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Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening
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ARTICLE IN PRESS Digestive and Liver Disease xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Digestive and Liver Disease journal homepage: www.elsevier.com/locate/dld
Oncology
Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening Fanny Le Pimpec a , Grégoire Moutel b , Christine Piette c , Astrid Lièvre d,e,f , Jean-Franc¸ois Bretagne c,d,e,∗ a
Département de médecine générale, Faculté de médecine, Université de Rennes 1, France Normandie Univ, Unicaen, Inserm U1086, Cancers et préventions, et CHU Caen, Caen, France c Association pour le dépistage des cancers en Ille-et-Vilaine (ADECI 35), Rennes, France d Service des maladies de l’appareil digestif, CHU Rennes, Rennes, France e Université de Rennes 1, Rennes, France f Inserm ER440-Oncogenesis, Stress and Signaling, Université de Rennes 1, Rennes, France b
a r t i c l e
i n f o
Article history: Received 11 May 2017 Received in revised form 29 June 2017 Accepted 1 August 2017 Available online xxx Keywords: Barriers and facilitators Colorectal cancer screening Fecal occult blood test Fecal immunological testing
a b s t r a c t Background: The reasons for participation in fecal immunological testing (FIT) of subjects who were previously non-respondents to guaiac fecal occult blood testing (g-FOBT) have not been assessed. Population and methods: We aimed to determine the reasons for current compliance with FIT among non-responders to g-FOBT, termed “converts”, in a French district. A questionnaire was returned by 170 converts aged from 55 to 75 years (response rate 75.2% after exclusions). Results: The major barriers to participation in screening with g-FOBT were test-related: the test was perceived as complicated (24%) and it required three consecutive stools (28%). Among the test-related major determinants of FIT compliance was the perception that the test was less complicated than previous test (30%) and that a unique stool sample was required (29%). Among the non-test related major determinants of FIT compliance were the perception that the general practitioner was more convincing (31%) and the feeling to be more concerned because of age (21%). The reasons for compliance among converts did not differ according to age, sex, and rural or urban residence. Conclusions: Our study demonstrated that the simplicity of FIT and the endorsement of practitioners were both major motivations for FIT compliance among non-respondents in at least two previous consecutive campaigns. © 2017 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.
1. Introduction Worldwide, colorectal cancer (CRC) is the third most common cancer in men and the second in women [1]. Organized and opportunistic screening programmes have been implemented throughout many countries to decrease the incidence and mortality rate of CRC [2]. Most European countries with an organized screening programme screen by means of a non-invasive stool test. Previously implemented guaiac fecal occult blood testing (g-FOBT)based programmes are being replaced by fecal immunologic testing (FIT) [2]. This is the case in France where the g-FOBT programme, which was instituted in 2003 and was implemented nationwide in 2008, was replaced by FIT in 2015. Similar to other programs, the French g-FOBT screening programme has faced disappointingly
∗ Corresponding author at: Service des maladies de l’appareil digestif, centre hospitalo-universitaire, 35033 Rennes, France. Fax: +33 2 99 28 41 89. E-mail address: [email protected] (J.-F. Bretagne).
low participation rates. While the European guidelines for quality assurance in CRC screening recommend a minimum uptake of 45% to keep the programme cost-effective [3], the participation rate in France was estimated to be 34.3% in 2008–2009 [4], which decreased to 29.8% in 2013–2014 [5]. Screening programme organizers expect a decrease in the gap between targeted and observed screening rates due to the switch to FIT because a meta-analysis of direct comparative studies reported that FIT resulted in a higher uptake (16%) compared with g-FOBT [6]. Despite the publication of pilot study results [7,8], the consequence of replacement of g-FOBT with FIT with respect to nationwide compliance is still unknown. A systematic review of factors associated with adherence to CRC screening presented in the literature has identified many factors related to socio-demographic, psychological, environmental, and health care provider-related characteristics [9,10]. To the best of our knowledge, the reasons for participation in FIT-based screening of subjects who were non-respondents to g-
http://dx.doi.org/10.1016/j.dld.2017.08.018 1590-8658/© 2017 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Le Pimpec F, et al. Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening. Dig Liver Dis (2017), http://dx.doi.org/10.1016/j.dld.2017.08.018
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Fig. 1. Flow chart of target and study population.
