Fecal occult blood testing instructions and impact on patient adherence

Cancer Epidemiology 36 (2012) e258–e264

Contents lists available at SciVerse ScienceDirect

Cancer Epidemiology The International Journal of Cancer Epidemiology, Detection, and Prevention journal homepage: www.cancerepidemiology.net

Fecal occult blood testing instructions and impact on patient adherence Sunita B. Bapuji a,*, Michelle M. Lobchuk b,1, Susan E. McClement b,2, Jeffrey J. Sisler c,d,e,3, Alan Katz d,f,g,4, Patricia Martens f,g,5 a

Winnipeg Regional Health Authority, Winnipeg, Manitoba, Canada Faculty of Nursing, University of Manitoba, Winnipeg, Canada c Primary Care Oncology Program, CancerCare Manitoba, Winnipeg, Canada d Department of Family Medicine, University of Manitoba, Winnipeg, Canada e Department of Internal Medicine, University of Manitoba, Winnipeg, Canada f Manitoba Center for Health Policy, University of Manitoba, Winnipeg, Manitoba, Canada g Department of Community Health Sciences, Faculty of Medicine, University of Manitoba, Winnipeg, Manitoba, Canada b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 24 January 2012 Received in revised form 12 March 2012 Accepted 13 March 2012 Available online 13 April 2012

Introduction: Although the physician’s role with patients is crucial in encouraging FOBT screening, the nature and content of physician-patient discussions about FOBT screening is unclear. As part of a larger study, this paper reports on our analyses of physician beliefs about fecal occult blood testing (FOBT) and strategies they employed to enhance patient adherence. The second aim of this paper is to report on the perceptions of individuals at average risk for colorectal cancer (CRC) in regard to their awareness of the FOBT and their responses to physician recommendations about FOBT screening. Methods: The larger study was conducted in urban and rural Manitoba, Canada between 2008 and 2010. We used a qualitative design and conducted semi-structured, audio-recorded interviews with 15 physicians and 27 individuals at average risk for CRC. We included data from 11 family members or friends on their perspectives of FOBT instructions as individuals who were also at average risk for CRC and had their own experiences with CRC screening recommendations. Results: Despite widespread knowledge of The Canadian Task Force on Preventive Health Care CRC screening guidelines, physician attitudes, behaviors, and instructions were not uniform in promoting patient adherence to FOBT screening. Individuals at average-risk for CRC identified that FOBT instructions were confusing and burdensome, which in turn served as a barrier in their adherence to FOBT screening. Conclusions: Variation in FOBT instruction counseling in relation to the recommended age of individuals at average risk for CRC, as well as adequate patient preparation affected patient adherence. We recommend uniform or standardized instructions and counseling by health care providers who administer the FOBT kit to patients to promote adherence to recommended CRC screening. ß 2012 Elsevier Ltd. All rights reserved.

Keywords: Colorectal cancer Screening Guidelines Compliance Fecal occult blood test Qualitative research

1. Introduction

* Corresponding author at: Research & Evaluation Unit, Winnipeg Regional Health Authority, 200-1155 Concordia Avenue, Winnipeg, Manitoba, Canada. Tel.: +1 204 926 7070; fax: +1 204 947 9970. E-mail addresses: [email protected] (S.B. Bapuji), [email protected] (M.M. Lobchuk), [email protected] (S.E. McClement), [email protected] (J.J. Sisler), [email protected] (A. Katz), [email protected] (P. Martens). 1 Tel.: +1 204 474 7135; fax: +1 204 474 7682. 2 Tel.: +1 204 787 4935; fax: +1 204 787 4937. 3 Tel.: +1 204 787 3595; fax: +1 204 786 0715. 4 Tel.: +1 204 789 3442; fax: +1 204 789 3910. 5 Tel.: +1 204 789 3791; fax: +1 204 789 3910. 1877-7821/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.canep.2012.03.007

Colorectal cancer (CRC) is the second leading cause of cancerrelated deaths in men and women combined in Canada [1]. In 2011, an estimated 22,500 individuals will be diagnosed with CRC and 9100 deaths could occur due to CRC [1]. CRC grows slowly in a predictable manner and is curable when diagnosed at an early stage [1]. The Canadian Task Force on Preventive Health Care (CTFPHC) [2] advocates that fifty years of age and above is an appropriate ‘time’ to introduce CRC screening with the fecal occult blood test (FOBT) to average risk individuals (designated as patients in this paper). Regular screening with FOBT could reduce CRC death rates by 15–33% [3,4]. In Manitoba, Canada it is recommended that most people aged 50–74 do a home FOBT every two years [5]. Lobchuk et al. provided a more thorough description

