Motives for Medical Tourism Amongst Cancer Patients in Oman: A Perspective From Patient’s Point of View

Background: Traveling abroad to seek an opinion about diagnosis or treatment is a common practice in medicine, especially in the field of oncology. In Oman, patients diagnosed with cancer frequently travel with their families to seek an opinion, sometimes even before consulting a medical/surgical oncologist at home. The purpose of this study was to report and study the prevalence and motives of medical tourism amongst patients diagnosed to have cancer in Oman. Methods: A cross sectional, retrospective study involving patients admitted to the medical oncology unit at the Sultan Qaboos University Hospital was conducted. Patients with a biopsy-proven cancer who were admitted to the wards and the day-care unit between October 2016 and March 2017 were invited to participate. A semi-structured interview consisting of 3 parts was used to obtain information on demographics, motives and satisfaction with travel. Results: Of the 100 patients who were invited, a total of 64 patients participated in the study and completed the questionnaire. Of these 64 subjects, 24 (38%) traveled abroad to seek a second opinion. The primary reasons for traveling abroad to seek a second opinion were as follows: poor perception about health care in Oman (31%), expectations of a better healthcare overseas (12%), dissatisfaction with the communication or explanation by the healthcare providers in Oman, or concerns about delay in treatment (24%), and societal pressures (33%). Conclusion: A significant proportion of patients traveled abroad to seek a second opinion after getting a diagnosis of cancer, main reasons being societal pressures, dissatisfaction with the communication, or concerns of delay in initiating treatment in Oman.


INTRODUCTION
Medical tourism is defined as "a set of activities in which a person travels, often long distance or across the border, to avail medical services with direct or indirect engagement in leisure, business or other purposes." i There are several reasons for medical tourism, and seeking a second opinion to confirm the diagnosis, especially of a life-threatening disease, or to explore treatment options is one of the most common. Seeking a second opinion is a common practice in medical field in patients with cancer. Sometimes the treating oncologist may seek an opinion from a specialist or expert in the field, especially in case of a rare or uncommon tumor 2 . In such cases, second opinion is doctor-initiated, usually for the review of pathological specimens or imaging studies. Up to 98% of physicians support the idea of seeking second opinions in case of rare cancer or uncertain diagnoses, as this may enhance patient satisfaction and improve quality of care. Almost two-thirds of physicians encouraged patients to seek second opinions to avoid fallacious diagnosis or treatment ii Less often, it is the patient who opts to seek a second opinion, especially when confronted with a life-threatening disease, such as cancer, and the possibility of complicated treatment. iii For example, in one study, more than 55% of cancer survivors obtained a second opinion regarding their treatment. iv On the other hand, oncologists report that they provided second opinion for 1-5 patients per month, to those who sought an opinion, as the patients either needed additional information or reassurance. v Although the reasons for doctor-initiated second opinion seeking are well known, the reasons for patient initiated second opinion are not always clear. There are very few reports to study the motives of seeking second opinions in cancer patients. Different reasons have been reported, the most common being to search for more information related to treatment, dissatisfaction with the information given by the first medical oncologist, and/or a lack of proper communication. vi For example, in one series, a number of patients were concerned about the communication with their first doctor and needed additional information and reassurance. 4 Several factors lead the patients to travel abroad in Oman, including a delay in presenting to the general practitioner and the delay in consulting a specialist due to perceived long waiting times. vii With the ease of travel, availability of resources, and marketing of foreign healthcare institutions, there is an increasing tendency for patients seeking a second opinion to travel overseas 7 . Once abroad, the consultation may go beyond seeking an opinion. A recently reported study from Oman suggested that amongst the patients who travelled, 85% received treatment, 10% travelled for treatment and tourism and 2.5% travelled abroad for general checkup. viii Seeking a second opinion by traveling overseas is fraught with several issues which could affect the outcomes of cancer, such as delay in treatment due to travel arrangements and seeking appointments 9 . Moreover, patients abroad usually will be seen there for a short period of time, so follow-up care is missed and possible complications or side effects of treatment will not be noted by the treating doctor. ix To seek a proper opinion, patients must be aware of the centers of excellence for different types of cancer. x If not guided properly, patients may choose a place for seeking second opinion without proper facilities and expertise, hence, negatively affecting their health 11 . For example, a study showed that the risk of in-hospital complications for "heavy doctor-shoppers" was significantly higher than that for patients who were not. xi Of the 1,358 newly diagnosed patients with colorectal cancer, the risk of in-hospital complications for heavy doctor-shoppers was significantly higher than no doctor-shoppers, however, the risk was significantly lower for the heavy "hospital-shoppers", suggesting that selection of right hospital was important rather than random choice. In Oman, it has been observed frequently that cancer patients seek a second opinion, and often travel abroad even before seeking opinion from an oncologist within the country 7,8,10 . The purpose of this study was to determine the prevalence of cancer patients who travel abroad to seek a second opinion, and to study their motives.