FOBT screening have not been explored. Therefore, the present study was aimed to assess the reasons for FIT compliance by nonrespondents who we have termed “converts”. These findings might be useful for the improvement of the quality of a nationwide screening programme and thereafter to further increase the observed participation rates. 2. Populations and methods 2.1. Study setting ‘Ille et Vilaine’ was one of the first French districts to implement the national screening programme based on biennial g-FOBT. The target population for screening consisted of asymptomatic men and women aged between 50 and 74 years with no other risk factor for CRC. Individuals with a personal or family history of CRC or adenoma, those with inflammatory bowel disease, and those who had undergone total colonoscopy in the previous five years were excluded from the mass screening programme. When the screening programme was launched in 2003, the total population of ‘Ille et Vilaine’ was 908,449, and the target resident population was 213,635. In 2015, the respective figures were 1,019,923 inhabitants and 223,329 target residents. The participation rate for g-FOBT testing, which was satisfactory during the first campaign in 2003–2004 (51.2%), constantly decreased to 42% in 2013–2014 [11]. High rates (>90%) of compliance with colonoscopy following positive testing were registered during each campaign. The shift from g-FOBT to FIT occurred in May 2015 in this district in France. The OC-Sensor test (Eiken, Tokyo, Japan), which consists of a single sampling tube, has been selected from various versions of FIT. Participants were instructed to scrape different parts of the surface of their stool with the test probe and to return the test by
mail to the central analysis center in a prepaid envelope as soon as possible. The maximum time between the fecal deposit and the processing of the test should be less than 6 days. The test was defined as positive at a cutoff of 150 ng hemoglobin per milliliter of sample solution, which corresponds to 30 g hemoglobin per gram of feces. The screening campaign began when each target subject was sent an information brochure and an invitation letter that invited the subjects to perform the screening test. The first 6 months of the screening campaign (May–November 2015) corresponded to the medical free-offer phase. People were invited to consult their general practitioners (GPs) who propose the screening test to eligible subjects seen at their practice. GPs were also asked to state the exclusion criteria, at which point they provided each eligible individual with one screening test. A reminder letter with the screening test along was sent 6 months later to non-respondents who were not excluded from participation. The screening strategy and the implication of GPs were similar for FIT and g-FOBT delivering. In both cases, their mission was to explain modalities and performance of the test, as well as its expected benefits. 2.2. Study sample In the present study, non-respondents to g-FOBT were defined as individuals who were invited to two or more previous campaigns and never completed the test despite two reminder letters and tests that were sent to them during each campaign. Due to the one year gap between when the use of g-FOBT was stopped and when the use of FIT began in the district, people aged 75 years (one year over 74 years) were also invited during the campaign for FIT. Therefore, the target population for the study consisted of people aged from 55 to 75 years who were born between 1940 and 1960. Among the 28,335
Please cite this article in press as: Le Pimpec F, et al. Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening. Dig Liver Dis (2017), http://dx.doi.org/10.1016/j.dld.2017.08.018
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recorded non-excluded non-respondents, 802 (2.8%) individuals completed FIT. The 551 of the 802 individuals who completed FIT by 1st March 2016 following the first invitation letter, but before the reminder and the test were mailed, comprised the target population for the survey. Finally, the study was restricted to a sample of 300 individuals after drawing lots (Fig. 1). 2.3. Data collection The 300 individuals were contacted by phone by one of the authors (FLP) and were asked to respond to a questionnaire either by phone, by return of the completed questionnaire in a pre-paid envelope, or by completion of the questionnaire via the Internet using the secured LimesurveyTM software, which was at our disposal by the University of Rennes1. Whatever the method used for the collection of the questionnaires, the aim of the study was explained and informed consent was obtained in all cases. The survey, in addition to follow-up phone calls, was conducted between May and August 2016. The questionnaire was generated according to the methods used in the social sciences. The questionnaire consisted of 4 sections. The aim of questions in the first section was to ascertain that individuals did not have contraindications to colorectal cancer mass screening with fecal occult blood test. The second section consisted of questions about sociodemographic characteristics. The third section was devoted to determinants for non-participation to g-FOBT screening before 2015 and for current participation to FIT. In the section four, questions aimed to search potential life changes since the period when individuals were non-respondents to screening. Regarding to the third section the questionnaire was built according to knowledge in the literature about participation – and non-participation determinants [12,13]. For every potential given reason, people have to tick one among 3 responses: 1) Yes, it was a major ground 2) Yes, it was a ground; 3) No, it was not a ground for doing or not doing the test. A major ground for doing the test was translated into top motivation. Furthermore, it was recommended that women should also respond to questions on their behavior regarding screening for gynecologic cancer. 2.4. Statistical analysis The characteristics of the converts, the reasons for noncompliance with g-FOBT and those for compliance with FIT were characterized using descriptive statistics. Given p values are associated with Wald chi-square test statistics. All analyses involved the use of SAS 9.3. 3. Results 3.1. Population Among the sample of 300 individuals, 74 people were unable to be contacted by phone despite four attempts. Nineteen people refused to complete the survey. Twenty-two people were excluded for the following reasons: they were unable to consent or to understand the aim of the survey because of cognitive disorders; they were revealed to be at high risk for CRC so that they should not have completed FIT or were revealed to have previously participated in g-FOBT screening outside the district. Lastly, 15 people did not return the questionnaire by mail despite their initial agreement to do so (Fig. 1). Among the 226 people contacted by phone, the response rate after exclusion was 75.2% (170 of 226 individuals). Among the 170 questionnaires, 115 (68%) were collected by phone interview, which lasted approximately 15 min, while the question-
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Table 1 Socio-demographic characteristics of the converts (n = 170). Study population n = 170 Sex Women Men
78 (45.9%) 92 (54.1%)
Age 55–59 years 60–64 years 65–69 years 70–75 years
47 (27.6%) 58 (34.1%) 44 (25.9%) 21 (12.4%)
Residence Rural Urban
78 (45.9%) 92 (54.1%)
naires of other attendees were collected by mail or via the Internet in 32 and 23 cases, respectively. Socio-demographic characteristics of the study population are given in Table 1. These characteristics did not differ from those of the target population of the survey (data not shown). Both groups were composed of more men than women, which was different than the sex distribution in g-FOBT attendees during the previous (2013–2014) campaign (women 54.5%). Among the 78 women who completed the survey, 57 (73%) declared their participation in breast cancer screening during the previous two years, while only 27 (42.8%) of the 63 women younger than 68 years of age declared that they did undergo cervical cancer screening. Since the period of time when they were considered nonrespondents to CRC screening, most survey attendees stated that they experienced no changes in their social, professional, familial, or financial position (Fig. 2). Nevertheless, 33% of the 170 survey attendees stated that they now have more free time because of retirement and a decrease in professional responsibilities; 31% declared that they have more health problems (Fig. 2).
