J Canc Educ DOI 10.1007/s13187-015-0806-3

Contrasts in Practices and Perceived Barriers to Colorectal Cancer Screening by Nurses and Physicians Working in Primary Care Settings in Oman Joshua Kanaabi Muliira & Melba Sheila D’Souza & Samira Maroof Ahmed

# American Association for Cancer Education 2015

Abstract Colorectal cancer (CRC) is the fourth most common type of cancer worldwide and it is responsible for 610, 000 deaths annually, despite availability of screening tests that ensure early detection. Predictions specific to the Middle East show that this region will experience a significant increase in cancer mortality over the next 15 years. This study explored the practices and perceived barriers to CRC screening from the perspective of health care providers (HCPs) working in primary care settings in Muscat, Oman. A cross-sectional design and self-administered questionnaires were used to collect data from 142 HCPs. The HCPs were nurses (57.7 %) and physicians (42.3 %) with average age and clinical experience of 32.5 and 9.5 years, respectively. The majority of the HCPs (64.8 %) rarely ordered, referred, health educated, or recommended CRC screening to eligible patients. The only major patient-related barrier to CRC screening reported by HCPs was lack of awareness about CRC tests (63.7 %). There were significant differences between nurses’ and physicians’ rating of patient-related barriers such as fear of cancer diagnosis (p= 0.037), belief that screening is not effective (p=0.036), embarrassment or anxiety about screening tests (p=0.022), and culture (p=0.001). The major system barriers to CRC screening were lack of hospital policy or protocols, lack of trained HCPs, lack of CRC screening services, and timely J. K. Muliira (*) : M. S. D’Souza College of Nursing, Department of Adult Health and Critical Care, Sultan Qaboos University, P. O. Box 66, 123Al Khod, Muscat, Oman e-mail: [email protected] J. K. Muliira e-mail: [email protected] S. M. Ahmed College of Nursing, Department of Community Health and Psychiatric Mental Health, Sultan Qaboos University, P. O. Box 66, 123Al Khod, Muscat, Oman

appointments to get CRC screening. The findings indicate a need for interventions to enhance patient awareness, HCPs CRC screening practices, and strategies to ameliorate patient and system barriers to CRC screening. Keywords Colorectal cancer . Cancer screening . Cancer prevention . Barriers . Practices . Primary care . Nurses . Physicians . Oman

Introduction Colorectal cancer (CRC) is the fourth most common type of cancer worldwide leading to 610,000 deaths annually and the majority of these deaths occur in middle- and low-income countries [1]. It is estimated that in the Middle East, the cancer mortality rate will increase by more than 100 % over the next two decades [2]. In Oman, a country located in the Middle East, trends of the past 10 years show that the incidence of cancer is increasing. In the year 2000, the Ministry of Health in Oman reported the crude incidence rate of cancer among males and females to be 50.5 per 100,000 and 48.6 per 100, 000, respectively [3]. The latest reports show that the annual adjusted incidence of cancer ranges from 70 to110 per 100, 000 population in Oman [4]. CRC is currently the fifth commonest cancer among Omani men [2] and the ageadjusted incidence is estimated at 4.8 per 100,000 in men and 4.2 per 100,000 in women, in this country of approximately 3.7 million people [5]. The incidence of colon adenomas in Omanis has been reported to be 12.2 % and the frequency of genetic microsatellite instability, which is responsible for initiation and progression of some sporadic and hereditary CRC, is reported to be the same as in American Caucasians [6]. Research shows that

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Omanis are affected by CRC at a younger age [7] and the risk factors for CRC such as diabetes (11.6 %), obesity or overweight (48.8–51 %) [8], and smoking (7 %) [9], are very prevalent in the country. The estimated overall prevalence of obesity in Middle East countries is close to 25 % [10, 11]. The risk factors for CRC and the morbidity and mortality due to CRC in Oman and the Middle East Region is increasing because of the changing standards of living, lifestyles, dietary practices, and other behaviors which enhance the risks for cancer. The changes in standards of living have also led to an increase in the Oman population’s life expectancy (74 years for men and 78 years for women) [5] and this has also contributed to the CRC risk burden. Although CRC is fatal, it can be prevented if detected early through screening [12, 13]. Therefore, one of the most crucial and needed response to the growing problem of CRC in Oman and the Middle East Region is prevention and early detection through screening. Research has shown that if CRC screening is implemented properly and followed with timely diagnosis and treatment, it can save thousands of lives [12]. In Oman, all nationals and government employees get free health care and the country has made efforts to respond to the increasing burden of cancer through strategies such as establishing the national cancer registry, provision of cancer screening and early detection services at the public primary health care facilities, and provision of cancer treatment at selected referral hospitals [14]. The most commonly provided cancer screening services are the tests for cervical cancer, breast cancer, and CRC [14]. The CRC screening test, which is commonly available in lower-level public primary health care centers, is fecal occult blood testing or fecal immunological test [14]. The higher level public primary health care centers (polyclinics) and hospitals provide all the different types of CRC screening tests. The screening tests are mostly provided upon a physician’s order and the nurses mostly participate in educating, teaching, and preparing eligible patients for the tests. However, the CRC screening tests are not regularly received or utilized by eligible patients and the country does not yet have an operational cancer policy or action plan [14]. In Oman, there are also no official statistics or studies which have reported about uptake of CRC screening services or general cancer screening rates. The available literature shows that in Oman, CRC is mostly diagnosed late [2, 5], and this suggests lack of optimal screening services. Screening is a systematic application of medical tests in asymptomatic populations and it helps to identify individuals with abnormalities suggestive of pre-cancer or cancer states and referring them to get prompt diagnosis and treatment. However, in order for health care providers (HCPs) to provide effective and optimal CRC screening, they must have good practices and should face minimal barriers when implementing screening services. Our study focused on understanding the practices and barriers related to CRC from the perspective of the HCPs