S.B. Bapuji et al. / Cancer Epidemiology 36 (2012) e258–e264

of the Manitoba Colorectal Cancer Screening Program that is known today as the ColonCheck Manitoba [6]. Even though the incidence of CRC and the number of deaths attributed to it are high, screening for CRC worldwide is not adequately utilized by individuals [7–10]. In Canada, only 40% of Canadians aged 50 years or older reported they had engaged in FOBT screening in the past two years [11]. FOBT is a unique test that requires patients to collect stool samples for three consecutive days at their dwelling place. This test involves placing a small sample of feces on a card, to which a chemical solution is added in the laboratory. If ‘occult’, ‘hidden’, or ‘difficult to see’ blood is identified, then it is considered to be positive and further testing (such as a colonoscopy) is required to determine the source of the bleeding. In Canada, there are several FOBT kits available that include hemocult, hemocult II, Sensa, and ColoCheck. These test kits are accompanied by instructions about dietary and medication alterations that, according to the kit manufacturers, should be followed by patients a few days prior to the collection date and then maintained during consecutive three collection days. The literature supporting these restrictions is contradictory [12] and the recommendations for dietary and medication alterations vary from kit manufacturer to manufacturer. Currently, primary care clinics and health authorities in Manitoba receive FOBT kits from several different manufacturers. FOBT instructions vary across manufacturers and provinces in Canada. For instance, CancerCare Manitoba’s website instructions for conducting the FOBT mention that patients should not take most non-steroidal anti-inflammatory drugs for seven days before they start the test and until they have completed the samples. Patients need to avoid ingesting red meats and more than 250 mg/ day vitamin C in any form for three days before they start the test and until they have completed their stool sample collection. In contrast, Ontario’s Colon Cancer Check website offers FOBT instructions that patients can continue to eat their normal diet and take their regular prescribed medications. However, patients should avoid vitamin C supplements and citrus fruit and juices for three days before the test and during the stool sample collection period. A significant barrier to CRC screening is believed to be related to patients’ lack of awareness about CRC screening and the absence of primary care physicians’ recommendations to engage in CRC screening [13]. Hence, cancer prevention education, health promotion, and increased physician or nurse practitioner recommendations in primary care are promising approaches to promote engagement by patients in cancer screening. The prevalence of CRC can be lowered with the help of improved health promotion and disease prevention screening programs [14]. Health promotion strategies need to be based on the knowledge level and health beliefs of individuals to improve their participation in recommended cancer screening [14,15]. Such strategies are expected to increase voluntary CRC screening behaviour in individuals over the age of 50 years. Some studies that explored CRC screening in primary care have been conducted in countries outside of Canada [16,17]. In their qualitative study, Wackerbarth et al. [17] found that most physicians included information to increase their patient’s knowledge about the screening test. However, the majority of physicians did not discuss the patient’s role in the decision to engage in FOBT, assess the patient’s understanding or preferences, or discuss alternatives to screening recommendations. Study findings by Sharma et al. [18] with 417 primary care physicians and internal medicine practitioners across the United States suggested that CRC screening practices varied widely regarding ‘age’ as to when they recommended starting and stopping CRC screening, dietary instructions, and advice regarding medications to avoid during screening. In addition, limited studies explored optimal

e259

approaches for making CRC screening recommendations [17]. To the best of our knowledge, there are no qualitative studies that explored physician beliefs about FOBT, FOBT kits and instructions to patients, and patient responses toward FOBT instructions within the Canadian context of CRC screening recommendations in primary care. Several studies have explored patients’ beliefs on barriers to engaging in recommended FOBT screening behaviors. For instance, Vernon’s [19] review found that patients reported difficulty in preparing for or performing the test regardless of physician instructions. Chapple et al. [16] reported ‘‘misunderstanding instructions’’ as one of the reasons for patients’ reluctance to do FOBT. In the last decade, a meta-analysis identified only five randomized trial studies that examined physician advice to perform dietary restriction during FOBT and their impact on screening adherence [20]. Pignone et al. [20] concluded that a restricted diet does not reduce the false positive results, but it may reduce patient compliance. Similarly, Konrad [12] reported that studies on the effects of dietary restrictions on patient compliance are dated and of suboptimal quality. Although Chapple et al.’s [16] findings suggested that physicians’ personal involvement with patients was crucial in encouraging FOBT screening (versus generalized mail-outs), the nature and content of physicianpatient discussions about FOBT screening remains unclear. This article reports on findings from a larger study that examined perceptions of primary care physicians (referred to as physicians henceforth), patients at average-risk for CRC, and family members or friends on the ‘role of family’ in promoting adherence to recommended FOBT screening [6]. This report focuses on two aspects of our findings. The first aspect involves our analysis of physicians’ beliefs about FOBT and their description of strategies employed to enhance patient adherence to FOBT screening. The second aspect reports on our analysis of patient narration on their awareness of the FOBT and their response to the physician’s recommendation and/or instructions about FOBT screening. 2. Materials and methods The article by Lobchuk et al. described our larger qualitative study that took a tripartite approach in describing the perspectives of physicians, average-risk individuals, and family in promoting adherence to FOBT [6]. A complete discussion of the methods is provided therein, including the setting, sample criteria and recruitment, data collection, the interview guide, and data analyses. Briefly, this study was conducted in urban and rural Manitoba, Canada with an aim to capture a diverse, maximum variation sample [21] of physician, patient, and family or friend responses to FOBT screening. Recruitment of participants and interviews occurred between October 2008 and March 2010. Physicians affiliated with the Uniting Primary Care and Oncology Network in Winnipeg and the Community Cancer Program Network in rural settings in Manitoba were approached to inquire about their willingness to participate in the study [6]. A total of 82 physician invitation letters were sent out and 15 of them agreed to participate in the study and were interviewed. After concluding each physician interview, he/she was requested to identify potential patients and handout an invitation letter to the eligible patients (50 years of age, at average risk of CRC and able to speak and read English). Due to their time constraints, the majority of the interviewed physicians invited the Research Nurse to visit their clinics and approach the identified patients with a letter of invitation. Patients who showed interest in participating in the study were contacted by phone to schedule an interview date and time. A total of 104 invitation letters were distributed to patients and 27 of them agreed to participate and were interviewed After interviewing each patient, he/she was requested to identify a