Patients and Study Design
A cross sectional, retrospective study was performed involving patients admitted to the medical oncology unit at the Sultan Qaboos University Hospital (SQUH). A semi-structured interview consisting of close and open-ended questions was conducted which provided opportunity for the researcher to interview the patients directly in order to explore the opinions and the thoughts of the patients regarding complex and sensitive issues. The study was conducted on patients either admitted to the wards or attending the day-care unit between the October 2016 and March 2017.. Consecutive patients more than 18 years of age and a histologically proven diagnosis of cancer were informed of the study and required to sign a written informed consent. The study was approved by the institutional ethics review committee.
The interview had three parts. The first part was related to socio-demographic background of patients, and part of the information, such as, histological diagnosis and date of diagnosis were obtained from the electronic health records. The second and the third part involved documenting motives for seeking a second opinion, consisting of both the close-ended and open-ended questions.
For those who sought a second opinion, further questions were asked about their satisfaction with the process.

Statistical Methodology
The responses to the close-ended and open-ended questions were reviewed, and the two authors categorized them independently into major categories. Following a discussion, wherever needed, the individual responses were allocated to one of the four major themes that emerged. This was a descriptive study. Results are expressed as numbers and percentages.

RESULTS
Over the study period, a total of 100 consecutive patients admitted to the in-patient wards or attending the day care unit for treatment were invited to participate in the study, of whom 64 patients either agreed to participate or were eligible or agreed to participate in the study. The reasons for exclusion were: untreated brain metastasis (n=7) with an inability of patients to respond coherently; advanced stage of the disease preventing the patient from being interviewed (n=11); sepsis precluding the patient to be interviewed (n=6); refusal to participate in the study (n=10) and age of less than 18 (n=2). Of the 64 patients who agreed to participate, 24 (37.5%) patients travelled abroad to seek a second opinion.
Demographic data of the participants is summarized in Table 1. The median age was 45 years, and 69% were females, 59% were unemployed and 64% had a high school education or higher. The monthly family income of 69% of the patient was less than 1000 Omani rials (1 OR=2.60US$), and 68% had a family size of more than 6 members. Thirty-two patients (50%) had a diagnosis of breast cancer, whereas 22% of patients had colon cancer, or less commonly, sarcoma, lymphoma, head and neck cancer, testicular cancer, cancers of the stomach, pancreas, uterus or the uterine cervix (18%) Table 2 compares the demographic characteristics of those who did and those who did not seek a second opinion. On a univariate analysis, there was no statistically significant difference between age, gender, residence, occupation, level of education, socio-economic status, family size, marital status, and the underlying diagnosis. Figure 1 describes the motives of 24 patients who travelled abroad to seek a second opinion. Thirtyone percent of the patients or their family members travelled abroad to seek a second opinion, because of a poor perception about health care in Oman, whereas 12% thought that although the health services in Oman met their expectations, the outcomes of cancer will be better if they got the opinion or treatment overseas. Twenty-four percent patients travelled abroad to seek a second opinion because they were not satisfied with the communication or explanation by the healthcare providers in Oman or thought that there might be a delay in initiating treatment in Oman. On the other hand, 33% patients travelled abroad because of societal pressures. The details are shown in Table 3. Table 4 shows that 67% patients traveled to India, and the others to Thailand, almost 80% paid out of their own pocket, 42% patients received not only an opinion and consultation, but also received part or entire treatment while abroad, but only 25% were satisfied with their decision and the outcome, and only 37% would recommend others to travel to the same place as these patients did in the first place.