3.2. Barriers to CRC screening by g-FOBT before 2015 Barriers to participation in CRC screening before 2015 are listed in Fig. 3. The major grounds were related to the method used for testing, which was perceived as complicated (24%), the need for three consecutive stool samples (28%) and the repulsive nature of the test since it requires contact with stool (16%). Negligence (19%), feelings of non-concern in the absence of symptoms (16%) and the fear of a cancer diagnosis (11%) were also recorded as major grounds for lack of participation. The lack of concern due to healthy lifestyle or age was recorded as a major ground in 9% of converts. The absence of cancer within the family was often recorded as a simple ground (40%), but it was a major ground in only 5% of converts. The lack of suggestion for CRC screening by GPs, the lack of free time, and the fear of a follow-up colonoscopy were recorded as major grounds in 6%–7% of cases. The distribution of barriers did not differ greatly according to sex, age and rural or urban residence. The differences we found statistically significant between groups were as followings: the lack of concern because of their age was more frequently recorded in men (43%) than in women (17%) (p < 0.05). Conversely, tests that require three consecutive stools were more frequently recorded as a barrier in women (61%) than in men (45%). The lack of free time was more frequently recorded in younger (55–64 years, 25%) individuals than in older (65–75 years, 11%) individuals. The perceived disgust in the manipulation of stools was more frequently recorded in urban residents (40%) than in rural (23%) residents.
Please cite this article in press as: Le Pimpec F, et al. Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening. Dig Liver Dis (2017), http://dx.doi.org/10.1016/j.dld.2017.08.018
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Fig. 2. Potential life changes since the period of time when the 170 converts were non-respondents to screening.
Fig. 3. Distribution of barriers to screening by g-FOBT in the 170 converts.
3.3. Reasons for compliance to FIT
3.4. The role of general practitioners
Greater concern because of aging was the most often (67%) recorded ground for compliance, but it was given as a major ground by only 21% of the survey respondents. The major grounds or top motivations most frequently cited were that the GP was more convincing than before implementation of FIT (31%), the FIT was perceived as less complicated than g-FOBT (30%) and that a unique stool sample was required (29%). The feeling of concern despite the absence of symptoms was also a frequent ground (47%), but it was stated as a top motivation by only 15% of the survey respondents. Other grounds are listed in Fig. 4. Among the 58 (34%) converts who knew that FIT was more reliable than g-FOBT, 71% of them believed that the reliability encouraged them to complete FIT. Facilitators did not differ significantly according to the sex, age and rural or urban residence of the survey participants.
The majority (68%) of survey respondents claimed to have the same GP while 29% had changed their GPs. Most respondents (54%) found that the explanations given by their GP regarding the test procedure were more lucid; 45% perceived that the GP had spent more time and 45% thought that the explanations given by their GPs regarding CRC screening in general were more lucid. Most people who found that their GP was more convincing and gave this as a top motivation for FIT compliance, belonged to one of the latter three groups.
4. Discussion The present study aimed to determine the reasons for compliance to FIT in non-respondents to g-FOBT, who we have termed
Please cite this article in press as: Le Pimpec F, et al. Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening. Dig Liver Dis (2017), http://dx.doi.org/10.1016/j.dld.2017.08.018
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Fig. 4. Distribution of facilitators to screening by fecal immunological testing in the 170 converts.
“converts”. The survey involved 170 converts who ranged in age from 55 to 75 years. The majority was composed of men (54.1%), which is unusual in screening-compliant populations in nationwide CRC screening programs based on g-FOBT [4,14]. The most frequent reasons quoted by converts as a top motivation for compliance emphasized both the endorsement and involvement of GPs, and the simplicity of the screening test. We reported that 50% converts perceived their GP as more convincing than before implementation of FIT, which was a determinant for participation. GPs gave more lucid explanations of the FIT procedure and CRC screening and spent more time on these explanations than in the past. Our results allow us to make the hypothesis that GPs were more motivated to present the new test because it was more reliable but also simpler to realize. GPs were sensitized on these two points during the implementation of the FIT through a new national information and training campaign. That is probably why patients perceived the FIT as better and accepted to do it more easily. Thus, the new test was directly or indirectly responsible of the participation of converts. The GP is often one of the interlocutors who is most knowledgeable about the psychology and reticence of his patients. Once convinced of the importance of screening, he is able to “lift the brakes” so to speak, to inform and explain the procedure to the patient. The physician’s attitude and discourse are important in adherence to screening. The quality of the doctor-patient relationship appears to be one of the key elements of the screening system [15,16]. It is well known that physician recommendations motivate individuals to undergo screening [16–19], but we suspect in the present study, that behavior changes of GPs might be linked to the higher performance of FIT compared with that of g-FOBT, which rendered GPs more confident in the new test and more comfortable in the discussion of the test with their patients. This indirect benefit of FIT is not easy to assess. Most of the GPs in the district had participated to training sessions before the replacement of g-FOBT with FIT, and therefore, they were aware of the reliability of the new test. Doctor-patient communication has been shown to be one of the possible targets for the improvement of patient adherence and the participation rate in the target population [20]. The present study did not aim to assess whether converts completed FIT to please their doctor, as has been previously suggested [13]. Only one third of the converts declared that they knew that FIT was a more reliable screening test than gFOBT. However, interestingly, among these patients, 71% declared that the performance of the new test was a determinant for their participation. This finding could have significance for the French