e260

S.B. Bapuji et al. / Cancer Epidemiology 36 (2012) e258–e264

Table 1 Sample questions from participant scripts. For physicians Can you tell me about your thoughts or beliefs about screening for bowel cancer with FOBT? In your experience, why do you think some patients adhere or not adhere to FOBT screening? For patients and family members or friends Can you tell me about your thoughts and beliefs about FOBT screening? Can you tell me whether your physician was involved with promoting you to do the FOBT? If yes, how the physician was involved with promoting you to do the FOBT.

family member who is influential in their health matters (also 18 years of age and able to speak and read English). Patients were also requested to put the family member in contact with Research Nurse. In this manner, the Research Nurse was able to approach the family members, explain the study and interview them if they were willing to participate in the study. A total of 32 family member invitation letters were distributed and 19 of them agreed to participate and were interviewed. Table 1 displays portion of the respective interview scripts for physicians, patients and family participants that invited them to share their beliefs and knowledge about FOBT screening. An interpretive description approach was used to explore and understand physicians’ views and beliefs about FOBT, FOBT instructions, and reasons for patient adherence or nonadherence to engaging in physician recommended FOBT screening behaviors. Interpretive description [22] employs a grounded approach to articulate patterns and themes emerging in relation to various clinical phenomena that yield implications for clinical application [23]. The validity and authenticity of our findings were confirmed by participants at our larger research team workshop who were primary care physicians, a gastroenterologist, epidemiologists, nurses, and patient advocates. 3. Results Interview data obtained from 15 physicians, 27 patients, and 11 family members (age 50 and above) are included in this report. The article by Lobchuk et al. described the characteristics of this study’s participants in our larger study [6]. Our analyses of data revealed three major themes: ‘‘Variation in physician beliefs about FOBT screening practice’’, ‘‘Concern about lack of uniform instructions provided by the health care team’’, and ‘‘Variation in patient FOBT knowledge and adherence to FOBT instructions.’’ 3.1. Variation in physician beliefs about FOBT screening practices Physician beliefs about FOBT screening practices and FOBT instructions were generally influenced by their awareness of Canadian guidelines about CRC screening methods and their perceptions of the usefulness of FOBT instructions in promoting adherence to FOBT. This major theme was comprised of two overlapping sub-themes that included: the evolution of CRC screening practices and variation in physician buy-in to the FOBT. 3.1.1. Evolution of CRC screening practices All physicians in the study indicated that they were following CTFPHC [2] recommendations by offering FOBT to their patients as part of the annual physical examination. However, our data also suggested that while some physicians approximately 60% were favorable, others were more skeptical about FOBT and held varying beliefs about the sensitivity and specificity of FOBT as a screening tool for CRC. This skepticism was fueled in part by the fact that historically FOBT has been in and out of favor as a recommended screening modality. One physician said, ‘‘It’s been a rocky road. Colorectal cancer screening over my career is gone from doing FOB

