performance, especially the exercise performance (6). The fact that the patients who had been completely fasting before the disease more commonly fasted after the disease compared with the patients who had been partially fasting before the disease could be related to the belief that the God will show more mercy to him/her if he/she fasts and that fasting will lead to the deprivation of the cancer cells. In addition, these patients were told that, even in the presence of the disease, leaving the habitudes that they were following for many years was difficult and they would fast as long as they tolerate. It was seen that the young patients more commonly fasted compared with the older patients. Because most common comorbidities were diagnosed in elderly population, the older patients who suffered these diseases should follow a life style change, diet and exercise, which are accepted as indispensable parts of the therapy and these patients could not fast due to above-mentioned reasons. Approximately one-quarter of our patients had comorbid diseases, and one of the most common comorbid diseases was diabetes mellitus. In these patients, it is recommended that eating less and frequent food in multiple meals set forth to prevent the complications of hypoglycemia and hyperglycemia. These patients could not fast because disease regulation is impaired due to increased food intake of two meals, iftar and sahur. It was stated that increased plasma blood glucose levels were observed during the fasting state and was associated with poor control of the diabetes, and combined with other reasons, it led to an impaired lipid profile (7). In terms of types of cancer and its effect on fasting, we found that the patients with lymphoma and urogenital tumor significantly were fasting more commonly, whereas the patients with gastrointestinal tumor and lung cancer were significantly not fasting. The patients with lymphoma and urogenital tumor (most commonly testicular tumor) had a good PS, were young and had curable disease in the off-treatment follow-up, and consequently they could fast. On the other hand, the patients with gastrointestinal system tumor and lung cancer did not fast because they were more symptomatic, had malnutrition and were receiving continuous intravenous
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10.29
Lung
710
Fasting in Turkish cancer patients
fasting state. As a result, the question ‘May I fast?’ posed by a cancer patient is difficult to answer for an oncologist. Most ideally, this decision should be taken by medical oncologist, psychiatrist and local religious official, altogether, and a consensus should be achieved among these groups. Mosque imams can play a major role in advising patients and should be educated on this subject (1 – 3,8). A similar study was conducted on 102 in- and out-patients with solid and hematologic cancer in Egypt that 60% of the patients fasted during the month of Ramadan (3). Using multivariate analysis, the factors that influenced fasting status of the cancer patients during the month of Ramadan in Egypt were determined to be female gender, good PS and being an outpatient. In our patient group, in addition to the these factors that affect the Egyptian patients, the absence of comorbidity, the presence of non-metastatic disease, the previous administration of radiotherapy and surgery and the administration of oral chemotherapy were found to be other significant effective factors in the multivariate analysis. While 46% of the Egyptian cancer patients consulted the doctor about fasting, this rate was as lower as 20.8% in our patient population. The marked differences of these rates in the two countries could have resulted from the differences of social status, behavior and thoughts and, finally, from the ability to give up the traditions. In conclusion, in Turkey as a Muslim country, majority of cancer patients are not fasting during the month of Ramadan and a small part of patients consult this situation to their physician. Oncologists should be aware of Ramadan and determine fasting practices among their Muslim patients to detect potential complications originating from this practice. Both physician and mosque imam can play a major role in advising cancer patients and should be educated on this subject.
Conflict of interest statement None declared.
References 1. Tazi I. Ramadan and cancer. J Clin Oncol 2008;26:5485. 2. Panju ZI. Patients who fast in Ramadan need better advice. BMJ 2012;345:e4754. 3. Zeeneldin AA, Taha FM. Fasting among Muslim cancer patients during the holy month of Ramadan. Ann Saudi Med 2012;32:243– 9. 4. Shehab A, Abdulle A, El Issa A, Al Suwaidi J, Nagelkerke N. Favorable changes in lipid profile: the effect of fasting after Ramadan. PLoS ONE 2012;7:e47615. 5. Iraki L, Bogdan A, Hakkou F, Amrani N, Abkari A, Touitou Y. Ramadan diet restrictions modify the circadian time structure in humans: a study on plasma gastrin, insulin, glucose, and calcium and gastric PH. J Clin Endocrinol Metab 1997;82:1261 –73. 6. Sarraf-Zadegan N, Atashi M, Naderi GA, et al. The effect of fasting in Ramadan on values and interrelations between biochemical, coagulation and hematological factors. Ann Saudi Med 2000;20:377–81. 7. Ziaee V, Razaei M, Ahmadinejad Z, et al. The changes of metabolic profile and weight during Ramadan fasting. Singapore Med J 2006;47:409–14. 8. Iqbal F. What should doctors do about fasting during Ramadan? BMJ 2012;345:e5629.
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chemotherapy. Likewise, it was seen that the patients who have previously undergone surgery and radiotherapy more commonly fast compared with the patients who have not. It may be explained by the fact that these patients were earlystage patients, without disease or who have been followed-up without therapy. These data support the finding that the patients with early disease significantly more commonly fasted compared with the patients with metastatic disease. In order to evaluate the correlation between chemotherapy and fasting status, the first of three parameters examined was the fact that the patients who did not receive chemotherapy significantly more commonly fasted compared with those who received chemotherapy. The patients who did not receive chemotherapy were in the follow-up period. These patients had very early stage who had never received an adjuvant therapy or those with good PS and non-metastatic disease who had received adjuvant therapy. The second parameter was the type of the chemotherapy. The patients treated with single-agent chemotherapy more commonly fasted compared with those treated with multiple-agent chemotherapy because the former showed better PS and earlier stage of disease compared with latter patients. In addition, the patients treated with multiple agents had more problems of compliance, had more difficulty to tolerate the therapy and had more commonly toxicity, and thereby, these cases had decreased tolerance against long-term fasting and they could not fast. The last parameter examined for the chemotherapy was the administration route of the chemotherapy. It was seen that the patients who received oral chemotherapy could fast for more days compared with those who received intravenous chemotherapy because these patients could receive their therapy during the two time intervals between sahur and iftar and they could fast. When the contents of the oral therapies taken by these patients, the drugs taken were adjuvant drugs with relatively less toxicity given during the early-stage diseases, rather than oral therapies taken by the patients with metastatic disease and these drugs were mostly hormonal. Another surprising finding is that there is a poor cooperation between the patient and the doctor about fasting, and that 83.2% of the recommendations given by the doctor was in favor of non-fasting. It was found that this recommendation did not have an effect on fasting state of the patient, and the patients who respected to the recommendations of the doctor showed significantly non-fasting state. It was seen that this recommendation was done especially to the patients with a high tumor burden with a high likelihood of tumor lysis syndrome, to the patients who were using nephrotoxic drugs among the chemotherapeutics and to the patients who were using the drugs that commonly lead to the events such as vomiting and diarrhea. This is because that the combination of these drugs and the dehydration due to fasting increases the risk for renal failure (5,6). Another factor that concerns the doctor is the likelihood that the preventive effects of the therapy disappear because the patient discontinues or decreases the curative therapy thinking that it prevents the