nationwide screening program and should prompt improvement in the communication of FIT performance to patient populations. As expected, test-related determinants were found to have a large role in participation in screening by converts. The perception that FIT was less complicated and that it required a unique stool sample was quoted as a determinant for participation in 55% and 54% of converts, respectively. Furthermore, 25% of converts mentioned that FIT was less repulsive than g-FOBT. We then related these findings with those for non-compliance to g-FOBT. Among the most frequently mentioned reasons for non-compliance in the present study demonstrated that the HemoccultTM test was previously perceived as complicated (50%). Another reason, mostly given by women (61%), was that this test required 3 consecutive stool samples (52%). Finally, 32% of converts mentioned that the test was repulsive because of stool contact. Even if the relationship between perceptions and participation is not as clear as one might expect [21], these findings could explain why comparative studies of both non-invasive tests demonstrated higher participation rates with FIT than g-FOBT [6]. Nevertheless, most of these studies were conducted in previously unscreened populations. FIT pilot studies conducted within a “live” screening program reported that overall uptake increased by over 7–9.5% points with FIT compared with g-FOBT [7,8] and that uptake of previous non-respondents to g-FOBT was doubled (FIT 23.9% vs g-FOBT 12.5%) [8]. However, none of these comparative studies was aimed to determine the reasons for better compliance to FIT. Our results are in agreement with findings from an intentionto-screen study that assessed the attitudes towards the g-FOBT versus FIT in a Scottish population [22]. In the latter study, participants reported a higher intention to complete and return the FIT materials versus the g-FOBT, which was largely due to a perception that FIT was easier and less repulsive to complete [22]. The present study has some limitations. First, the target population was restricted to converts who responded during the medical free-offer phase before the second letter and the FIT materials were mailed. As the campaign did not end, we did not know the precise proportion of individuals who later became compliant with FIT, or whether the determinants for compliance were similar in both groups of converts. Nevertheless with the data available at the present time of the first campaign with FIT, we could expect a participation rate of 52–55%, as compared to 42% for the previous campaign with g-FOBT. Second, the survey respondents were questioned retrospectively with a time delay that ranged from 4 months to 10 months after completion of the test, and thus we cannot exclude bias in the collection of data. Third, while most sur-
Please cite this article in press as: Le Pimpec F, et al. Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening. Dig Liver Dis (2017), http://dx.doi.org/10.1016/j.dld.2017.08.018
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vey participants were interviewed by phone, we cannot exclude bias among the different modalities used to complete the questionnaires. Fourth, while we suspect that most of the non-respondents to g-FOBT will remain non-respondents to FIT at the end of the first campaign, the reasons for this remain to be determined. It will be of interest to assess if the determinants for the participation of converts identified in the present study could improve most the CRC screening-resistant population, even if a range of approaches may be required to improve screening uptake. Finally, the lack of control group could be a limitation of the study. Comparing the barriers to screening in definitive non-responders with that of converts would add much to our understanding to screening. But unfortunately, we presume that the response rate to survey of definitive non-responders to screening should be very low. Furthermore, comparing the reasons for compliance of converts selected at the medical free-offer phase of the screening round and those of converts selected after the mailing of the test would add much to our understanding. In conclusion, our study demonstrated that the simplicity of FIT and the endorsement of GPs were both major determinants for compliance to FIT among converts. These latter, along with the higher performance of FIT, could positively influence the participation of people resistant to colorectal cancer screening by g-FOBT. Conflicts of interest The authors Fanny Le Pimpec, Grégoire Moutel, Christine Piette, Astrid Lièvre, Jean-Franc¸ois Bretagne have no conflicts of interest or financial ties to disclose with regard to this article. References [1] IARC. Estimated cancer incidence, mortality, and prevalence worldwide in; 2012 http://globocan.iarc.fr/Pages/fact sheets cancer.aspx. [2] Schreuders EH, Ruco A, Rabeneck L, Schoen RE, Sung JJ, Young GP, et al. Colorectal cancer screening: a global overview of existing programmes. Gut 2015;64:1637–49. [3] Minozzi S, Armaroli P, Segnan N. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition–principles of evidence assessment and methods for reaching recommendations. Endoscopy 2012;44(Suppl. 3):SE9–14. [4] Leuraud K, Jezewski-Serra D, Viguier J, Salines E. Colorectal cancer screening by guaiac faecal occult blood test in France: evaluation of the programme two years after launching. Cancer Epidemiol 2013;37:959–67. [5] INCa Participation au programme national du dépistage organisé du cancer http://lesdonnees.e-cancer.fr/Themes/Depistage/Le-depistagecolorectal. du-cancer-colorectal/Taux-de-participation-au-programme-national-dudepistage-organise-du-cancer-colorectal.