testing to saying it’s useless to perhaps for recommending that everybody might have a colonoscopy but that recommendation never came through. And back to FOB testing again. And so it’s been actually kind of a confusing thing for many years now.’’ Another physician said, ‘‘I’ve been in practice 26 years and it’s kind of gone in and out of favor. It’s interesting that the fecal occult blood has come back because there have been several times since I’ve been in practice where it was considered a fairly useless test. So it’s kind of interesting that it’s now come back again and is the test that is being used.’’ 3.1.2. Variation in physician buy-in to FOBT The majority of physicians indicated that, at the time of interview, they were already involved in a provincial initiative to facilitate systematic improvements in the delivery of primary care: for example, they were engaged in quantitative data collection on FOBT screening in their respective practices. As a result, the majority of physicians in this study were motivated to promote FOBT. One physician said, ‘‘Well we did it all the time when I was in training. And then we stopped doing it. And then we started doing it. And then we stopped doing it. And now we are doing it again. . . Well I am definitely promoting it more than I used to, well partly because of the Physician Integrated Network (PIN6). I think that helps motivate because they [PIN] are capturing [FOBT] data.’’ However, some physicians reported not being very satisfied with recommending the FOBT to their patients. As one physician said, ‘‘Well certainly it’s [FOBT] not a 100% for sure test because we certainly have cases where there are negative tests and patients show up with cancer sometime down the road.’’ Another physician said, ‘‘We’re very happy with mammograms for women. Quite happy with PSA and digital rectal exam for males for prostate cancer. And, with colorectal with the occult blood somewhat happy. . .. I know the task force recommends it. Getting colonoscopy done here in this province is difficult. Waiting times right now are six months to a couple of years. The occult blood tests that I’ve had positive the last five in a row have all turned out to be negative on the colonoscopy. I wish we had something a little bit more sensitive for the cancer process. But for right now it’s all we have so we use it.’’ In contrast, other physicians indicated their satisfaction with research evidence that has shown improved mortality rates with FOBT screening. One physician said, ‘‘Well over the years there’s been lots of back and forth on a number of screening issues and there continues to be debate about what ages to start screening and what not and that does create some confusion in the mind of physicians and in patients. My personal feeling is we need evidence and if we have evidence, we should do it. Now since the recommendations have come out more clearly that we should be doing it, we try to screen all of our patients between the ages of 50 and 70 with FOBT.’’ In keeping with CTFPHC guidelines, physicians indicated that if the FOBT result was positive then they ordered a colonoscopy. Although some of these physicians reported that they do not follow research closely, they continued to adhere to the CTFPHC recommendations. Some physicians mentioned that they introduced FOBT to patients at the age of 40 years if their patients had a relative who was diagnosed with CRC after the age of 60. One of the physicians said, ‘‘Doing FOBT and looking at it in conjunction with hemoglobin is a responsible use of resources.’’ Another physician said, ‘‘Offering sigmoidoscopy along with FOBT would have been better but the province is not prepared to pay for it.’’ 3.2. Concern about lack of uniform instructions provided by the health care team The second major theme, concern about lack of uniform instructions provided by the health care team addressed a range 6

Pay for performance type of situation.

S.B. Bapuji et al. / Cancer Epidemiology 36 (2012) e258–e264

of health care team practices or behaviors in relation to CRC screening counseling and FOBT screening. The majority of the physicians distributed FOBT requisition forms to patients during scheduled annual physical examinations. These physicians then directed patients to collect the FOBT kit from the laboratory technician, receptionist, or clinic nurse. Although these physicians directed their patients to the lab technician or the clinic nurse for further instructions, these physicians were not sure about what FOBT instructions were actually being provided to their patients. One physician said: ‘‘One little problem. I may say to the patient don’t worry about stopping your aspirin or eating red meat. And yet the lab is the provider of the test and gives them written instructions to do opposite to what I say. That could actually drive a wedge of mistrust between the provider, the lab and the physician. So, I think is a bit of a problem. Need to have uniform instructions for patients across the province as opposed to different sets of instructions.’’ Another physician said: ‘‘I don’t do it beyond the instructions. I give them instructions and just mention that they should read this because they are pretty clear directions. Actually you know something; it’s our nurses that give out these kits. So, I don’t know what they say.’’ The remaining physicians indicated that they clearly instructed patients to not follow any FOBT instructions about diet or medications, or instructions they might receive from the lab technician or anyone else (e.g., family or friends) about doing the FOBT. One physician said, ‘‘They come with all sorts of instructions or maybe even the lab personnel will talk to you about how to do this. But I’m telling you, ignore all those instructions, none of them have ever been shown to be valuable and all they do is prevent patients from collecting their stool test. And so ignore it all. Just go home, pick 3 days, do it and bring them back in.’’ 3.2.1. Variation in physician instruction content to patients While the second major theme, in the above, captured physicians’ concerns about variation in instruction content by other health care providers, this sub-theme captured the type of information that a smaller number of physicians provided ‘directly’ to their patients about dietary and medication restrictions over the course of taking this unique self-sampling test. When providing the FOBT kit ‘directly’ to the patient, some of these physicians asked the patient to read the kit instructions carefully before taking the test and others downplayed the FOBT instructions by asking patients to completely ignore them. The following excerpts capture this variation in physician instructions to patients. The first type of instructions was ‘to carefully follow physician instructions’. One physician stated, ‘‘I give the hemocult card. I tell them that they need to limit their intake of red meats and that they need to avoid taking iron supplements or Vitamin C or using inflammatory drugs during the collection period. I tell them to read the instructions carefully.’’ The second type of instructions was to ‘somewhat follow instructions’. One physician stated, ‘‘I usually tell them to try and avoid what it says to avoid but not to worry too much about what it says to eat because I find that if you give people too many restrictions, they just won’t bother doing the test. So I do try and tell them to avoid, you know, a lot of red meat or aspirin or things like that. But it also has some things it tells you to eat and I usually tell them not to worry too much about that.’’ The third type of instructions was to ‘completely ignore instructions’. One physician said, ‘‘We do not actually insist on that [instructions] just because it’s so hard to get people to do that [FOBT] then. If you insist on the dietary requirements and so on, then, uh, your rate of getting the result back is so small. They [patients] just say, well I couldn’t follow that. Or, five times I went to do the test and I remembered I’d eaten something I shouldn’t have the night before and therefore I didn’t do it. And so we just, we downplay that side of it. So if you have a negative result and they’ve been eating meat, it’s still a good result. . .. if it comes back positive, they go for a colonoscopy. I don’t care whether they’ve been eating things or not. It’s just a practical way of dealing with