working in primary care settings. The HCPs working in primary care settings are uniquely positioned to provide CRC screening and preventive services through health education, counseling, referral, and follow-up care because they are usually the first point of contact with the health care system and get a chance to have multiple contacts with eligible patients. The HCPs working in primary care settings also play an important role in the process of implementing CRC screening guidelines because they are in a better position to recommend screening or initiate referrals to hospitals for specific tests to eligible patients. However, as HCPs in primary care settings dispense CRC screening services, they are bound to be influenced by certain factors or barriers. Understanding of what the HCPs perceived to be the barriers can unlock important insights about the interventions needed to enhance CRC screening and cancer prevention services. Previous studies have attributed the barriers to CRC screening to patients and the health care system [15]. The patient-related barriers to CRC screening include lack of trust in HCPs, co-morbid medical illnesses, lack of symptoms, fatalistic views and fear of news about cancer, lack of knowledge [16], fear of embarrassment, privacy issues, and cost [17]. The system barriers include lack of systems to identify eligible patients (chart reminders and pop up messages on computer) and lack of clear protocols on how to provide results to the patients [18]. The other system barriers reported by patients include difficulty in scheduling appointments for screening and lack of reminders of scheduled appointments [19]. In Oman, there are no studies which have explored the barriers to CRC screening and early detection. The current study focused on CRC screening practices and perceived barriers from the perspective of the HCPs. The Preventive Health Model (PHM) [20] was used to guide our conceptualization of how the HCPs practices and perceived barriers can impact the phenomenon of CRC screening (cancer prevention behavior) in primary care settings. The PHM has been used widely to explain factors associated with cancer screening behaviors [21]. The PHM has constructs focusing on the patient characteristics; patient behavior factors (affect, values, self-efficacy, social influence, and others); HCPs factors (barriers, experience, perceptions, care setting, screening tests, and others); systems of support (guidelines, information systems, community resources, and others); and the outcome of the patient’s behaviors (intention, planning, action, and experience with cancer screening). The PHM model posits that patient’s intention, planning, action, and experiences related to CRC screening are all directly influenced by the HCPs and system factors. Therefore, the purpose of this study was to explore the HCPs practices and perceived barriers related to CRC screening in primary care settings.

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A descriptive study with a cross-sectional design was used to collect data from HCPs working in government primary care settings (health centers) located in Muscat, the capital of Oman. Oman is one of the countries located in the Middle East and the population census data of December 2010 shows that the country has a population of approximately 3,632,000 million people and 27.3 % of this population resides in the city of Muscat [22]. The residents of Muscat receive their primary care mainly from 27 government health centers and polyclinics which are staffed by nurses, physicians, and laboratory technicians. The government of Oman provides free health care to all Omanis and government employs (regardless of their nationality). The participants for this study were HCPs (nurses and physicians) working at the 27 health centers in the city of Muscat. The HCPs working in the health centers are qualified with at least a diploma or associate degree-level professional education in their respective fields and serve different roles in the process of providing primary care to the population. The language used during training of HCPs and documentation of patient care in Oman is English. Therefore, all nurses and physicians working in the health centers are able to read and write in English. The primary care services provided at the health centers emphasize maternal and child health, treatment of common diseases and injuries, health education, and preventive and screening services for communicable and noncommunicable diseases. The health centers are equipped with laboratory facilities to provide the needed screening services and are the first points of contact with the health care system. The health centers are responsible for initiating referrals to local and regional hospitals if required. The data for this study was collected from the HCPs in the 27 health centers in the period of January 2014 to July 2014. All available HCPs (nurses and physicians) meeting the inclusion criteria were targeted as participants in the study. In order to be included in the study, the participants had to be: a nurse or physician officially employed at the health center and directly involved in patient care; involved in care of adult patients; and qualified with a minimum of a diploma or associate degree in their respective profession. The nurses and physicians who were on work leaves (for any reason) were not included in the study. The nurses and physicians who were working exclusively in clinics taking care of antenatal, pediatric, and adolescent patients were also excluded from the study.

participants included demographic and clinical practice setting characteristics, CRC screening practices, factors influencing practices, and perceived barriers to CRC screening. The demographic characteristics considered were age, gender, level of education, clinical experience, years since completion of basic professional training, involvement in teaching of students, and years spent in current practice setting. The clinical practice setting characteristics considered were affiliations with a training institution, percentage of patients paying for their own health care, and availability of CRC screening services or tests. The items used to measure CRC screening practices, factors influencing screening practices, and perceived barriers to CRC screening were adopted from the National Cancer Institute (NCI) Survey of Colorectal Cancer Screening Practices Questionnaire for primary care physicians and diagnostic radiologists [23]. The NCI questionnaire has been used and adopted for use in several CRC-related surveys of HCPs [13, 24]. In order to ascertain the CRC screening practices, participants were asked to respond to questions seeking to determine if they have ever ordered, recommended, health educated, or referred a patient to get CRC screening or genetic testing for suspected susceptibility to CRC. For instance, the section on CRC screening practices had items such as BHave you ever health educated a patient about CRC screening? How often during your clinical practice do you order, refer, health educate, or recommend CRC screening to eligible patients?^ and others. To determine the factors influencing CRC screening practices, participants were asked to rate the level to which factors such as health facility policy, evidence-based guidelines and others influence their practices. The participant were required to rate the influence of each factor as: not available or not influential = 1, somewhat influential = 2, and very influential=3. The perceived barriers to CRC screening were determined by requesting HCPs to use their experiences and opinion to rate specific patient and system related factors as: not a barrier=0, minor barrier=1, and major barrier=3. The SAQ was given to three experts (gastroenterology, nursing, and family medicine) to review it for accuracy, face, and content validity. The three reviewers recommended the SAQ and found it to be appropriate for use in Oman. All the reviewers recommended adding open-ended questions for participants to list other factors, barriers, and additional comments. After adjustments were made to the SAQ, the questionnaire was pre-tested among 22 HCPs working at a University Hospital in Oman. The pre-testing was done to establish clarity of items and the time required to complete the questionnaire. The SAQ required 25 to 30 min to complete.

