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Comparison of endoscopic procedures for colorectal cancer screening in women with mammography and Pap smear
Comparison of endoscopic procedures for colorectal cancer screening in women with mammography and Pap smear Fiona B. Nicholson, MBBS, FRACP, Melvyn G. Korman, MBBS, FRACP, PhD Clayton, Australia
Background: This study compared the experiences of women who underwent endoscopic screening for colorectal cancer vs. their experiences with breast and cervical cancer screening by mammography and Pap smear, respectively. Methods: Women who had either flexible sigmoidoscopy or colonoscopy as a screening procedure for colorectal cancer were asked to return a questionnaire by mail. In the questionnaire, they were asked about the procedure they had just undergone and to compare it with recent mammograms and Pap smears. Flexible sigmoidoscopy was performed without sedating the patient; colonoscopy was performed with the patient under deep sedation (midazolam, fentanyl, and propofol administered by an anesthesiologist). Results: Responses were obtained from 258 women (88%). Of these, 152 had colonoscopy and 106 had flexible sigmoidoscopy. A total of 72% of respondents found colonoscopy to be a comfortable test. Only 26% found flexible sigmoidoscopy uncomfortable, which was similar to mammography and Pap smear, at 22%. In terms of the test considered to be the most embarrassing, the highest response rate (38%) was for the Pap smear. Most women had no preference as to the gender of the endoscopist, but 46% preferred a woman doctor for a Pap smear (p < 0.001). Preparation was regarded as the worst part of the colonoscopy procedure; for flexible sigmoidoscopy, the procedure itself and the preparation were equivalent. Conclusions: Women found flexible sigmoidoscopy or colonoscopy comfortable and less embarrassing than a Pap smear or a mammography. There was no preference with respect to the gender of the physician who performed the colorectal screening procedures, unlike the Pap smear. Most respondents would have the procedure again and would recommend it to others. (Gastrointest Endosc 2004;60:400-7.)
Colorectal cancer (CRC) is a common but potentially preventable disease. Most CRCs develop over a period of 5 to 10 years from a precursor adenoma.1 If screening or surveillance programs for the prevention of CRC are to be effective, individuals must undergo procedures over many years. Appropriate screening tests for CRC include fecal occult blood tests (FOBT), flexible sigmoidoscopy (FS), and colonoscopy. Compliance is critical to the success of
Received December 16, 2003. For revision March 10, 2004. Accepted May 7, 2004. Current affiliations: GE Unit, Monash Medical Centre, Clayton Victoria, Australia. Presented at Australian Gastroenterology Week, October 2002, Adelaide, Australia. Grant support: Monash Postgraduate Scholarship, Melbourne GI Research Foundation. Reprint requests: Assoc. Professor Melvyn G Korman, Director of Gastroenterology, Monash Medical Centre, 246 Clayton Rd., Clayton Victoria 3168 Australia. Copyright Ó 2004 by the American Society for Gastrointestinal Endoscopy 0016-5107/$30.00 PII: S0016-5107(04)01708-0 400
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screening programs and essentially depends on the acceptance and the tolerance of patients for the test used. Thus, it is necessary to know which features of the test patients consider important, as well as the barriers that prevent individuals from considering either screening or surveillance. For health care providers, knowledge of these factors may influence the choice of test and/or the way the test is conducted. There are well-established, federally funded screening programs for cervical and breast cancer in Australia. The national program for cervical cancer screening was started in 1990,2 and the breast cancer screening program started in 1991.3 However, compliance with these procedures also is an ongoing problem: in 1998 to 1999, 55.9% of eligible women had a mammogram and 64.8% had a Pap smear.4 Although the incidence of CRC is less in women than in men,4 the mortality rate for this disease in women is second only to that of breast cancer,5 making prevention of CRC an important health issue for women. The aims of this study were to compare endoscopic screening and surveillance for CRC in women with existing screening methods for cervical and breast cancer and to elucidate factors related to VOLUME 60, NO. 3, 2004
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endoscopic screening or surveillance that may influence compliance. PATIENTS AND METHODS Patients Women patients were recruited from an existing CRC screening program (The Bowel Cancer Prevention Program) that was developed over a decade ago by a group of Melbourne gastroenterologists to target community groups with an interest in CRC prevention. The program is based on the return of a mailed questionnaire that allows a medical panel to assess bowel-cancer risk. A written response is sent to individuals who submit a completed questionnaire. This written response recommends colonoscopy surveillance for those at increased risk (e.g., a family history of CRC) and includes a menu of screening options, mainly FS with or without FOBT, for those at average risk (age $50 years). Women who chose to