e261

this.’’ Another physician said, ‘‘So often it seems that compliance is hindered because of the recommendations that are presented with the FOB tests. . .. So I always tell my patients, ignore everything they tell you and everything that you read with regards to the screening and just do it. Don’t change your lifestyle. Don’t change your medicines. Don’t change your diet. Just do the screening’’. 3.3. Variation in patient FOBT knowledge and following FOBT instructions The third major theme, variation in patient FOBT knowledge and following FOBT instructions captures patient perceptions about their knowledge of FOBT screening, their sources of FOBT information, and how they followed instructions and collected the stool samples. This theme is subdivided into two sub-themes: Patient knowledge and sources of information and Patient instruction reception, ability to follow instructions, and collect sample. 3.3.1. Patient knowledge and sources of information For this sub-theme, the majority (approximately 80%) of patients indicated that they were informed about CRC screening by their physician. One patient said, ‘‘Well he [doctor] explained to me that he’s doing this [FOBT] because it’s once a year. He gives a check-up, you know. You go for a physical check-up once a year. And all this has to be done and included in the check-up. So he gave the paper and he said, you don’t have to come, just put it in the mail.’’ Other patients mentioned sources such as a relative or a friend, poster information, and mailed information. A minority of patients stated that they never heard of CRC or FOBT. Most patients (approximately 80%) indicated that they had received the FOBT requisition from the physician and upon showing the physician requisition to the laboratory technician or a nurse they received the FOBT kit. The remaining participants described that they had either received a FOBT kit from the physician or nurse in the clinic, laboratory technician, receptionist at the mammogram clinic, or in the mail shortly after their 50th birthday. Some even received the kit from multiple sources (i.e., from the physician and in the mail). Overall, the type or detail of instructions received from the numerous sources was variable ranging from receiving no instructions (approximately 30% of the participants) to a detailed explanation (approximately 25%) of how to collect the sample. Approximately 45% of the participants received some FOBT instructions. With detailed instructions, one patient said, ‘‘it was written instructions and it was from the lab. But each time I go to the lab with this test they do hand out written instructions because there is diet that goes that you have to do when you’re doing this test.’’ When some patients received the FOBT kit in the mail, without any prior notification from their physician, they discarded the FOBT kit. Other patients, who received the FOBT kit from their physician with instructions to ‘just do it’, tended to procrastinate in collecting the stool sample. Overall, the majority of participants perceived that receiving the FOBT kit from their physician along with an explanation would help them to adhere to recommended screening in comparison to a generalized mail-out of the kit to eligible individuals. 3.3.2. Patient instruction reception, ability to follow instructions and collect sample All the adherent patients mentioned that they received instructions from their physician which accompanied the FOBT kit. However, patients’ responses varied when the research nurse explicitly asked about their opinion about dietary and medication instructions. While some patients said that they followed dietary and medication instructions, other patients stated that they followed a normal diet and took their medication as usual. It was unclear if the patient’s decision to follow or not follow dietary