[6] Hassan C, Giorgi Rossi P, Camilloni L, Rex DK, Jimenez-Cendales B, Ferroni E, et al. Meta-analysis: adherence to colorectal cancer screening and the detection rate for advanced neoplasia, according to the type of screening test. Aliment Pharmacol Ther 2012;36:929–40. [7] Liles EG, Perrin N, Rosales AG, Feldstein AC, Smith DH, Mosen DM, et al. Change to FIT increased CRC screening rates: evaluation of a US screening outreach program. Am J Manage Care 2012;18:588–95. [8] Moss S, Mathews C, Day TJ, Smith S, Seaman HE, Snowball J, et al. Increased uptake and improved outcomes of bowel cancer screening with a faecal immunochemical test: results from a pilot study within the national screening programme in England. Gut 2017;66:1631–44, http://dx.doi.org/10.1136/gutjnl-2015-310691, pii: gutjnl-2015-310691. [9] Gesink D, Filsinger B, Mihic A, Norwood TA, Sarai Racey C, Perez D, et al. Cancer screening barriers and facilitators for under and never screened populations: a mixed methods study. Cancer Epidemiol 2016;45:126–34. [10] Wools A, Dapper EA, de Leeuw JR. Colorectal cancer screening participation: a systematic review. Eur J Public Health 2016;26:158–68. [11] Insee. La population des communes au 1er janvier 2013. https://www.insee.fr/ fr/statistiques/1895161. [12] 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;66:2425–35. [13] Gordon NP, Green BB. Factors associated with use and non-use of the Fecal Immunochemical Test (FIT) kit for colorectal cancer screening in response to a 2012 outreach screening program: a survey study. BMC Public Health 2015;15:546. [14] Lo SH, Halloran S, Snowball J, Seaman H, Wardle J, von Wagner C. Colorectal cancer screening uptake over three biennial invitation rounds in the English bowel cancer screening programme. Gut 2015;64:282–91. [15] Gilbert A, Kanarek N. Colorectal cancer screening: physician recommendation is influential advice to Marylanders. Prev Med 2005;41:367–79. [16] Lafata JE, Divine G, Moon C, Williams K. Patient physician colorectal cancer screening discussions and screening use. Am J Prev Med 2006;31:202–9. [17] Cole SR, Young GP, Byrne D, Guy JR, Morcom J. Participation in screening for colorectal cancer based on a faecal occult blood test is improved by endorsement by the primary care practitioner. J Med Screen 2002;9:147–52. [18] Faivre J, Tazi MA. Role of the general practitioner in the screening of colorectal tumors. Gastroenterol Clin Biol 1995;19:361–3. [19] Honein-AbouHaidar GN, Kastner M, Vuong V, Perrier L, Daly C, Rabeneck L, et al. Systematic review and meta-study synthesis of qualitative studies evaluating facilitators and barriers to participation in colorectal cancer screening. Cancer Epidemiol Biomark Prev 2016;25:907–17. [20] Aubin-Auger I, Laouénan C, Le Bel J, Mercier A, Baruch D, Lebeau JP, et al. Efficacy of communication skills training on colorectal cancer screening by GPs: a cluster randomised controlled trial. Eur J Cancer Care (Engl) 2016;25:18–26. [21] van Rijn AF, van Rossum LG, Deutekom M, Laheij RJ, Fockens P, Bossuyt PM, et al. Low priority main reason not to participate in a colorectal cancer screening program with a faecal occult blood test. J Public Health (Oxf) 2008;30:461–5. [22] Chambers JA, Callander AS, Grangeret R, O’Carroll RE. Attitudes towards the Faecal Occult Blood Test (FOBT) versus the Faecal Immunochemical Test (FIT) for colorectal cancer screening: perceived ease of completion and disgust. BMC Cancer 2016;16:96.
Please cite this article in press as: Le Pimpec F, et al. Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening. Dig Liver Dis (2017), http://dx.doi.org/10.1016/j.dld.2017.08.018
ARTICLE IN PRESS Digestive and Liver Disease xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Digestive and Liver Disease journal homepage: www.elsevier.com/locate/dld
Oncology
Fecal immunological blood test is more appealing than the guaiac-based test for colorectal cancer screening Fanny Le Pimpec a , Grégoire Moutel b , Christine Piette c , Astrid Lièvre d,e,f , Jean-Franc¸ois Bretagne c,d,e,∗ a
Département de médecine générale, Faculté de médecine, Université de Rennes 1, France Normandie Univ, Unicaen, Inserm U1086, Cancers et préventions, et CHU Caen, Caen, France c Association pour le dépistage des cancers en Ille-et-Vilaine (ADECI 35), Rennes, France d Service des maladies de l’appareil digestif, CHU Rennes, Rennes, France e Université de Rennes 1, Rennes, France f Inserm ER440-Oncogenesis, Stress and Signaling, Université de Rennes 1, Rennes, France b
a r t i c l e
i n f o
Article history: Received 11 May 2017 Received in revised form 29 June 2017 Accepted 1 August 2017 Available online xxx Keywords: Barriers and facilitators Colorectal cancer screening Fecal occult blood test Fecal immunological testing
a b s t r a c t Background: The reasons for participation in fecal immunological testing (FIT) of subjects who were previously non-respondents to guaiac fecal occult blood testing (g-FOBT) have not been assessed. Population and methods: We aimed to determine the reasons for current compliance with FIT among non-responders to g-FOBT, termed “converts”, in a French district. A questionnaire was returned by 170 converts aged from 55 to 75 years (response rate 75.2% after exclusions). Results: The major barriers to participation in screening with g-FOBT were test-related: the test was perceived as complicated (24%) and it required three consecutive stools (28%). Among the test-related major determinants of FIT compliance was the perception that the test was less complicated than previous test (30%) and that a unique stool sample was required (29%). Among the non-test related major determinants of FIT compliance were the perception that the general practitioner was more convincing (31%) and the feeling to be more concerned because of age (21%). The reasons for compliance among converts did not differ according to age, sex, and rural or urban residence. Conclusions: Our study demonstrated that the simplicity of FIT and the endorsement of practitioners were both major motivations for FIT compliance among non-respondents in at least two previous consecutive campaigns. © 2017 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.
1. Introduction Worldwide, colorectal cancer (CRC) is the third most common cancer in men and the second in women [1]. Organized and opportunistic screening programmes have been implemented throughout many countries to decrease the incidence and mortality rate of CRC [2]. Most European countries with an organized screening programme screen by means of a non-invasive stool test. Previously implemented guaiac fecal occult blood testing (g-FOBT)based programmes are being replaced by fecal immunologic testing (FIT) [2]. This is the case in France where the g-FOBT programme, which was instituted in 2003 and was implemented nationwide in 2008, was replaced by FIT in 2015. Similar to other programs, the French g-FOBT screening programme has faced disappointingly
∗ Corresponding author at: Service des maladies de l’appareil digestif, centre hospitalo-universitaire, 35033 Rennes, France. Fax: +33 2 99 28 41 89. E-mail address: [email protected] (J.-F. Bretagne).
low participation rates. While the European guidelines for quality assurance in CRC screening recommend a minimum uptake of 45% to keep the programme cost-effective [3], the participation rate in France was estimated to be 34.3% in 2008–2009 [4], which decreased to 29.8% in 2013–2014 [5]. Screening programme organizers expect a decrease in the gap between targeted and observed screening rates due to the switch to FIT because a meta-analysis of direct comparative studies reported that FIT resulted in a higher uptake (16%) compared with g-FOBT [6]. Despite the publication of pilot study results [7,8], the consequence of replacement of g-FOBT with FIT with respect to nationwide compliance is still unknown. A systematic review of factors associated with adherence to CRC screening presented in the literature has identified many factors related to socio-demographic, psychological, environmental, and health care provider-related characteristics [9,10]. To the best of our knowledge, the reasons for participation in FIT-based screening of subjects who were non-respondents to g-
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Fig. 1. Flow chart of target and study population.