DISCUSSION
To the best of our knowledge, this is the first study from Oman and Arabian gulf countries describing the motives of cancer patients traveling abroad to seek a second opinion after getting diagnosis of cancer in the country of origin. Thirty-eight percent of the patients travelled abroad to seek a second opinion, with the majority within the first month of getting the diagnosis. The study employed a semi-structured face-to-face interview with the patients, as this method of data collection provides the chance to clarify the questions being asked to an audience with different and varied level of education. Open-ended questions may identify areas of concern, that were not considered by the researcher. Close-ended questions allow the patients to focus and explore their ideas about common reasons of seeking second opinion. Hence, both types of questions were employed in the interview to seek reliable qualitative data. xii A similar survey of patients with advanced stage cancer to elicit the reasons for medical tourism was reported from Australia. 6 Out of 1892 new patients, 123 (6.5%) agreed that they sought a second opinion, 22 declined to participate, and another 24 did not fill the questionnaire. Of the 101 evaluable patients, only 77 completed a questionnaire. The majority (77%) were women. The reasons for seeking a second opinion were to obtain more information about treatment (70%), reassurance about diagnosis and treatment (61%), and dissatisfaction by the information given by the first medical oncologist (31%).
In Oman, healthcare is free for the Omani nationals, and expatriate workers with contracts. The WHO ranked Oman's healthcare system as 8 th best among all the 191 member states on the basis of several healthcare related factors. xiii Harvard University and other joint commissioned organizations appreciated Oman's healthcare achievements and considered it as a model for other countries. xiv This study attempts to address the important question, why more than 1/3 rd of cancer patients chose to travel abroad, mostly on their own expenses.
Usually, second opinion means seeking of an opinion from second health professional of the same specialty as the one who has already given opinion. Most patients in our series had not seen a surgical or a medical oncologist in Oman, and preferred to travel abroad by themselves, to seek the opinion of an oncologist abroad. The breakdown in communication or a lack of trust may have occurred at a primary or secondary healthcare level, but this remains speculative and need to be studied systematically.
Lack of communication and trust in health care was found to be the most common reason for seeking a second opinion in the several studies. 5, xv A study aimed to elicit experiences of patients attending the Sydney Cancer Center reported 123/1892 (6.5%) of patents sought a second opinion. The majority were educated young women. The main motive to seek the second opinion was the need for detailed information to reach satisfaction, validation or reassurance about the first consultation. Besides communication skills, personal characteristics of the physician, was the other strong motive which influenced the patients to seek a second opinion in that study 6 .
In a different study setting, Al Hinai et al. interviewed 45 patients who had travelled abroad for treatment 8 . The vast majority of patients had diseases related to bone and joints. Thailand was the most popular destination, and 85% of patients traveled for treatment only, 10% for treatment and tourism. Interestingly, 15% traveled abroad without first seeking medical care locally, and the reasons for this remain speculative. Almost 75% patients received information about the foreign center for treatment abroad from a friend.
This study showed that the most common factor which influenced the Omani patients to travel abroad to seek an opinion and many times before seeking an oncologist's opinion in Oman, was the family and societal pressure. This could be attributed to the family structure in Oman which consists of large and extended families. Family members not only participate in decision making in routine issues, but also when it comes to health-related issues of an individual. This observation has been reported from a study of multi-ethnic patient population during critical care where the families considered it their responsibility to figure out whether the right medical care was offered to the patient or not, so they seek a second opinion. xvi In the study from Australia, Philip also identified that 70% of the patients were encouraged to seek a second opinion by family and friends, amongst many other reasons.
High expectation of patients on the health care outside the county one of the most motives for seeking a second opinion. A questionnaire based study by University of Hong Kong to determine the behaviors of seeking a second opinion in gynecologic cancer patients reported that 41.9% patients had consulted other health care professionals for a second opinion after their diagnosis. xvii Patients who thought they will receive better health care elsewhere and who were concerned about their current intervention were reported to be more likely to seek a second opinion than other patients. This observation was predicted in several studies determining the primary reasons to seek a second opinion is to find other and new treatment options, however many of them planned to return back to the first oncologist. xviii Moreover, department of surgical oncology in Netherlands reported that 68% of patients sought a second opinion, hoping it will be different from the first. 11 There are some limitations of the study. Firstly, the study was carried out in one cancer center. The university hospital is a tertiary referral center and receives cancer patients from all over the country. It is clear from table 1, that almost 45% patients came from outside the two most populous governates, whereas, another 45% came from the less populous governates. Hence, the patients interviewed in the university hospital may represent a good case distribution. Secondly, the semi-structured interview depended on the recall, and hence may be subjected to recall bias. However, the patients were interviewed, and wherever, appropriate the family members also participated in the discussion. Furthermore, participation of a family member in the discussion may have helped to minimize the recall bias. Finally, although the mean age of the sample cohort represents the mean age of diagnosis of common cancers in Oman, such as, the breast cancer, there were significantly more female patients than males. However, the vast majority of decisions are taken by family members, including both males and females, it is unlikely that the gender distribution among the cohort may have influenced the results.

CONCLUSION
We report that almost 40% of the cancer patients travel abroad to seek an opinion from cancer specialist outside of Oman and 1/3 rd of them travel because of familial and societal pressures. Although fullfledged diagnostic and therapeutic cancer care services are available in Oman, yet patients travel overseas to seek opinion and treatment. There is a need to disseminate the information concerning the type and availability of services, expertise, and address the concerns of patients. Also, there is a need to improve the communication skills of the primary care physicians, who either establish the diagnosis or raise the suspicion of the diagnosis of cancer. The primary care physicians need to hone their professional skills of being effective educators and collaborators. Furthermore, the communication channels between the primary care and the tertiary care need to be studied and strengthened.

APPENDIX
Appendixes should appear before the acknowledgment.