Survey on colorectal cancer screening knowledge, attitudes, and practices of general practice physicians in Lazio, Italy

Preventive Medicine 41 (2005) 30 – 35 www.elsevier.com/locate/ypmed

Survey on colorectal cancer screening knowledge, attitudes, and practices of general practice physicians in Lazio, Italy Antonio Federicia, Paolo Giorgi Rossia,*, Francesco Bartolozzib, Sara Farchia, Piero Borgiaa, Gabriella Guastcchia a

Agency for Public Health, Lazio Region, via di S. Costanza 53, 00198 Rome, Italy b Campus Biomedico, University Hospital, Rome, Italy Available online 30 December 2004

Abstract Background. Several international guidelines have recommended the involvement of general practitioners (GPs) in screening programs, but current evidence suggests this is very difficult. We implemented a survey to understand the attitudes, knowledge, and practices regarding colorectal cancer screening of GPs in the Lazio region. Methods. Survey of all GPs working in 13 of the 50 districts in Lazio using a mail-in questionnaire. Results. Out of 1192 GPs, 699 responded (59%). Ninety-four percent consider CRC a preventable disease. Knowledge about oncological screenings is higher in GPs using the guidelines as source of information. Twenty-five percent properly recommend the available screening tests for colorectal cancer, 22% do not recommend any, 6% under-recommend, and 47% over-recommend. Adequate knowledge of oncological screenings is positively associated with correct recommendation. Thirty-two percent of GPs recommend inappropriate follow-up tests for patients with positive fecal occult blood test. Conclusions. The low response rate reveals the lack of GP’s interest in screening. Knowledge about screening and use of guidelines as sources of scientific information are important factors to improve attitudes about screening, but there is a large percentage of well-informed GPs who do not recommend colorectal cancer screening at all. Currently, many GPs do not properly follow the patients up after a positive FOBT. D 2004 Elsevier Inc. All rights reserved. Keywords: General practitioner; Colorectal neoplasm; Cancer screening; Fecal occult blood test

Background Colorectal cancer (CCR) is one of the leading causes of death. However, CCR is a preventable disease; there are various types of screening procedures that can diagnose it early. Early diagnosis in these cases can effectively reduce both mortality and incidence of malignant neoplasm [1–4]. The target populations of effective CRC screening are men and women between 50 and 74 years of age. Another target population is the relatives of cases, even in the 75% cases where there is no evidence of the hereditariness of the illness [5]. The screening test most commonly recommen-

* Corresponding author. Fax +39 0683060463. E-mail address: [email protected] (P. Giorgi Rossi). 0091-7435/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ypmed.2004.11.010

ded by scientific organizations and government agencies is the fecal occult blood test (FOBT) every 1 or 2 years, followed by a colonoscopy (CS), or double contrast barium enema (DCBE), for positives. Other evidence-based recommendations proposed by some organization are flexosigmoidoscopy (FS) every 5 years, or CS (or DBCE) ranging from once every 10 years to once a lifetime [5–8]. The involvement of general practitioners (GP) or family practitioners has been recommended by several guidelines for screening program implementation [9,10]. Even though GPs are considered very important in any preventive practice because of their natural proximity to healthy beneficiaries, several studies have showed that GPs are not always well informed about CRCS practice. A high percentage (varying from 60% [11,12] to 70% [13]) do not trust FOBT as a very effective screening test, and some do

A. Federici et al. / Preventive Medicine 41 (2005) 30–35

not recommend any CRCS test to their beneficiaries in the baverage riskQ group (general 50–75 year old population) [13]. Several professional, personal, and socio-environmental characteristics influence the GPs’ attitudes to screening; they have also been shown to influence their beneficiaries’ compliance to screening programs [14]. The Italian government in 2003 established a law that guaranteed the right to be screened for CRC with FOBT for people aged 50–74. The regional Health Authorities have the mandate to implement screening programs. In our region, to date, there are no organized CRCS programs and nothing is known about opportunistic practice of testing for people at average risk. Although the mission of the GP includes prevention, the breast cancer and cervical cancer screening programs already implemented do not actually involve the GPs in an active role. The Agency for Public Health of the Lazio region conducted a survey about GP’s attitudes to CRC screening, their knowledge about screening, and screening procedures. The aim of this survey was to measure GPs’ knowledge of the efficacy of several screening tests, the extent they follow existing guidelines for CRC screening, and to describe the recommendations they give their beneficiaries for CRC screening. Other factors analyzed were GPs’ opinions regarding non-compliance by the beneficiaries and reasons they may not recommend CRC screening.