undergo FS or colonoscopy form the basis of the study group. The enrollment period for the study was October 1, 2001 through March 31, 2002. Before the screening procedure, patients were given ‘‘explanatory information,’’ which included the informed consent process. At this time, they were asked by the admitting nurse whether they were interested in completing a questionnaire (Table 1). If so, the questionnaire was given to the patient when she was ready to be discharged from the recovery area. The patient was asked to fill in the questionnaire at home and to return it in the stamped, addressed envelope provided. All patients were contacted by telephone 3 days after the procedure and were reminded about the questionnaire. Exclusion criteria were refusal and a lack of English language skills sufficient to complete the questionnaire. Procedures Endoscopic procedures were performed in outpatient endoscopy centers by experienced gastroenterologists (at least 10 years’ experience in endoscopy). Patients were deeply sedated for colonoscopy by an anesthesiologist who administered midazolam, fentanyl, and propofol intravenously; FS was performed without sedation. The results of the procedures were not part of the study. For completion of the cervical cancer screening section (Pap smear) and the breast cancer screening section (mammography), women were asked about their memory of the most recent experience with these procedures. Questionnaire The questionnaire (Table 1) developed for the study was intended to elucidate factors relating to compliance with an endoscopy-based screening program. It was based on the ‘‘Health Belief Model,’’6 which was used as a reference for question development. The aim of the questionnaire was to assess perceived barriers to undergoing the procedures, including pain and embarrassment. Before the study, the performance of the questionnaire instrument was assessed in a small group of patients. The question methodology was based on other standard formats, such as the Likert scale and multiple-choice questions. VOLUME 60, NO. 3, 2004
F Nicholson, M Korman
Statistical analysis The data obtained with the questionnaire were statistically analyzed by using a computer software program (SPSS, Chicago, Ill.), predominately with chi-square tests and the Yates correction for continuity when appropriate. Pain scores were compared by using techniques of analysis of variance (ANOVA). It is recognized that there was multiple testing of response data arising from individual respondents. The p values presented are without correction, but it is indicated wherever application of the method of Bonferroni would remove statistical significance from any results found to have nominal significance in a single test of hypothesis. The Southern Health Human Research Ethics Committee granted approval of the study. Return of the questionnaire was considered as consent to participation in the study.
RESULTS Questionnaires were given to 293 patients. The total number of replies received was 258, a response rate of 88%. The study group comprised 152 women (mean age 55 years, range 40-77 years) who had undergone colonoscopy and 106 women (mean age 54 years, range 50-75 years) who had FS. Of the 258 questionnaires received, the Pap smear section was completed for 248; 10 of the 258 women replied that they had undergone a hysterectomy and no longer had Pap smears. The mammogram section was complete on 237 questionnaires; 18 women replied that they had not had mammography (presumably because of age, because these women were <50 years old, the recommended age for initial mammography); 3 had refused mammography in the past. Number and timing of procedures All endoscopic procedures were performed just before the administration and the return of the questionnaire. The majority of the women who had FS underwent the procedure for the first time (mean number of FS per patient, 1.2). However, the majority of women who had colonoscopy had previously undergone the procedure (mean number of colonoscopies per patient, 2). For mammogram and Pap smear, the women were asked about their recollection of the most recent procedures. For mammography, 135/237 (57%) respondents had the procedure within the prior year, 28/237 (12%) within the last month, and 73/237 (31%) within 3 years. The average number of mammograms recalled per patient was 3.3. Similarly, for Pap smear, 118/248 (47%) responded that they had the test within the last year, 14/248 (6%) within the last month, 47/248 (19%) within the last 2 years, and GASTROINTESTINAL ENDOSCOPY
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Table 1. The questionnaire Breast Cancer Screening 1. Have you ever had a mammogram? If No, go to ‘Cervical cancer screeningÕ If yes, how recently? a. Within the last month b. Within the last year c. 2 years ago 2. Was the experience a. Comfortable b. Tolerable c. Uncomfortable d. Unbearable—would never have another one 3. Did you find it a. Embarrassing b. Humiliating c. Painful d. Don’t remember 4. If you found it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 5. Have you had more than one mammogram? If yes, how many? 1 2 3 >3 6. Would you recommend this procedure to other women? 7. Do you have any friends or family who have had breast cancer? 8. Will you have this procedure again when it is recommended in the future?