Data Collection Questionnaire

Ethics and Protection Human Subjects

A self-administered questionnaire (SAQ) written in English was used to collect data from HCPs. The data collected from

The study was reviewed and approved by the research committee of the College of Nursing at Sultan Qaboos University

Methods Participants and Setting

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and the Directorate of Research and Studies of the Ministry of Health in Oman. The participants were required to read and sign a written consent form before participating in the study. The consent form had information explaining the study purpose, study procedures, and participants’ rights. Participants were provided an opportunity to ask questions before completing the study questionnaire. The study did not collect any personal information which could be used to identify the participants. Data Collection Two registered nurses working at the University Hospital were trained and hired as research assistants. The research assistants (RA) were given copies of letters approving the study and letters introducing them to the health centers. On data collection days, both RA went to one specific health center and introduced themselves to the manager of the health center. After meeting with the manager, the RA proceeded to approach all the available HCPs (nurses and physicians) to explain the study purpose. The HCPs who agreed to participate in the study were given a consent form to complete. After the consent process, the HCPs were given the SAQ to be completed in 1 hour. The period of one hour was given to limit disruption of patient care activities and the temptation of discussing items on the SAQ with others. The HCPs were instructed to drop off the completed SAQ in a receiving box located in a specific room at the health center. On returning the SAQ, the RA waiting in the room checked it for completeness before the HCPs dropped it off in the receiving box. The RA also tracked HCPs who delayed to return the SAQ on time by going to their work stations to retrieve the SAQ after the 1hour period elapsed. A total of 241 HCPs were approached during the period of data collection in all the 27 health centers to participate in the study and 183 of these agreed to participate in the study. A total of 142 returned the questionnaire or were contactable to retrieve the questionnaire after the stipulated time. Therefore, the response rate in this study was 58.9 % and the refusal rate was 24.1 %. Data Analysis The data from the completed questionnaires was entered, cleaned, and analyzed using SPSS (Statistical Package for Social Sciences) version 20. Descriptive statistics were used to describe the sample, CRC screening practices, factors influencing practices, and perceived barriers to CRC screening. The Fisher’s exact test (FET) was used to examine potential differences between nurses’ and physicians’ practices, perceptions about factors influencing CRC screening practices, and barriers to CRC screening. The FET was used since it is the most robust when working with a small sample size and cross tabulation tables with expected frequency counts less

than 5. The level of significance for all analyses and statistical tests was set at p10 years ≤5 years 6–10 years >10 years Doctorate degree Masters degree Bachelors degree Associate degree Yes No ≤5 years 6–10 years >10 years

36 (25.4) 58 (40.8) 48 (33.8) 38 (26.8) 58 (40.8) 46 (32.4) 3 (2.1) 12 (8.4) 59 (41.6) 68 (47.9) 68 (47.9) 74 (52.1) 72 (50.7) 45 (31.7) 25 (17.6)

10 (12.2) 40 (48.8) 32 (39) 11 (13.4) 40 (48.8) 31 (37.8) 0 (0) 0 (0) 18 (22) 64 (78) 48 (58.5) 34 (41.5) 36 (43.9) 30 (36.6) 16 (19.5)

26 (43.3) 18 (30) 16 (26.7) 27 (45) 18 (30) 15 (25) 3 (5) 12 (20) 41 (68.3) 4 (6.7) 20 (33.3) 40 (66.7) 36 (60) 15 (25) 9 (15)

Category

CRC screening to patients during clinical practice. There were no significant differences between the nurses’ and physicians’ self-reported CRC screening practices.

Colorectal cancer screening practices of the participants

Item

Response

Sample N=142 F (%)

Nurses N=82 F (%)

Physicians N=60 F (%)

p value Fisher’s exact test (one sided)

Orders, refers, health educates, or recommends CRC screening to patients during clinical practice

Rarely Often

92 (64.8) 5 (3.5)

58 (70.7) 4 (4.9)

34 (56.7) 1 (1.7)

0.047

Very often Yes Yes Yes Yes Yes

45 (31.7) 11 (7.7) 11 (7.7) 12 (8.5) 12 (8.5) 2 (1.4)

20 (24.4) 7 (8.5) 5 (6.1) 8 (9.8) 7 (8.5) 2 (2.4)

25 (41.7) 4 (6.7) 6 (10) 4 (6.7) 5 (8.3) 0 (0)

0.469 0.292 0.369 0.608 0.332

Yes

7 (4.9)