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university hospitals, 2 large research hospitals, 6 local hospitals) and different geographic areas (7 in the metropolitan area of Rome, 2 in the outskirts of Rome, 4 in towns and rural areas). We included all 1192 GPs with an active practice in any of the 13 districts in the survey (out of 50 existing in Lazio). In June 2002, we mailed the questionnaire with a pre-paid return envelope. After 1 month, we called the non-respondents to complete the questionnaire via a telephone interview. This process lasted from July to October 2002; and a second round of phone interviews was performed in the spring of 2003. Our sample is not representative of the entire GP population of our region, it is only representative of the population in the 13 districts we included. We do not produce prevalence estimates for the region, in fact no confidence interval accompanies the percentages reported. However, we think that the associations between GP screening knowledge and practice and the determinants observed are not biased by the sampling strategy. Our study had a statistical power of 90% to observe a significant (alpha 0.05) relative risk of 1.3 for a binary outcome (i.e., to properly recommend CRC screening or not), and a binary exposure, given the mean prevalence of properly recommending GPs of 50%, a minimum of 25% of exposed GPs, and a response rate of 60%. Analysis

Materials and methods The questionnaire The questionnaire was adapted from a questionnaire proposed and validated by the National Cancer Institute [13]. We modified or dropped the items concerning insurance and reimbursement problems (the authors can provide a copy on request). It was designed to be selfadministered and takes 15 min to complete. The questionnaire was tested by 10 GPs employed at the Agency for Public Health. It included demographic characteristics, knowledge about oncological screenings, agreement with international guidelines on CRCS, and prescription or recommendation of CRCS tests to the practice population (FOBT, sigmoidoscopy, and colonoscopy). We also gathered some general information about the work load of the GP. Sample size and survey conduction The Lazio region has 5.3 million inhabitants and includes the city of Rome. A complex pilot trial about CRC screening involved 13 gastroenterology wards and general practitioners from the health districts represented. The survey we present here was part of the trial phase. We selected these 13 hospitals in order to represent different gastroenterology units (5

We classified the GPs as properly recommending (that is, FOBT every 1 or 2 years, or FS every 5 years, or CS every 10 years or more, in people over 50); over-recommending (recommending screening to people younger than 50 or more frequently than every 5 or 10 years for FS and CS, respectively); under-recommending (beginning after 50 and with periods longer than 2 and 5 years for FOBT and FS, respectively); and non-recommending. We classified the GPs by each screening strategy recommended, i.e., FOBT, FS, and CS, and for the three strategies together. We computed a screening knowledge score on the basis of 13 questionnaire items (regarding the efficacy of the following screening tests in people over 50: digital rectal exam for CRC, digital rectal exam for prostate, FOBT at home, FOBT digital sampling, FS, DCBE, CS, clinical breast exam, breast self-exam, mammography, pelvic exam, Pap test, prostate specific agent; the answers were evaluated according to the Italian guideline recommendations [6]), the range was from 0, the worst, to 18, the best. The associations between screening knowledge and GPs’ characteristics were tested using an ANOVA regression model; we adopted a forward strategy to build the model, the criteria for the inclusion were a P value for the coefficient z0.1 and an improvement in the adjusted r 2 Stata 7 [15]. The associations between correct recommendations and GPs’ characteristics were tested by performing a logistic regression, with a backward strategy, the criteria for exclusion were a P value for the OR in the model z0.1 and a non-significant difference

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A. Federici et al. / Preventive Medicine 41 (2005) 30–35

between the models with or without (log likelihood ratio test P N 0.05), Stata 7 [15].