FOBT screening have not been explored. Therefore, the present study was aimed to assess the reasons for FIT compliance by nonrespondents who we have termed “converts”. These findings might be useful for the improvement of the quality of a nationwide screening programme and thereafter to further increase the observed participation rates. 2. Populations and methods 2.1. Study setting ‘Ille et Vilaine’ was one of the first French districts to implement the national screening programme based on biennial g-FOBT. The target population for screening consisted of asymptomatic men and women aged between 50 and 74 years with no other risk factor for CRC. Individuals with a personal or family history of CRC or adenoma, those with inflammatory bowel disease, and those who had undergone total colonoscopy in the previous five years were excluded from the mass screening programme. When the screening programme was launched in 2003, the total population of ‘Ille et Vilaine’ was 908,449, and the target resident population was 213,635. In 2015, the respective figures were 1,019,923 inhabitants and 223,329 target residents. The participation rate for g-FOBT testing, which was satisfactory during the first campaign in 2003–2004 (51.2%), constantly decreased to 42% in 2013–2014 [11]. High rates (>90%) of compliance with colonoscopy following positive testing were registered during each campaign. The shift from g-FOBT to FIT occurred in May 2015 in this district in France. The OC-Sensor test (Eiken, Tokyo, Japan), which consists of a single sampling tube, has been selected from various versions of FIT. Participants were instructed to scrape different parts of the surface of their stool with the test probe and to return the test by
mail to the central analysis center in a prepaid envelope as soon as possible. The maximum time between the fecal deposit and the processing of the test should be less than 6 days. The test was defined as positive at a cutoff of 150 ng hemoglobin per milliliter of sample solution, which corresponds to 30 g hemoglobin per gram of feces. The screening campaign began when each target subject was sent an information brochure and an invitation letter that invited the subjects to perform the screening test. The first 6 months of the screening campaign (May–November 2015) corresponded to the medical free-offer phase. People were invited to consult their general practitioners (GPs) who propose the screening test to eligible subjects seen at their practice. GPs were also asked to state the exclusion criteria, at which point they provided each eligible individual with one screening test. A reminder letter with the screening test along was sent 6 months later to non-respondents who were not excluded from participation. The screening strategy and the implication of GPs were similar for FIT and g-FOBT delivering. In both cases, their mission was to explain modalities and performance of the test, as well as its expected benefits. 2.2. Study sample In the present study, non-respondents to g-FOBT were defined as individuals who were invited to two or more previous campaigns and never completed the test despite two reminder letters and tests that were sent to them during each campaign. Due to the one year gap between when the use of g-FOBT was stopped and when the use of FIT began in the district, people aged 75 years (one year over 74 years) were also invited during the campaign for FIT. Therefore, the target population for the study consisted of people aged from 55 to 75 years who were born between 1940 and 1960. Among the 28,335
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recorded non-excluded non-respondents, 802 (2.8%) individuals completed FIT. The 551 of the 802 individuals who completed FIT by 1st March 2016 following the first invitation letter, but before the reminder and the test were mailed, comprised the target population for the survey. Finally, the study was restricted to a sample of 300 individuals after drawing lots (Fig. 1). 2.3. Data collection The 300 individuals were contacted by phone by one of the authors (FLP) and were asked to respond to a questionnaire either by phone, by return of the completed questionnaire in a pre-paid envelope, or by completion of the questionnaire via the Internet using the secured LimesurveyTM software, which was at our disposal by the University of Rennes1. Whatever the method used for the collection of the questionnaires, the aim of the study was explained and informed consent was obtained in all cases. The survey, in addition to follow-up phone calls, was conducted between May and August 2016. The questionnaire was generated according to the methods used in the social sciences. The questionnaire consisted of 4 sections. The aim of questions in the first section was to ascertain that individuals did not have contraindications to colorectal cancer mass screening with fecal occult blood test. The second section consisted of questions about sociodemographic characteristics. The third section was devoted to determinants for non-participation to g-FOBT screening before 2015 and for current participation to FIT. In the section four, questions aimed to search potential life changes since the period when individuals were non-respondents to screening. Regarding to the third section the questionnaire was built according to knowledge in the literature about participation – and non-participation determinants [12,13]. For every potential given reason, people have to tick one among 3 responses: 1) Yes, it was a major ground 2) Yes, it was a ground; 3) No, it was not a ground for doing or not doing the test. A major ground for doing the test was translated into top motivation. Furthermore, it was recommended that women should also respond to questions on their behavior regarding screening for gynecologic cancer. 2.4. Statistical analysis The characteristics of the converts, the reasons for noncompliance with g-FOBT and those for compliance with FIT were characterized using descriptive statistics. Given p values are associated with Wald chi-square test statistics. All analyses involved the use of SAS 9.3. 