3 (3.7)

4 (6.7)

0.331

Yes

5 (3.5)

3 (3.7)

2 (3.3)

0.645

Yes

12 (8.5)

8 (9.8)

4 (6.7)

0.369

Has ordered CRC screening for patients Has referred patients to get CRC screening Has health educated patients about CRC screening Has recommended CRC screening to patients Has ordered genetic testing for patients suspected of inherited susceptibility to CRC Has referred patients for genetic testing for suspected inherited susceptibility to CRC Has health educated patients a about genetic testing for a suspected inherited susceptibility to CRC Has recommended patients for genetic testing for a suspected inherited susceptibility to CRC

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Factors Perceived to Influence Health Care Providers’ Colorectal Cancer Screening Practices The results summarized in Table 3 indicate that the factors perceived by nurses to have the most influence on their CRC screening practices were availability of a system to identify patients eligible for CRC screening (44 %), continuing professional education on cancer prevention (46 %), availability of specialists in cancer (49 %), and a health facility policy on cancer screening (54 %). A large number of physicians also rated factors such as availability of a system to identify patients eligible for CRC screening (42 %), continuing professional education on cancer prevention (57 %), availability of specialists in cancer (45 %), and a health facility policy on cancer screening (57 %), as very influential in regard to their CRC screening practices. There were significant differences in the perceptions of nurses and physicians regarding the influence of knowledge and skills acquired during formal Table 3

professional education (p=0.009) and the American Cancer Society guidelines (p=0. 019) on CRC screening practices. However, the majority of nurses and physicians reported that they were not familiar with or were only somewhat influenced by factors such as evidence published in scientific journals, guidelines, or recommendations for cancer screening by the local Ministry of Health, the Independent Expert Panel on CRC screening guidelines, the American Cancer Society guidelines, and the US Preventive Services Task Force (USPSTF) guidelines. Participants’ Perceptions About Barriers to Colorectal Cancer Screening in the Primary Care Setting The results presented in Table 4 shows that according to the HCPs, the only major patient-related barrier to CRC screening is lack of awareness about screening tests (63.7 %). All the other patient-related barriers were perceived to be minor by

Factors perceived by participants to influence their colorectal cancer screening practices

Factor

Rating of level influence

Nurses N=82 F (%)

Physicians N=60 F (%)

p value Fisher’s exact test (one sided)

Knowledge and skills acquired during formal professional education

Not influential Somewhat influential Very influential Not available or not influential Somewhat influential Very influential Not available or not influential Somewhat influential Very influential Not available or not influential Somewhat influential Very influential Not available or not influential Somewhat influential Very influential Not available or not influential Somewhat influential

45 (54.9) 12 (14.6) 25 (30.5) 18 (22) 28 (34.1) 36 (43.9) 17 (20.7) 27 (32.9) 38 (46.3) 23 (28) 19 (23.2) 40 (48.8) 21 (25.6) 44 (53.7) 17 (20.7) 34 (41.5) 21 (25.6)

19 (31.7) 20 (33.3) 21 (35) 11 (18.3) 24 (40) 25 (41.7) 9 (15) 17 (28.3) 34 (56.7) 10 (16.7) 23 (38.3) 27 (45) 10 (16.7) 30 (50) 20 (33.3) 24 (40) 20 (33.3)

0.009

Very influential Not available or not influential Somewhat influential Very influential Not familiar Somewhat influential Very influential Not familiar Somewhat influential Very influential Not familiar Somewhat influential Very influential

27 (32.9) 16 (19.5) 22 (26.8) 44 (53.7) 52 (63.4) 19 (23.2) 11 (13.4) 53 (64.3) 18 (22) 11 (13.4) 49 (59.7) 15 (18.3) 18 (22)

16 (26.7) 11 (18.3) 15 (25) 34 (56.7) 37 (61.7) 17 (28.3) 6 (10) 32 (53.3) 22 (36.7) 6 (10) 27 (45) 20 (33.3) 13 (26.7)

Availability of system to identify patients eligible for CRC screening services Continuing professional education on cancer prevention Availability of a specialist in cancer

Evidence published in scientific journals

Guidelines or recommendations by the local ministry of health Policy on cancer screening

Independent expert panel on CRC screening: guidelines and rationale United States Preventive Services Task Force (USPSTF) guidelines American Cancer Society Guidelines.

0.503

0.157

0.327

0.043

0.346

0.469

0.519

0.200

0.019

J Canc Educ Table 4

Perceived patient- and system-related barriers to colorectal cancer screening

Category of barrier

Barrier

Rating of barrier

Sample N=142 F (%)

Nurses N=82 F (%)

Physicians N=60 F (%)

p value Fisher’s exact test (one sided)

Patient-related barriers

Patients’ fear of finding out that they have cancer Patients believe screening is not effective

Major

68 (47.9)

45 (54.9)

23 (38.3)

0.037

Major

46 (32.4)

32 (39)

14 (23.3)

0.036

Major

60 (42.3)

41 (50)

19 (31.7)

0.022

Major

89 (63.7)

50 (61)

39 (65)

0.378

Major

51 (35.9)

33 (40.2)

18 (30)

0.140

Major

58 (40.8)

38 (46.3)

20 (33.3)

0.083

Major

49 (34.5)

37 (45.1)

12 (20)

0.001

Major Major Major

62 (43.7) 86 (60.6) 94 (66.2)

35 (42.7) 52 (63.4) 56 (68.3)

27 (45) 34 (56.7) 38 (63.3)