Table 2 Percent distribution of GPs’ answers to questions about efficacy of oncological screening tests and agreement with international guidelines on colorectal cancer screening

Results Compliance to the study The response rate to the questionnaire was 58.6% (699/ 1192): 22.1% responded by mail, 23.2% to the first telephone contact, and 13.3% to the second. Table 1 shows the GPs’ characteristics according to their response speed: GPs who visited less than 26 patients per day responded more promptly. We compared the respondents with nonrespondents: although no statistically significant difference was found, GPs working in Rome responded 9% more frequently (the P is border-line = 0.057). Screening knowledge Ninety-four percent of the GPs interviewed think that CRC is a preventable disease. Table 2 shows which tests the GPs consider to be effective for oncological screening; the proposed list contains both tests with evidence-based efficacy and tests for which there is no proof of efficacy. The degree of compliance with international guidelines of CRC screening is also reported. The mean value of the knowledge score was 12.2 with a standard deviation of 2.16, the range was from 4 to 17 (acceptable values 0 to 18). The sources of information about screening used by the GPs were evidence published in the scientific literature (83%), national guidelines and government recommendations (87.3%), continuous medical education courses (75.7%), university courses (57.7%), communications with other practitioners (39.3%), the mass media (13.9%), and the local medical community habits (9.4%) (more than one answer was admitted). Multivariate regression analysis (Table 3) highlighted a positive association between the

Table 1 Characteristics of respondents by mode of response Total Mode of response respondents Mail Phone

263 277 159 22.1 23.2 13.3

Relatively Not effective effective

25.6

48.8

22.2

3.4

41.8

48.2

7.0

3.0

26.5

49.4

14.6

9.5

46.5

47.6

3.0

2.9

79.3 49.9

16.7 43.6

1.3 2.7

2.7 3.8

96.1 42.6

1.6 48.6

0.3 4.7

2.0 4.1

34.6

51.8

8.9

4.7

86.6 31.6 82.4 66.1

10.0 41.8 14.0 29.9

0.6 8.3 1.0 2.2

2.8 18.3 2.6 1.8

Agreement Neutral Agreement with CRC screening guidelines

77.6

12.9

Don’t know/ No answer

Disagreement Don’t know/ No answer 5.9

3.6

use of national guidelines and government recommendations as sources of information and knowledge score, while the use of local medical community habits and university courses as sources of information had a negative association with knowledge score. No association was found between knowledge about screening and gender, age, number of patients visited per day, year of graduation, agreement with international guidelines, and the use of other sources of information.

Non-respondents

Screening practice

First Second round round No. 699 Total 58.6 percentage Percentage 66.8 resident in Rome Percent female 24.3 Mean age 49.6 Properly 38.8 recommending screening N26 patient  day 28.6

Digital rectal exam for CRC Digital rectal exam for prostate cancer FOBT—home test FOBT—digital sample test Flexosigmoidoscopy Double barium contrast enema Colonoscopy Physical breast examination Physical breast self-examination Mammography Pelvic exam Pap test Prostatic specific agent (PSA)

Very effective

493 41.4

55.1

78

66.7

61.5

22.4 49.1 48.3

26.7 50 35.7

23.3 49.9 28.3

24.9 49.6

21.7

28.5

40.2

Table 4 shows the distribution of GPs according to the FOBT, FS, and CS recommendations as primary tests for CRC screening. They were classified, both for each single strategy and the combination, as properly recommending, over-recommending, under-recommending, and non-recommending. Table 5 shows the results of the multivariate logistic regression. We compared the properly recommending versus the non-properly recommending GPs (over-, under-, and non-recommending together): a high screening knowledge score increased the probability that screening was properly recommended, as was the use of scientific

A. Federici et al. / Preventive Medicine 41 (2005) 30–35 Table 3 Linear regression: determinants of GPs’ oncological screening knowledge Coefficient Source of information University courses Guidelines and recommendations Local medical community habits Intercept

95% confidence interval

0.46 1.97

0.90 1.26

0.03 2.69

0.89

1.44

0.34

18.70

17.96

19.45

Notes. Number of observations = 426; F(3,422) = 14.7, P b 0.00005; adjusted R 2 = 0.088.