e262

S.B. Bapuji et al. / Cancer Epidemiology 36 (2012) e258–e264

and medication instructions was based on the physician’s opinion, written instructions, or a self-determined decision. One patient said: ‘‘he [doctor] said, you have to watch your diet ahead of time for it. So that’s one thing you have to think of ahead of time and as far as doing it, just follow the instructions on the package.’’ Another patient said: ‘‘Doctor said you follow your regular diet and they didn’t tell me to eat anything special or go on any special diet. But I just follow the kit instructions and, you know, do what the instructions say.’’ Similarly, when asked about the steps taken during the sample collection, it appeared that some patients misinterpreted the instructions on how to collect the stool sample. For instance, rather than collecting a stool sample from one bowel movement each day, some patients collected stool samples from three consecutive bowel movements on the same day. Physician recommendations about adhering to dietary or medication restrictions had a major influence on how participants engaged in doing the FOBT test. There were some participants who received the package without any explanation from the physician or another health care provider (e.g., clinic nurse or laboratory technician). One patient said, ‘‘I find that whoever gives you the FOBT little package doesn’t give you a lot of information orally. They just tell you to read what’s inside and to do it. I am not sure whether its time factor for the people who are giving it to you or whether they don’t want to talk about it.’’ Some of these patients followed the manufacturer’s instructions, ‘‘You have to watch what you eat a few days prior to and during the test. Stay away from red meat. . . those kind of things.’’ Other patients either procrastinated in taking the test or did not follow the instructions as given along with the kit. 4. Discussion This report focused on two aspects of our findings. The first aspect focused on physicians’ beliefs about FOBT and their description of strategies employed to enhance patient adherence to doing FOBT screening. The second aspect focused on patients’ reports about their awareness of the FOBT and their responses to their physician’s recommendation and/or instructions about engaging in FOBT screening. Our themes reflected variation in physician beliefs about FOBT screening practice and modes of FOBT kit distribution and instruction delivery, and patients’ FOBT knowledge and adherence to FOBT instructions. Over time, with the evolution of evidence, FOBT has fallen ‘in and out of favor’ with physicians. Our findings indicated that physicians held varying beliefs about the sensitivity and specificity of FOBT as a screening tool for CRC. Similarly, physicians’ perceptions varied about the need to adhere to dietary and medication restriction in preparing to collect samples for FOBT. The literature indicates that FOBT results were not impacted by restrictions in diet in three large randomized trials involving FOBT. In other words, there was no difference in FOBT test outcomes involving two studies where patients were placed on a restricted diet [4,24] and a third study where patients were not placed on a restricted diet [25]. While there appears to be a paucity of literature that examined variation in FOBT counseling, there is some evidence that suggested the variation in health care practices can have a profound effect on the quality of care and system costs [26–31]. We also found that while the majority of patients received a FOBT requisition from their physician, FOBT kits and instructions were provided by a range of health care providers. Likewise, there appeared to be a marked variation in the information provided on credible cancer agency websites regarding patient preparation for FOBT. For instance, the Canadian Cancer Society’s website indicates that in preparation for FOBT, no red meat should be consumed, and that medication such as Ibuprofen and Vitamin C should not be taken before or during sample collection days [1]. As mentioned earlier, CancerCare Manitoba’s website provides FOBT instructions

that differ from instructions provided on the Ontario Colon Cancer Check’s website. Overall, it appears that patients might not be receiving uniform FOBT counseling from health care providers and instructions from cancer agency websites. There are some studies that examined physician reported barriers to CRC screening (e.g., [13]). However, the literature is sparse with regard to counseling content about dietary and medication restrictions that physicians share with their patients about FOBT and the impact of dietary restrictions [32]. This study is one of the first to explore physician beliefs about FOBT and counseling behaviors. Finally, we found that there was variation in patients’ FOBT knowledge and adherence to FOBT instructions. Several participants reported that they received FOBT requisition forms from their physicians. Participants also described that when they received the FOBT kit, they did not always receive instructions on how to do the FOBT from different health care providers. On the other hand, it appears that when physicians took time to provide patients with information about CRC and FOBT screening, patients described their tendency to adhere to FOBT screening recommendations. This finding supports growing evidence for the importance of physician recommendation for patients to engage in CRC screening [8,13,17]. Similarly, previous research supports our findings that FOBT instructions are confusing and burdensome [16]. As described in the above, guidelines about how to engage in the FOBT test vary across Canada. To the best of our knowledge, there is no other literature that has captured the content of screening counseling by physicians for patients to properly engage in CRC screening tests, like FOBT (e.g., specific instructions about dietary and medication restrictions) and the impact of physician instructions about dietary and medication restrictions on patient behavior when engaging in the FOBT. Several limitations to this study warrant further discussion. First, this study was based on a small convenience sample of participants who were recruited from one urban area and six rural areas in one province in western Canada. Second, physician participants were affiliated with networks that linked primary care physicians with the oncology health care system in the province: thus, this affiliation likely impacted physician screening counseling behaviors. Of interest, however, our findings indicated that physicians’ behaviors in this study were not all similar in following CRC guidelines as evidenced by their reports of variable instructions provided to patients. Some physician clinics in this study were involved with a provincial initiative to facilitate systemic improvements in the delivery of primary care that targeted colorectal cancer screening rates. The inclusion of these clinics pose a caveat in being able to generalize findings to physicians in other primary care settings, nurse practitioners, and community care nurses who are involved with cancer screening. Third, our study did not have the opportunity to include immigrant or minority populations whose awareness, beliefs, and values about CRC screening recommendations may vary from our study sample. Despite these limitations, this study is the first of its kind to examine more closely the beliefs of physicians about FOBT screening recommendations and the impact of physician counseling on CRC screening behaviors of their patients who are at average risk for CRC. To conclude, our study findings indicated that primary care physicians do not follow a standardized regimen with patients during counseling sessions about CRC screening and instructions about the FOBT. Even though this study’s physician participants were affiliated with the same provincial cancer agency that endorses guidelines for CRC screening, variability in their respective CRC screening instructions existed. The evolution of evidence that inconsistently supports current CRC screening recommendations appeared to have had an effect on physician ‘buy-in’ about the feasibility, sensitivity, and specificity of the