0.458 0.261 0.330

Major

79 (55.6)

48 (58.5)

31 (51.7)

0.260

Major

68 (47.9)

40 (48.9)

28 (46.7)

0.469

Major

90 (63.4)

53 (64.6)

37 (61.7)

0.425

Major

83 (58.5)

48 (58.5)

35 (58.3)

0.558

Major

31 (21.8)

22 (26.8)

9 (15)

0.680

Major

50 (35.2)

28 (34.1)

23 (38.3)

0.106

System-related barriers

Patient’s embarrassment or anxiety about screening tests Patients are unaware of CRC screening tests and when they should be done Patients think CRC screening procedures cause a lot of discomfort Patients do not perceive CRC as a serious health problem Patient’s culture is not favorable to procedures used for CRC screening Screening costs are very expensive Screening services are not available Long waiting time for screening appointments Lack of hospital policy or protocol on cancer screening Healthcare providers do not actively recommend CRC screening to patients Shortage of trained healthcare workers to conduct CRC screening Shortages of trained providers to conduct follow-up with invasive procedures CRC is not a common health problem in our patients The patient load is very big

the HCPs. However, there were some significant differences between nurses’ and physicians’ rating of four patient-related barriers. Significantly more nurses, compared to physicians, perceived patient’s fear of finding out about cancer diagnosis (p=0.037), beliefs that screening is not effective (p=0.036), embarrassment or anxiety about screening tests (p=0.022), and culture (p=0.001), as major barriers to CRC screening. The major system barriers to CRC screening were lack of hospital policy or protocols for cancer screening (55.6 %), shortage of trained HCPs to conduct CRC screening (63.4 %) or to follow up with invasive procedures (58.5 %), limited availability of screening services (60.6 %), and long waiting time for screening appointments (66.2 %). There were no significant differences between nurses’ and physicians’ perceptions of minor and major system barriers to CRC screening.

Discussion This study explored the practices and barriers to CRC screening in primary care settings as perceived by HCPs. To our knowledge, this is the first study to report about HCPs

practices and barriers to CRC screening in any health care setting in Oman. The study focused on HCPs working in primary care settings because they are uniquely positioned to advance CRC screening services since they get multiple contacts with eligible patients when they are seeking for primary care. The HCPs working in primary care settings get adequate opportunities to health educate, counsel, order, recommend, and refer eligible patients to get CRC screening. The findings of our study show that the majority (65 %) of HCPs had poor CRC screening practices because they rarely performed activities such as ordering, referring, health educating, or recommending CRC screening to eligible patients. The factors which were reported to influence the HCPs colorectal cancer screening practices were lack of systems to identify patients eligible for CRC screening, specialists in cancer, continuing professional education on cancer prevention, and health facility policies on cancer screening. The main patient-related barrier to CRC screening reported by HCPs was lack of awareness about screening tests. The major system barriers to CRC screening reported by HCPs were lack of hospital policies or protocols for cancer screening, shortage of trained HCPs to conduct CRC screening or to follow up with invasive procedures, limited availability of screening services,

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and long waiting time for screening appointments. The findings of this study highlight areas that need improvement in order to enhance CRC screening and prevention in Oman. The specific areas that the study seems to point out are those related to HCPs practices, system barriers, and patient awareness about CRC screening, and these are discussed below.

Health Care Providers’ Colorectal Cancer Screening Practices One of the most intriguing finding of this study was the poor CRC screening practices of the participants. The majority of HCPs (64.8 %) reported that they rarely order, refer, health educate, or recommend CRC screening to patients during clinical practice (Table 2). Less than 10 % of the participants had ever recommended, ordered, health educated, or referred eligible patients to get CRC screening or to get genetic testing for suspected inherited susceptibility to CRC. The level of CRC screening practices was poor despite the availability of basic CRC screening tests such as FOBT, patient eligible for screening, free health care services, and work settings which are affiliated with training institutions. There were no significant differences in the CRC practices of nurses and physicians. The poor practices of HCPs may be fueling the patients’ lack of awareness of cancer risk and cancer screening tests. A recent study has reported that the majority of adult Omanis are not aware of the risk factors for cancer such as eating less fruits and vegetables, high consumption of red or processed meat, being overweight, doing less exercise, and others [25]. Therefore, in Oman, poor CRC screening practices among HCPs is one of the barriers to CRC screening. One of the explanations of the poor CRC screening practices could be the level of profession education of the nurses and physicians working in primary care settings. The majority of nurses (48 %) had associate degree-level professional education, while most of the physicians had bachelor-level (78 %) professional education (Table 1). It is possible that the curriculum used to train nurses and physicians at these levels of professional education do not give enough emphasis on aspects related to cancer screening and prevention. The findings of this study showing poor practices are similar to what has been reported about HCPs in other countries. A recent study conducted among primary care nurses, physicians, and other HCPs in Jordan (a country located in the Middle East) also found poor CRC screening practices with less than 15 % reporting ordering, referring, educating, or recommending CRC screening to eligible patients [26]. In Malaysia, a study of CRC screening practices of primary care providers, found that only 21 % were recommending FOBT in more than 50 % of their eligible patients [27]. And in USA, primary care physicians practicing in community health centers have also been reported to have poor CRC screening practices such as not adequately following CRC screening