3. Results 3.1. Population Among the sample of 300 individuals, 74 people were unable to be contacted by phone despite four attempts. Nineteen people refused to complete the survey. Twenty-two people were excluded for the following reasons: they were unable to consent or to understand the aim of the survey because of cognitive disorders; they were revealed to be at high risk for CRC so that they should not have completed FIT or were revealed to have previously participated in g-FOBT screening outside the district. Lastly, 15 people did not return the questionnaire by mail despite their initial agreement to do so (Fig. 1). Among the 226 people contacted by phone, the response rate after exclusion was 75.2% (170 of 226 individuals). Among the 170 questionnaires, 115 (68%) were collected by phone interview, which lasted approximately 15 min, while the question-
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Table 1 Socio-demographic characteristics of the converts (n = 170). Study population n = 170 Sex Women Men
78 (45.9%) 92 (54.1%)
Age 55–59 years 60–64 years 65–69 years 70–75 years
47 (27.6%) 58 (34.1%) 44 (25.9%) 21 (12.4%)
Residence Rural Urban
78 (45.9%) 92 (54.1%)
naires of other attendees were collected by mail or via the Internet in 32 and 23 cases, respectively. Socio-demographic characteristics of the study population are given in Table 1. These characteristics did not differ from those of the target population of the survey (data not shown). Both groups were composed of more men than women, which was different than the sex distribution in g-FOBT attendees during the previous (2013–2014) campaign (women 54.5%). Among the 78 women who completed the survey, 57 (73%) declared their participation in breast cancer screening during the previous two years, while only 27 (42.8%) of the 63 women younger than 68 years of age declared that they did undergo cervical cancer screening. Since the period of time when they were considered nonrespondents to CRC screening, most survey attendees stated that they experienced no changes in their social, professional, familial, or financial position (Fig. 2). Nevertheless, 33% of the 170 survey attendees stated that they now have more free time because of retirement and a decrease in professional responsibilities; 31% declared that they have more health problems (Fig. 2).
3.2. Barriers to CRC screening by g-FOBT before 2015 Barriers to participation in CRC screening before 2015 are listed in Fig. 3. The major grounds were related to the method used for testing, which was perceived as complicated (24%), the need for three consecutive stool samples (28%) and the repulsive nature of the test since it requires contact with stool (16%). Negligence (19%), feelings of non-concern in the absence of symptoms (16%) and the fear of a cancer diagnosis (11%) were also recorded as major grounds for lack of participation. The lack of concern due to healthy lifestyle or age was recorded as a major ground in 9% of converts. The absence of cancer within the family was often recorded as a simple ground (40%), but it was a major ground in only 5% of converts. The lack of suggestion for CRC screening by GPs, the lack of free time, and the fear of a follow-up colonoscopy were recorded as major grounds in 6%–7% of cases. The distribution of barriers did not differ greatly according to sex, age and rural or urban residence. The differences we found statistically significant between groups were as followings: the lack of concern because of their age was more frequently recorded in men (43%) than in women (17%) (p < 0.05). Conversely, tests that require three consecutive stools were more frequently recorded as a barrier in women (61%) than in men (45%). The lack of free time was more frequently recorded in younger (55–64 years, 25%) individuals than in older (65–75 years, 11%) individuals. The perceived disgust in the manipulation of stools was more frequently recorded in urban residents (40%) than in rural (23%) residents.
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Fig. 2. Potential life changes since the period of time when the 170 converts were non-respondents to screening.
Fig. 3. Distribution of barriers to screening by g-FOBT in the 170 converts.
3.3. Reasons for compliance to FIT
3.4. The role of general practitioners
Greater concern because of aging was the most often (67%) recorded ground for compliance, but it was given as a major ground by only 21% of the survey respondents. The major grounds or top motivations most frequently cited were that the GP was more convincing than before implementation of FIT (31%), the FIT was perceived as less complicated than g-FOBT (30%) and that a unique stool sample was required (29%). The feeling of concern despite the absence of symptoms was also a frequent ground (47%), but it was stated as a top motivation by only 15% of the survey respondents. Other grounds are listed in Fig. 4. Among the 58 (34%) converts who knew that FIT was more reliable than g-FOBT, 71% of them believed that the reliability encouraged them to complete FIT. Facilitators did not differ significantly according to the sex, age and rural or urban residence of the survey participants.
The majority (68%) of survey respondents claimed to have the same GP while 29% had changed their GPs. Most respondents (54%) found that the explanations given by their GP regarding the test procedure were more lucid; 45% perceived that the GP had spent more time and 45% thought that the explanations given by their GPs regarding CRC screening in general were more lucid. Most people who found that their GP was more convincing and gave this as a top motivation for FIT compliance, belonged to one of the latter three groups.
4. Discussion The present study aimed to determine the reasons for compliance to FIT in non-respondents to g-FOBT, who we have termed
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Fig. 4. Distribution of facilitators to screening by fecal immunological testing in the 170 converts.