S.B. Bapuji et al. / Cancer Epidemiology 36 (2012) e258–e264

FOBT. Furthermore, equivocal evidence on dietary and medication restrictions likely supported physician perceptions that FOBT instructions are cumbersome for patients: thus inconsistent recommendations to continue with one’s regular diet and medication regimens are made by physicians. Depending on the physician’s confidence in the evidence to support current CRC screening recommendations and the patient’s unique circumstances, variability in physician counseling behaviors will likely remain. Moreover, the source (i.e., physicians, nurses, laboratory technicians, or other clinic personnel) of instructions for patients to engage in FOBT screening can also mediate variability in how patients are instructed to prepare for the FOBT. It is important for primary care providers to consider the significance of a trusting relationship with their patients and how they actually impart screening test instructions as major factors in promoting patient adherence. Our results have implications for clinical practice since they provide evidence that patients often receive different FOBT screening instructions from various health care providers (i.e., physicians or nurses in primary care clinics, laboratory technicians, health care providers at breast screening clinics, and mass mail outs) which can impact patients’ successful execution or adherence to doing FOBT. It is unclear from the literature whether the restriction of certain food items or medicines produces clinically important differences in test accuracy. Nevertheless, we believe that these findings should encourage health care providers, like physicians and nurse practitioners in primary health care, to question whether the degree of practice variation within the field is desirable in terms of its impact on quality of care and cost to the system (i.e., costly follow-up colonoscopies that reveal negative results). Our study identified that patients received the FOBT kit and instructions from a range of health care providers who provided varied or no instructions to properly execute the FOBT. Further studies are required to capture the exact content of instructions (e.g., recommendations for diet and medication restrictions) that patients might receive about the FOBT and the impact of different health care providers (i.e., physicians, nurses, laboratory technicians, or cancer screening office personnel) on patient behaviors involving the FOBT. Until such studies are conducted, we believe that our findings imply a need for health care providers involved in CRC screening to discuss the issue of variance in instructions about FOBT screening. Conflict of interest None of the authors in this study have any financial or personal relationships with other people or organizations that could inappropriately influence (bias) the work contained within this paper. Funding source This research is supported by a New Emerging Team (NET) Grant provided by the Canadian Institutes of Health Research and CancerCare Manitoba. Acknowledgments We thank all members of the CIHR/CCMB Team in Primary Care Oncology (listed): Jennifer Baker, Yvonne Block, Sid Chapnick, Joanne Chateau, Dr. Habtu Demsas, Herold Driedger, Jeanette Edwards, Melissa Fuerst, Marion Harrison, Dr. Duane Hartley, Scott Kirk, Dr. Gerald Konrad, Dr. Yatish Kotecha, Paul Nyhof, Dr. Sunil Patel, Dr. Harminder Singh, Diane Stolar, Dr. Karen Toews, Dr. Debrah Wirtzfeld, Dr. Cornelius Woelk, and the physicians,

e263

patients, family members and friends who agreed to participate in the study. Dr. Michelle Lobchuk acknowledges funding from her Manitoba Health Research Council Chair in Caregiver Communication. Dr. Patricia Martens acknowledges funding from her CIHR/ PHAC Applied Health Chair.