Yes
No
Yes Yes Yes Yes
No No No No
Yes Yes Yes Yes
No No No No
Yes
No
Yes Yes Yes
No No No
Cervical Cancer Screening 1. Have you ever had a pap smear? Yes No If yes, how recently? a. Within the last month b. Within the last year c. >2 years ago 2. Was the experience a. Comfortable Yes No b. Uncomfortable Yes No c. Tolerable Yes No d. Unbearable—would never have another one Yes No 3. Did you find it a. Embarrassing Yes No b. Humiliating Yes No c. Painful? Yes No d. Don’t remember Yes No 4. If you found it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 5. Have you had more than one? If yes, how many? 1 2 3 >3 6. Do you have a preference for the gender of the doctor doing the Yes No procedure? 7. If you would you prefer a FEMALE doctor, please give the MAIN reason why a. I am used to having a female doctor b. A female doctor would make me feel more comfortable c. A female doctor would respect my concerns about modesty/skin exposure d. A female doctor would be more understanding e. A female doctor would make me feel less embarrassed f. A female doctor would be more competent g. Other _____ 8. If you would prefer a MALE doctor, please give the MAIN reason why a. I am used to having a male doctor b. A male doctor would make me feel more comfortable
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Table 1. Continued c. A male doctor would be more understanding d. A male doctor would make me feel less embarrassed e. A male doctor would be more competent f. Other _____ 9. Would you recommend this procedure to other women? 10. Do you have any friends or family who have had cervical cancer? 11. Will you have this procedure again when it is recommended in the future?
Yes Yes Yes
No No No
Colon Cancer Flexible Sigmoidoscopy 1. Was the experience a. Comfortable Yes No b. Tolerable Yes No c. Uncomfortable Yes No d. Unbearable—would never have another one Yes No 2. Did you find it a. Embarrassing Yes No b. Humiliating Yes No c. Painful Yes No d. Don’t remember Yes No 3. If you find it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 4. What was the part of the procedure that concerned you most? (circle one only) a. Worry about the procedure b. Drinking the preparation/enema preparation c. The procedure itself d. Recovery after the procedure e. The embarrassment of having the procedure 5. Have you had more than one flexible sigmoidoscopy? Yes No If yes, how many? 1 2 3 >3 6. Do you have a preference for the gender of the doctor doing the Yes No procedure? 7. If you would you prefer a FEMALE doctor, please give the MAIN reason why a. I am used to having a female doctor b. A female doctor would make me feel more comfortable c. A female doctor would respect my concerns about modesty/skin exposure d. A female doctor would be more understanding e. A female doctor would make me feel less embarrassed f. A female doctor would be more competent g. Other _____ 8. If you would prefer a MALE doctor, please give the MAIN reason why a. I am used to having a male doctor b. A male doctor would make me feel more comfortable c. A male doctor would be more understanding d. A male doctor would make me feel less embarrassed e. A male doctor would be more competent f. Other______ 9. Do you have any friends or family who have had colon cancer? Yes No 10. Would you recommend this procedure to other women? Yes No 11. Will you have this procedure again when it is recommended in the Yes No future? Colon Cancer Colonoscopy 1. What was the reason that you had a colonoscopy? a. Rectal bleeding b. Diarrhoea or constipation c. Family history of bowel cancer/polyps d. Past history of polyps e. Age related screening for bowel cancer (continued on next page)