literature as source of information. A positive but not statistically significant effect can be seen for agreement with the international guidelines. No association was found between the probability of providing correct recommendations and gender, age, number of patients visited per day, year of graduation, and the use of other sources of information. Reasons for resistance to FOBT and FS We asked GPs how important some plausible reasons their beneficiaries may not comply to FOBT screening: on a scale from 1, not important at all, to 5, the most important, the bconcern about the resultQ was the most important with a mean score of 2.81; the second was bdiscomfortQ with a mean score of 2.68; followed by the black of risk perceptionQ, mean score 2.26; the bcost of testQ, mean score 2.13; the brisk of testQ, mean 1.74; and finally bthe procedure is advised against by other physiciansQ, mean score 1.46. The same questions were posed for FS, obtaining similar results, but the brisk of the testQ and the bdiscomfortQ obtained a higher mean score, 2.37 and 3.59, respectively. We also asked GPs why other practitioners do not recommend FOBT: lack of confidence in the test, i.e., btoo many false positivesQ and btoo many false negativesQ were among the most cited reasons, mean score 2.51 and 2.37, respectively, together with blow compliance of the practice populationQ, mean score 2.47; followed by bdisadvantages for the beneficiariesQ, the bcost of the testQ, and the bbelief that the CRC is not a preventable diseaseQ, mean score 1.89, 1.64, and 1.33, respectively. The same questions were asked for FS for CRC screening: the concern about

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the bcost of the testQ increased, mean score 1.76, as well as the blow compliance of the practice populationQ, mean score 2.78; but the concern about test validity decreased, mean score 1.26. Disease management and follow-up Slightly more than 52% (235) of the GPs who recommended FOBT personally follow positive patients up. On the other hand, 79.1% (296) of the GPs who recommend FS refer the patient to a gastroenterologist for follow-up. Many GPs (n = 109) follow-up these two tests in different ways. Only 4.1% of the GPs perform the FS by themselves. After a positive FOBT, 68.3% (362) of GPs recommend CS or DBCE as a second level test, as recommended by the majority of guidelines; whereas 17.4% (109) recommend repeating the FOBT, 12.1% (76) recommend FS, and 9 GPs recommend pelvic gastroscopy, 2 GPs digital rectal exam, 2 others blood exams, and 1 cancer biomarkers. The second level tests recommended in case of abnormal FS were CS or DBCE for 80.3% of GPs (354), FOBT for 11.6% (51), and another FS for 6.3% (28); four GPs recommend hepatic echography, two abdomen computer tomography, and two cancer biomarkers.

Discussion The response rate is close to 60% and is similar to that obtained in other surveys involving GPs or FPs [12,13]. The efforts we made to get this result confirm how difficult it is to obtain participation by most of the GP population [16]. Even though we are satisfied with this result and we did not find any significant difference between compliant and noncompliant practitioners in the demographic characteristics, there are still two main concerns: the scarce interest in this questionnaire, though proposed by a government agency with authority on screening program planning, may reflect a scarce interest in the CRC screening program. We observed a decreasing percentage of GPs who properly recommended CRC screening the longer it took for them to respond: 33.1% in the group who responded by mail, 21.3% who responded at the first phone request, and 17.6% who responded at the second. What could the proportion of

Table 4 Distribution of GPs according to colorectal cancer screening recommendations Primary screening test

Not recommended

Over-recommended

Under-recommended

N FOBT Flexosigmoidoscopy Colonoscopy Double barium contrast enema Any test

248 312 362 450 152

21.7

According to guidelines

%

N

%

N

%

N

%

35.5 44.6 51.8 64.4

127 166 193 157

18.2 23.7 27.6 22.5

93 129 43 39

13.3 18.5 6.2 5.6

231 92 101 53

33.0 13.2 14.4 7.6

330

47.2

43

6.2

174

24.9

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A. Federici et al. / Preventive Medicine 41 (2005) 30–35

Table 5 Logistic regression: determinants of GPs’ correct recommendation

Knowledge score Use of scientific literature Use of CRC screening guidelines

Odds ratio

95% confidence interval

1.11 5.25

1.02 1.24

1.22 22.24

2.10

0.80

5.52

Notes. Number of observations = 631; LR chi2, 3 df = 18.6, P = 0.0003; Pseudo R 2 = 0.026.