guidelines [28]. Poor CRC screening practices have also been reported by studies conducted in rural areas of USA [29]. The CRC screening practices of HCPs deserve constant attention and monitoring because they are critical in ensuring early diagnosis of CRC, patient knowledge about CRC and screening tests, and uptake of CRC screening. Research shows that HCP practices such as making screening recommendation to patients are significantly associated with adherences to CRC screening [30]. The findings of this study about HCPs CRC screening practices highlight the need for continuing education to enhance HCPs awareness of patients eligible or at risk of CRC and utilization of evidence-based CRC screening guidelines. Increasing the HCPs awareness of CRC risk in patients may enhance their screening practices. A study conducted in Turkey showed that when physicians are aware of the cancer risk of their patients, they tend to recommend more CRC screening test such as annual FOBT [31]. Factors Perceived to Influence Colorectal Cancer Screening Practices In this study, the HCPs reported that the main factors which mostly influenced their CRC screening practices were availability of a system to identify patients eligible for CRC screening, continuing professional education on cancer prevention, availability of specialists in cancer, and the health facility policy on cancer screening. On the other hand, the HCPs reported that they were not much influenced or not familiar with the widely recognized evidence-based guidelines about CRC screening such as the USPSTF and American Cancer Society guidelines (Table 3). There were significant difference between nurses’ and physicians’ perception regarding the influence of knowledge and skills acquired during formal professional education (p=0.009) and American Cancer Society guidelines (p=0.019). The physicians perceived these two factors to be very influential compared to nurses. These findings highlight opportunities which can be taken advantage of to enhance CRC screening. For instance, interventions such as establishing specialized CRC screening clinics or programs, conducting regular continuing professional education programs for HCPs, orienting HCPs about evidence-based CRC screening guidelines, and having a visiting oncologist in the primary care settings can be used to enhance CRC screening practices. However, in order to successfully implement such interventions and to positively influence HCPs, there is a need for synergistic multi-faceted interventions, coordination, and collaboration between stakeholders (HCPs, education providers and administrator or managers of primary care facilities). In primary care settings of other countries, strategies such as having reminders for both HCPs and patients, cancer screening policies, protocols, and patient navigators, have been found to be very effective at enhancing CRC screening [32].

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Barriers to Colorectal Cancer Screening in Primary Care Settings In the current study, the only patient-related barrier to CRC screening perceived as major by the majority of HCPs (63.7 %) was patients’ lack of awareness about screening tests (Table 4). All the other patient-related barriers were mostly perceived to be minor. However, significantly more nurses, compared to physicians, perceived patient-related barriers such as fear of finding out about cancer diagnosis (p = 0.037), beliefs that screening is not effective (p=0.036), embarrassment or anxiety about screening tests (p=0.022), and culture, as major barriers (p=0.001). The differences between the perceptions of nurses and physicians about some of the patient factors could be because of the difference in the professional approach to patient care. In nursing practice, the nurses are expected and tend to emphasize holistic care and this enables them to examine more about patients’ feelings and perceptions during health care. This approach to patient care enables nurses to elicit information about patients’ fears and psychosocial aspects such as culture. In clinical practice, these differences in perceptions are critical and can be a barrier because they can influence the HCPs’ actions and decision to health educate, recommend, order, or initiate a referral to get CRC screening. There were no significant differences in the perceptions of nurses and physicians about system barriers to CRC screening. The lack of differences in perceptions about system barriers suggests a general agreement by HCPs about health care system factors that impede CRC screening. The top five major system barriers to CRC screening reported by HCPs were lack of hospital policy or protocols for cancer screening, shortage of trained HCPs to conduct CRC screening or follow up with invasive procedures, limited availability of screening services, and long waiting time for screening appointments (Table 4). The finding about patientrelated barrier of lack of awareness is similar to what has been reported in other countries such as Jordan, Malaysia, and USA [26, 27, 29, 33]. However in other countries, the HCPs tend to rate more patient factors as some of the major barriers to CRC screening. For instance, HCP working in rural parts of USA, in addition to lack of patient awareness, they reported patient beliefs and fear of embarrassment, as significant barriers [29, 33]. In other studies conducted in the USA, the nurses and physicians working in primary care settings reported the major patient-related barriers to be lack of knowledge, fear, poor compliance [34], and having multiple health problems [28, 35]. In Jordan, the other major patient-related barrier to CRC screening reported by HCPs working in primary care settings included fear of cancer diagnosis and patients lack of awareness [26]. In countries which do not have free health care, the HCPs working in primary care settings tend to report lack of insurance coverage as a major barrier [28, 34, 35]. In the current

study, the HCPs perceived cost as only a minor barrier. The findings about the factor of cost are not surprising because in Oman, the government provides free health care to all Omanis and government employees. The findings of the current study about other system-related barriers to CRC screening are similar to what has been reported by HCPs working in rural and urban areas of other countries. The major system barriers reported by HCPs in this study are similar to what has been reported in Jordan and USA. In Jordan, the major reported system barriers (apart from cost) included availability of screening services, long waiting time for appointments, lack of hospital policies, lack of recommendations by HCPs, shortage of HCPs, and patient load [26]. The system barriers commonly cited in other countries like USA include limited access and long waiting time for screening appointments for specific types of procedures, especially colonoscopy [35]. The findings about patient- and system-related barriers to CRC screening highlight the gaps that need to be addressed in order to enhance CRC screening. The best way forward to address the patient and system barriers to CRC screening is to view them as opportunities for health care managers or administrators, HCPs, educators, researchers, and policy makers to enhance screening and cancer prevention. For instance, research has already shown that education interventions for HCPs such as academic detailing can increase CRC screening rates when implemented in primary care practice settings [36]. Academic detailing is a method of continuing professional education where HCPs are instructed through personal contact with an individual or as a group on a specific topic [37]. Other studies have also shown that interventions such as introduction of specific tools in clinical practice such as decision aids [38] and provider reminder and recall systems to inform those who deliver health services of patient due (reminder) or overdue (recall) for screening [39], are effective at increasing CRC screening. Therefore, the patient and system barriers highlighted by this study reveal the available opportunities for all stakeholders to contribute to the efforts of increasing CRC screening through strengthening screening capacity of HCPs, screening facilities, screening services, and public awareness. Study Limitations The findings of our study need to be considered in view of the study limitations. The limitations of this study include a small sample size and reliance on self-report data from HCPs. Large-scale national studies of both HCPs and patients to examine the current rates, practices, and barriers to CRC screening are needed to provide a clear national picture of the status of CRC screening in Oman and other Middle East countries. Despite its limitations, the results of this study point to need for specific interventions to reduce the barriers to CRC screening and to enhance nurses’ and physicians’ CRC screening