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Table 1. Continued 2. Was the experience a. Comfortable Yes b. Tolerable Yes c. Uncomfortable Yes d. Unbearable—would never have another one Yes 3. Did you find it a. Embarrassing Yes b. Humiliating Yes c. Painful Yes d. Don’t remember Yes 4. If you found it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 5. What was the part of the procedure that concerned you most? (circle one only) a. Drinking the preparation b. Not eating or drinking before the procedure c. Worry about the procedure d. The procedure itself e. IV needle/sedation f. Recovery after the procedure g. Concern about the result of the procedure 6. Have you had more than one colonoscopy? If yes, how many? 1 2 3 >3 7. Do you have a preference for the gender of the doctor doing the Yes procedure? 8. If you would you prefer a FEMALE doctor, please give the MAIN reason why a. I am used to having a female doctor b. A female doctor would make me feel more comfortable c. A female doctor would respect my concerns about modesty/skin exposure d. A female doctor would be more understanding e. A female doctor would make me feel less embarrassed f. A female doctor would be more competent g. Other_____ 9. If you would prefer a MALE doctor, please give the MAIN reason why a. I am used to having a male doctor b. A male doctor would make me feel more comfortable c. A male doctor would be more understanding d. A male doctor would make me feel less embarrassed e. A male doctor would be more competent f. Other _____ 10. Would you recommend this procedure to other women? Yes 11. Do you have any friends or family who have had colon cancer? Yes 12. Will you have this procedure again when it is recommended Yes in the future?
No No No No No No No No
No
No No No
69/248 (28%) within 3 years. The average number of Pap smears recalled was 3.8.
Pap smear (p < 0.001) but not with the impression of the CRC screening procedures.
Overall experience with the procedure
Embarrassment
The majority of women 117/152 (77%) found the overall experience of colonoscopy more comfortable than all of the other screening procedures (Fig. 1). Most patients found FS more tolerable (60/106, 57%) than uncomfortable (28/106, 26%; p < 0.001). Flexible sigmoidoscopy compared favorably with the other screening procedures with respect to tolerability and discomfort, with no significant differences between them. There was a significant relationship between a positive impression of the mammogram and of the
Embarrassment associated with the procedures was tested with a yes/no question. Overall embarrassment was extremely low for the endoscopic procedures. Of those who had colonoscopy or FS, 11% and 5%, respectively, reported embarrassment. Of patients who had mammography, 9% reported embarrassment; 38% reported that they found the Pap smear to be embarrassing. There was no significant difference between colonoscopy and FS. However, significantly more women reported embarrassment
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Figure 1. Tolerability of screening procedures. Colon, Colonoscopy; FS, flexible sigmoidoscopy; Mamm, mammography; Pap, Pap smear.
during a Pap smear compared with FS, colonoscopy, and mammography ( p < 0.0001).
Figure 2. Likert scale scores for pain experienced during cancer screening procedures (shown as percentage of patients).
Pain
Compared with both FS and colonoscopy, this preference for performance of a Pap smear by a woman physician was significant (p < 0.0001). The major reason given was that the Pap smear was less embarrassing if performed by a woman. Patients were not asked whether they had a preference for the gender of the physician who performed mammography. The majority of mammograms actually are made by technicians and not medical doctors; the patient has limited direct contact with the radiologist. Thus, a comparison of gender preference for the doctor involved in mammography was not included.