properly recommending GPs be among the 493 nonrespondents? We do not have these data, but continuing this trend the non-respondents would have a very low proportion of correct recommendations. Screening knowledge and practice Even though 95% of the GPs understand that CRC is a preventable disease, more than 20% of them do not recommend any screening test to their beneficiaries. These results fall in the middle of other recent studies: 42% in Canada [17], 5–15% in the US [13,18]. Most of the practitioners consider that the most effective screening test for CRC is CS, followed by FS. The percentage of GPs that consider FOBT very effective is quite low (26–46%), and most of them consider the test more effective when it is performed in the GP’s office based on a single digital sampling than when it is performed at home on three different evacuations. Although the most recommended test is FOBT, there is greater confidence in endoscopic tests like CS and FS as primary screening, meaning that recommendation habits do not reflect the conviction of the test’s efficacy. Even though in Italy there is a higher percentage of GPs who do not recommend any tests, similar results have been observed by Klabunde and colleagues for the GPs in the US [13]. The question about agreement with international guidelines was asked in a single item, reporting the three strategies recommended by the vast majority of scientific organizations or government agencies: FOBT yearly, FS every 5 years, or CS every 10 years for people older than 50. It was impossible to answer separately for each of the three strategies, which is probably why we obtained a low degree of agreement. The multivariate analysis shows, not surprisingly, a strong association between the knowledge score and the use of international guidelines as source of information about screening. In a field as crucial as public health, guidelines are regularly updated and very carefully evaluated by government agencies and represent the best synthesis of available knowledge about the effect of diagnostic technologies on a healthy population. The negative association found regarding local medical community habits is easily interpretable, because in our region

organized screening programs are still not widespread and the tradition is that the GPs are not involved in screening at all. On the contrary, the negative association found with university courses as a source of information is not easily understood. One explanation may be that most of the GPs currently practicing attended university when screening programs were not yet included as course topics. Only one-third of the GPs properly recommend CRC screening and most of the GPs who over- or underrecommend the tests do not have a clear strategy adopted, other studies found similar results [11,13,18,19]. The multivariate analysis shows an association between correct recommendation and the knowledge score, yet 10% of the GPs with a very high score (9/95 for score z15) did not recommend CRC screening at all, and more than 50% (51/ 95) recommended it not properly. The use of scientific literature as source of information and agreement with international guidelines was also found to be associated with correct recommendations. The second association, despite the strength of the effect, is not statistically significant because of the colinearity of the two variables. Reasons for resistance to FOBT and FS The first and third reasons healthy beneficiaries resist FOBT for CRC screening, in the GPs’ opinion, are the fear of a positive result and lack of risk perception. These beliefs should be the focus of information given by the GP when recommending a test for prevention [20]. The second reason, the discomfort, is probably linked to test requirements, like in the Guaiaco test that needs samples from three different evacuations [21]. It is hard to explain the concern about the cost of the test, given that FOBT screening is completely free for beneficiaries aged 50–74. The picture is very similar for FS, but in this case the GPs think that the beneficiaries are more concerned about the discomfort and risk of the test. The lack of validity of the test is the principal reason that, in the GPs’ opinion, prevents their colleagues from recommending FOBT for CRC screening. This finding is consistent with the observation that a higher screening knowledge score is associated with a higher probability to properly recommend screening [12,13]. Another important reason is the belief that beneficiaries are not compliant. This is even more relevant if we talk about FS, even though GPs consider this test more valid. The assumption of noncompliance reflects the limited awareness of GP’s role in health education and prevention [22]. Disease management and follow-up The different strategies for primary CRC screening, FOBT, and endoscopy represent two different approaches to disease, better health, management, and providing for the patient: 52% of the GPs follow-up after a positive FOBT,

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but only 21% of them follow-up after FS. This is probably the consequence of the setting in which the test is performed: the FOBT is usually performed at home or in the GP’s office; FS is performed in a gastroenterology unit by a specialist who will follow-up the patient without any more contact with the GP [23]. The picture emerging from the questionnaire about follow-up particularly concerns the 32% of GPs who recommend something besides CS or DBCE after a positive FOBT, and the 20% after an abnormal FS.

Conclusions The involvement of GPs in CRCS is fundamental but critical [9,10]; in fact, of all health professionals, they are in a position to have the closest relationship with the healthy population. Knowledge, agreement with guidelines, and good sources of scientific information are important factors to improve screening practice, as confirmed by our and other studies [11,18], but we found a large percentage of well-informed GPs who do not recommend this effective screening at all. This highlights the need for not only informing and improving knowledge among GPs, but also for increasing the awareness of their role in prevention and public health intervention. Unfortunately, in our region, many GPs currently do not provide a proper diagnostic follow-up after a positive FOBT, and this finding must be taken into account in the planning of screening programs involving GPs. Therefore, we recommend a strong central coordination and control by the health service authority for the management of screening and particularly of positive patients.

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