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practices in primary care settings. Such interventions can be in the form of continuing education programs, system reminder to identify patients eligible for screening, and others addressing specific perceived patient and system barriers. In order to ensure sustained good practices related to CRC screening among HCPs, it is also important to make sure that the curricula used to train nurses and physicians emphasize aspects related to cancer screening and cancer prevention. Acknowledgments The study was funded by Sultan Qaboos University, Deanship of Research grant number IG/CN/AHCC/13/01. The authors would like to acknowledge the Ministry of Health of Sultanate of Oman and the health care providers working in primary care settings for their participation in the study. Conflict of Interest The authors declare that they have no conflict of interest.

References 1. World Health Organization. 2011. Cancer. Down loaded from http:// www.who.int/mediacentre/factsheets/fs297/en/index.html. Accessed on 30 September, 2014. 2. Dey S, Soliman AS (2010) Cancer in the global health era: opportunities for the Middle East and Asia. Asia Pac J Public Health 22(3 Suppl):75S–82S 3. Ministry of Health Sultanate of Oman (2000) Cancer incidence in Oman report of 2000, non-communicable diseases control section, Directorate General of Health Affairs. Ministry of Health Sultanate of Oman, Muscat, Oman 4. Al-Lawati JA, Mabry R, Mohammed AJ (2008) Addressing the threat of chronic diseases in Oman. Prev Chronic Dis 5(3):A99 5. Ministry of Health Sultanate of Oman (2009) Cancer incidence in Oman report of 2009, non- communicable diseases control section, Directorate General of Health Affairs. Ministry of Health Sultanate of Oman, Muscat, Oman 6. Ashktorab H, Brim H, Al-Riyami M, Date A, Al-Mawaly K, Kashoub M, Al-Mjeni R, Smoot DT, Al-Moundhri M, Al-Hashemi S, Ganguly SS, Raeburn S (2008) Sporadic colon cancer: mismatch repair immunohistochemistry and microsatellite instability in Omani subjects. Dig Dis Sci 53(10):2723–2731 7. Brim H, Mokarram P, Naghibalhossaini F, Saberi-Firoozi M, AlMandhari M, Al-Mawaly K, Al-Mjeni R, et al (2008). Impact of BRAF, MLHI on the incidence of microsatellite instability high colorectal cancer in populations based study. Mol Cancer 7 (68): doi: 10.1186/1476-4598-7-68. 8. Ng SW, Zaghloul S, Ali HI, Harrison G, Popkin BM (2011) The prevalence and trends of overweight, obesity and nutrition related non-communicable diseases in the Arabian Gulf states. Obes Rev 12(1):1–13 9. Al Riyami AA, Afifi M (2004) Smoking in Oman: prevalence and characteristics of smokers. East Mediterr Health J 10(4–5):600–609 10. Motlagh B, O’Donnel M, Yusuf S (2009) Prevalence of cardiovascular risk factors in the Middle East: a systematic review. Eur J Cardiovasc Prev Rehabil 16(3):268–280 11. Musaiger AO (2004) Overweight and obesity in the Eastern Mediterranean region: can we control it? East Mediterr Health J 10(6):789–793 12. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225–249