“converts”. The survey involved 170 converts who ranged in age from 55 to 75 years. The majority was composed of men (54.1%), which is unusual in screening-compliant populations in nationwide CRC screening programs based on g-FOBT [4,14]. The most frequent reasons quoted by converts as a top motivation for compliance emphasized both the endorsement and involvement of GPs, and the simplicity of the screening test. We reported that 50% converts perceived their GP as more convincing than before implementation of FIT, which was a determinant for participation. GPs gave more lucid explanations of the FIT procedure and CRC screening and spent more time on these explanations than in the past. Our results allow us to make the hypothesis that GPs were more motivated to present the new test because it was more reliable but also simpler to realize. GPs were sensitized on these two points during the implementation of the FIT through a new national information and training campaign. That is probably why patients perceived the FIT as better and accepted to do it more easily. Thus, the new test was directly or indirectly responsible of the participation of converts. The GP is often one of the interlocutors who is most knowledgeable about the psychology and reticence of his patients. Once convinced of the importance of screening, he is able to “lift the brakes” so to speak, to inform and explain the procedure to the patient. The physician’s attitude and discourse are important in adherence to screening. The quality of the doctor-patient relationship appears to be one of the key elements of the screening system [15,16]. It is well known that physician recommendations motivate individuals to undergo screening [16–19], but we suspect in the present study, that behavior changes of GPs might be linked to the higher performance of FIT compared with that of g-FOBT, which rendered GPs more confident in the new test and more comfortable in the discussion of the test with their patients. This indirect benefit of FIT is not easy to assess. Most of the GPs in the district had participated to training sessions before the replacement of g-FOBT with FIT, and therefore, they were aware of the reliability of the new test. Doctor-patient communication has been shown to be one of the possible targets for the improvement of patient adherence and the participation rate in the target population [20]. The present study did not aim to assess whether converts completed FIT to please their doctor, as has been previously suggested [13]. Only one third of the converts declared that they knew that FIT was a more reliable screening test than gFOBT. However, interestingly, among these patients, 71% declared that the performance of the new test was a determinant for their participation. This finding could have significance for the French
nationwide screening program and should prompt improvement in the communication of FIT performance to patient populations. As expected, test-related determinants were found to have a large role in participation in screening by converts. The perception that FIT was less complicated and that it required a unique stool sample was quoted as a determinant for participation in 55% and 54% of converts, respectively. Furthermore, 25% of converts mentioned that FIT was less repulsive than g-FOBT. We then related these findings with those for non-compliance to g-FOBT. Among the most frequently mentioned reasons for non-compliance in the present study demonstrated that the HemoccultTM test was previously perceived as complicated (50%). Another reason, mostly given by women (61%), was that this test required 3 consecutive stool samples (52%). Finally, 32% of converts mentioned that the test was repulsive because of stool contact. Even if the relationship between perceptions and participation is not as clear as one might expect [21], these findings could explain why comparative studies of both non-invasive tests demonstrated higher participation rates with FIT than g-FOBT [6]. Nevertheless, most of these studies were conducted in previously unscreened populations. FIT pilot studies conducted within a “live” screening program reported that overall uptake increased by over 7–9.5% points with FIT compared with g-FOBT [7,8] and that uptake of previous non-respondents to g-FOBT was doubled (FIT 23.9% vs g-FOBT 12.5%) [8]. However, none of these comparative studies was aimed to determine the reasons for better compliance to FIT. Our results are in agreement with findings from an intentionto-screen study that assessed the attitudes towards the g-FOBT versus FIT in a Scottish population [22]. In the latter study, participants reported a higher intention to complete and return the FIT materials versus the g-FOBT, which was largely due to a perception that FIT was easier and less repulsive to complete [22]. The present study has some limitations. First, the target population was restricted to converts who responded during the medical free-offer phase before the second letter and the FIT materials were mailed. As the campaign did not end, we did not know the precise proportion of individuals who later became compliant with FIT, or whether the determinants for compliance were similar in both groups of converts. Nevertheless with the data available at the present time of the first campaign with FIT, we could expect a participation rate of 52–55%, as compared to 42% for the previous campaign with g-FOBT. Second, the survey respondents were questioned retrospectively with a time delay that ranged from 4 months to 10 months after completion of the test, and thus we cannot exclude bias in the collection of data. Third, while most sur-
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vey participants were interviewed by phone, we cannot exclude bias among the different modalities used to complete the questionnaires. Fourth, while we suspect that most of the non-respondents to g-FOBT will remain non-respondents to FIT at the end of the first campaign, the reasons for this remain to be determined. It will be of interest to assess if the determinants for the participation of converts identified in the present study could improve most the CRC screening-resistant population, even if a range of approaches may be required to improve screening uptake. Finally, the lack of control group could be a limitation of the study. Comparing the barriers to screening in definitive non-responders with that of converts would add much to our understanding to screening. But unfortunately, we presume that the response rate to survey of definitive non-responders to screening should be very low. Furthermore, comparing the reasons for compliance of converts selected at the medical free-offer phase of the screening round and those of converts selected after the mailing of the test would add much to our understanding. In conclusion, our study demonstrated that the simplicity of FIT and the endorsement of GPs were both major determinants for compliance to FIT among converts. These latter, along with the higher performance of FIT, could positively influence the participation of people resistant to colorectal cancer screening by g-FOBT. Conflicts of interest The authors Fanny Le Pimpec, Grégoire Moutel, Christine Piette, Astrid Lièvre, Jean-Franc¸ois Bretagne have no conflicts of interest or financial ties to disclose with regard to this article. References [1] IARC. Estimated cancer incidence, mortality, and prevalence worldwide in; 2012 http://globocan.iarc.fr/Pages/fact sheets cancer.aspx. [2] Schreuders EH, Ruco A, Rabeneck L, Schoen RE, Sung JJ, Young GP, et al. Colorectal cancer screening: a global overview of existing programmes. Gut 2015;64:1637–49. [3] Minozzi S, Armaroli P, Segnan N. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition–principles of evidence assessment and methods for reaching recommendations. Endoscopy 2012;44(Suppl. 3):SE9–14. [4] Leuraud K, Jezewski-Serra D, Viguier J, Salines E. Colorectal cancer screening by guaiac faecal occult blood test in France: evaluation of the programme two years after launching. Cancer Epidemiol 2013;37:959–67. [5] INCa Participation au programme national du dépistage organisé du cancer http://lesdonnees.e-cancer.fr/Themes/Depistage/Le-depistagecolorectal. du-cancer-colorectal/Taux-de-participation-au-programme-national-dudepistage-organise-du-cancer-colorectal.
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