References [1] Canadian Cancer Society’s Steering Committee. Canadian cancer statistics 2011. Toronto: Canadian Cancer Society, 2011. [2] Canadian Task Force for Preventive Health Care. Colorectal cancer screening. Can Med Assoc J 2011;165(2):206–8. [3] Heresbach D, Manfredi S, D’halluin PN, Bretagne JF, Branger B. Review in depth and meta-analysis of controlled trials on colorectal cancer screening by fecal occult blood test. Eur J Gastroenterol Hepatol 2006;18(4):427–33. [4] Mandel J, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood Minnesota colon cancer control study. N Engl J Med 1993;328(19):1365–71. [5] CancerCare Manitoba. Coloncheck CancerCare Manitoba: frequently asked questions, http://www.cancercare.mb.ca/home/prevention_and_screening/ general_public_screening_programs/manitoba_colorectal_screening_program/frequently_asked_questions/; 2011 [accessed 12.12.11]. [6] Lobchuk MM, Bapuji SB, McClement SE, Sisler J, Katz A, Martens P, et al. What is the role of family in promoting faecal occult blood test screening? Exploring physician, average-risk individual, and family perceptions. Cancer Epidemiology (2012), doi:10.1016/j.canep.2012.01.002, in press. [7] Green PM, Kelly BA. Colorectal cancer knowledge, perceptions, and behaviours in African Americans. Cancer Nurs 2004;27(3):206–15. [8] Honda K. Factors associated with colorectal cancer screening among the US urban Japanese population. Am J Public Health 2004;94(5):815–22. [9] Shokar NK, Vernon SW, Weller SC. Cancer and colorectal cancer: knowledge, beliefs, and screening preferences of a diverse patient population. Fam Med 2005;37(5):341–7. [10] Zarychanski R, Chen Y, Berstein CN, Hebert PC. Frequency of colorectal cancer screening and the impact of family physicians on screening behaviour. Can Med Assoc J 2007;177(6):593–7. [11] Wilkins K, Shields M. Colorectal cancer testing in Canada – 2008. Health Rep 2009;20(3):21–30. [12] Konrad G. Dietary interventions for fecal occult blood test screening – systematic review of the literature. Can Fam Physician 2010;56(3):229–38. [13] Klabunde CN, Vernon SW, Nadel MR, Breen N, Seeff LC, Brown ML. Barriers to colorectal cancer screening: a comparison of reports from primary care physicians and average-risk adults. Med Care 2005;43(9):939–44. [14] Janz NK, Wren PA, Schottenfeld D, Guire KE. Colorectal cancer screening attitudes and behaviour: a population-based study. Prev Med 2003;37(6 Pt1):627–34. [15] Leslie NS, Deiriggi P, Gross S, DuRant ME, Smith C, Veshnesky JG. Knowledge, attitudes, and practices surrounding breast cancer screening in educated Appalachian women. Oncol Nurs Forum 2003;30(4):659–67. [16] Chapple A, Ziebland S, Hewitson P, McPherson A. What affects the uptake of screening for bowel cancer using a faecal occult blood test (FOBT): a qualitative study. Soc Sci Med 2008;66(12):2425–35. [17] Wackerbarth BS, Tarasenko YN, Joyce JM, Haist SA. Physician colorectal cancer screening recommendations: an examination based on informed decision making. Patient Educ Couns 2007;66(1):43–50. [18] Sharma VK, Vasudeva R, Howden CW. Colorectal cancer screening and surveillance practices by primary care physicians: results of a national survey. Am J Gastroenterol 2000;95(6):1551–6. [19] Vernon SW. Participation in colorectal cancer screening: a review. J Natl Cancer Inst 1997;89(19):1406–22. [20] Pignone M, Campbell MK, Carr C, Phillips C. Meta-analysis of dietary restriction during fecal occult blood testing. Eff Clin Pract 2001;4(4):150–6. [21] Coyne IT. Sampling in qualitative research. Purposeful and theoretical sampling: merging or clear boundaries? J Adv Nurs 1997;26(3):623–30. [22] Thorne S, Kirkham SR, MacDonald-Emes J. Interpretive description: a noncategorical qualitative alternative for developing nursing knowledge. Res Nurs Health 1997;20(2):169–77. [23] Thorne S, Kirkham SR, O’Flynn-Magee K. The analytic challenge in interpretive description. Int J Qual Methods 2004;3:1–11. [24] Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O. Randomized study of screening for colorectal cancer with faecal-occult-blood test. Lancet 1996;348(9040):1467–71. [25] Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, Amar SS, Balfour TW. Randomized controlled trial of fecal-occult-blood screening for colorectal cancer. Lancet 1996;348(9040):1472–7. [26] Wennberg DE. Variation in the delivery of health care: the stakes are high. Ann Intern Med 1998;128(10):866–8. [27] Anderson C. Promoting oral health: nurses and pharmacists working together. Brit J Community Nurs 1998;3(1):41–4. [28] Yan W. Evaluation on ability of health education and health promotion of medical staff in Haidian district. Modern Preventive Medicine 3, http:// en.cnki.com.cn/Article_en/CJFDTOTAL-XDYF200803057.htm; 2008 [accessed 12.12.11].

e264

S.B. Bapuji et al. / Cancer Epidemiology 36 (2012) e258–e264

[29] Melia J, Coulson P, Moss S, Coleman D. Effects of a prostate awareness pilot on GP consultations and PSA requests. Fam Pract 2010;27(1):69–76. [30] A’Campo LE, Wekking EM, Spliethoff-Kamminga NG, Le Cessie S, Roos RA. The benefits of a standardized patient education program for patients with Parkinson’s disease and their caregivers. Parkinsonism Relat Disord 2010;16(2): 89–95.

[31] Lee SJ, Joffe S, Artz AS, Champlin RE, Davies SM, Jagasia M, et al. Individual physician practice variation in hematopoietic cell transplantation. J Clin Oncol 2008;26(13):2162–70. [32] Burch JA, Soares-Weiser K, St John D, Smith S, Kleijinen J, Westwood M. Diagnostic accuracy of faecal occult blood tests used in screening for colorectal cancer: a systematic review. J Med Screen 2007;14(3):132–7.