13. Klabunde CN, Frame PS, Meadow A, Jones E, Nadel M, Vernon SW (2003) A national survey of primary care physicians’ colorectal cancer screening recommendation and practices. Prev Med 36(3):352– 362 14. World Health Organization. 2015. Oman cancer country profile. Downloaded from http://www.who.int/entity/cancer/countryprofiles/omn_fr.pdf-36k. Accessed on 5 January, 2015. 15. Jo AM, Maxwell AE, Rick AJ, Cha J, Bastani R (2009) Why are Korean American physicians reluctant to recommend colorectal cancer screening to Korean American patients? Exploratory interview findings. J Immigr Minor Health 11(4):302–309 16. Lasser KE, Ayanian JZ, Fletcher RH, Good M-JD (2008) Barriers to colorectal cancer screening in community health centers: a qualitative study. BMC Fam Pract 9:15. doi:10.1186/1471-2296-9-15 17. Filippi MK, James AS, Brokenleg S, Talawyma M, Perdue DG, Choi WS, Greiner KA, Daley CM (2013) Views, barriers, and suggestions for colorectal cancer screening among American Indian women older than 50 years in the Midwest. J Prim Care Community Health 4(3): 160–166 18. Levy BT, Daly JM, Schmidt EJ, Xu Y (2012) The need for office systems to improve colorectal cancer screening. J Prim Care Community Health 3(3):180–186 19. Medina GG, McQueen A, Greisinger AJ, Bartholomew LK, Vernon SW (2012) What would make getting colorectal cancer screening easier? Perspectives from screeners and non screeners. Gastroenterol Res Pract. doi:10.1155/2012/895807 20. Green BB, Wang CY, Horner K, Catz S, Meenan RT, Vernon SW, Carrell D, Chubak J, Ko C, Laing S, Bogart A (2010) Systems of support to increase colorectal cancer screening and follow-up rates (SOS): design, challenges, and baseline characteristics of trial participants. Contemp Clin Trials 31(6):589–603 21. McQueen A, Vernon SW, Myers RE, Watts BG, Lee ES, Tilley BC (2007) Correlates and predictors of colorectal cancer screening among male automotive workers. Cancer Epidemiol Biomarkers Prev 16(3):500–509 22. Ministry of National Economy (Oman) (2010) Oman general census of population, housing and establishments. Ministry of National Economy (Oman), Muscat, Oman 23. National Cancer Institute (2011). Survey of Colorectal cancer screening practices—diagnostic radiologist questionnaire. Available at: http://healthservices.cancer.gov/surveys/colorectal/rad0604.pdf. Accessed 2 January, 2013. 24. Klabunde CN, Lanier D, Nadel MR, McLeod C, Yuan G, Vernon SW (2009) Colorectal cancer screening by primary care physicians: recommendations and practices, 2006-2007. Am J Prev Med 37(1):8–16 25. Al-Azri M, Al-Rasbi K, Al-Hinai M, Davidson R, Al-Maniri A (2014) Awareness of risk factors for cancer among Omani adults— a community based study. Asian Pac J Cancer Prev 15(3):5401–5406 26. Omran S, Barakat H, Muliira JK, Aljadaa N (2014) Knowledge, experiences, and barriers to colorectal cancer screening: a survey of health care providers working in primary care settings. J Cancer Educ. doi:10.1007/s13187-014-0676-0 27. Norwati D, Harmy MY, Norhayati MN, Amry R (2014) Colorectal cancer screening practices of primary care providers: results of a national survey in Malaysia. Asian Pac J Cancer Prev 15(6):2901– 2904 28. Nadora JN, Martz WD, Ashbeck EL, Jacobs ET, Thompson PA, Martínez ME (2011) Primary care physician compliance with colorectal cancer screening guidelines. Cancer Causes Control 22(9): 1277–1287 29. Rosenwasser LA, McCall-Hosenfeld JS, Weisman CS, Hillemeier MM, Perry AN, Chuang CH (2013) Barriers to colorectal cancer screening among women in rural central Pennsylvania: primary care physicians’ perspective. Rural Remote Health 13(4):2504–2520

J Canc Educ 30. Post DM, Katz ML, Tatum C, Dickinson SL, Lemeshow S, Paskett ED (2008) Determinants of colorectal cancer screening in primary care. J Cancer Educ 23(4):241–247 31. Uysal-Sonmez O, Tanriverdi O, Uyeturk U, Budakoglu II, Turker I, Budakoglu B, Yalcintas-Arslan U, Oksuzoglu B (2014) Awareness of cancer screening during treatment of patients with renal failure. A physician survey in Turkey. Asian Pac J Cancer Prev 15(5):2165– 2168 32. Sarfaty M, Doroshenk M, Hotz J, Brooks D, Hayashi S, Davis TC, Joseph D, Stevens D, Weaver DL (2013) Strategies for expanding colorectal cancer screening at community health centers. CA Cancer J Clin 63(4):221–231 33. Hatcher J, Dignan MB, Schoenberg N (2011) How do rural health care providers and patients view barriers to colorectal cancer screening? Insights from Appalachian Kentucky. Nurs Clin N Am 46(2): 181–192 34. Rowe S, Goldsmith G, Price R, Brooks A, Harvey A (2012) Health care providers’ perspectives of an intervention designed to improve colorectal cancer screening rates in family medicine residency clinics. J Cancer Educ 27(4):695–702

35. Coronado GD, Petrik AF, Spofford M, Talbot J, Do HH, Taylor VM (2014) Clinical perspectives on colorectal cancer screening at LatinoServing federally qualified health centers. Health Educ Behav. doi: 10.1177/1090198114537061 36. Dignan M, Shelton B, Slone SA, Tolle C, Mohammad S, Schoenberg N, Pearce K, Van Meter E, Ely G (2014) Effectiveness of a primary care practice intervention for increasing colorectal cancer screening in Appalachian Kentucky. Prev Med 58:70–74 37. Gorin SS, Ashford AR, Lantigua R, Hossain A, Desai M, Troxel A, Gemson D (2006) Effectiveness of academic detailing on breast cancer screening among primary care physicians in an underserved community. J Am Board Fam Med 19(2):110–121 38. Schroy PC, Mylvaganam S, Davidson P (2014) Provider perspectives on the utility of a colorectal cancer screening decision aid for facilitating shared decision making. Health Expect 17(1):27–35 39. Baron RC, Melillo S, Rimer BK, Coates RJ, Kerner J, Habarta N, Chattopadhyay S, Sabatino SA, Elder R, Leeks KJ, The Task Force on Community Preventive Services (2010) Interventions to increase recommendation and delivery of screening for breast, cervical, and colorectal cancers by healthcare providers. Am J Prev Med 38(1):110–117