Individuals were asked to rate pain experienced during each procedure on a Likert scale of 0 to 10 (Fig. 2). There essentially was no pain associated with colonoscopy; this was expected because all of these procedures were performed with the patient under deep sedation. Flexible sigmoidoscopy was well tolerated; the pain score was less than 3 in a majority of cases (58/106, 55%). Mean pain scores for the procedures were the following: FS, 2.7; mammogram, 1.8; Pap smear, 0.8; colonoscopy, 0.3. The ANOVA showed a significant difference between the mean pain scores of all of the procedures (p < 0.001). Gender preference Patients were asked whether they had a preference for the gender of the endoscopist who performed the procedure. If they answered yes, a multiplechoice question asked for the reason. The most common reason given was that they were less embarrassed if the procedure was performed by a woman endoscopist. Most women did not have a preference with respect to the gender of the endoscopist. Overall, 11% preferred a woman (16% for FS, 7% for colonoscopy; p = 0.03 in a single test hypothesis; but, Bonferroni correction for multiple testing removes this significance). Patients also were asked whether they had a preference for the gender of the physician who performed their Pap smear. A significant number (114/248, 46%) preferred a woman doctor. VOLUME 60, NO. 3, 2004
Worst part of the procedure A multiple-choice question was asked about the worst part of the endoscopic procedures. For colonoscopy, the majority of women (114/152 [75%]) found the preparation to be the worst aspect (p < 0.001). However, for FS, the procedure itself (25/106 [24%]) and the preparation (21%) were not significantly different. General compliance The women participants were asked a yes/no question whether they would have the procedure again if advised to do so. The vast majority would have colonoscopy or FS again (Table 2). Similarly, they were asked whether they would recommend the procedure to other women. The willingness to recommend FS and colonoscopy also was extremely high. GASTROINTESTINAL ENDOSCOPY
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Table 2. General compliance for colorectal cancer screening or surveillance
Willingness to have procedure again Recommend procedure to others
Colonoscopy
Flexible sigmoidoscopy
99%
96%
95%
95%
DISCUSSION This novel study compared the experiences of women who have undergone either colonoscopy or FS for CRC prevention with their experience with accepted tests for breast and cervical cancer screening. The best, most acceptable method for screening for CRC is controversial. Acceptance by the patient of whatever test is chosen is critical to ongoing compliance with any screening or surveillance program for CRC prevention. Colonoscopy in this study was the most comfortable and the least painful of all the screening/ surveillance tests. This was expected because colonoscopy was performed with the patient under deep sedation with propofol, which has been shown to significantly decrease the discomfort of the procedure.7 However, participants found FS, which was performed without sedating the patient, to be only slightly more painful than a mammography and a Pap smear. This finding suggests that both FS and colonoscopy are comparable with existing screening procedures that have some level of discomfort. The worst part of the endoscopic procedures was clearly the preparation for colonoscopy, which also is the case for related imaging methodologies, including CT colonography.8 For FS, the procedure itself did not differ significantly from the preparation. This suggests that although FS is not more uncomfortable than the other screening modalities, it, nevertheless, is not pleasant, and this may influence compliance. Pain and embarrassment are powerful factors that motivate avoidance behavior. The majority of women in the present study who had all 4 screening procedures experienced minimal pain with each. It is interesting that more women gave mammography a higher overall pain score than FS. However, the distribution of the results showed that the mean pain score for FS was higher than that for mammography. Other studies have found the pain associated with FS to be significant9,10 and a possible deterrent to CRC screening. In the study by Zubarik et al.,11 a significant number of patients experienced greater pain with FS compared with colonoscopy, with pain being a factor that influences the likelihood of future compliance with CRC screening. Women rated the 406
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Pap smear as the most embarrassing procedure, followed by FS, and colonoscopy as a distant last. This finding was surprising, because FS is as invasive as a Pap smear and was generally perceived to be an embarrassing procedure. A preference for the gender of the physician is thought to influence compliance with procedures that are perceived as intimate, such as gynecologic examination, although not for physicians who perform ‘‘instrumental’’ procedures, such as surgeons or anesthesiologists.12 Interestingly, only 16% of women preferred a woman endoscopist for FS and only 7% of women preferred a woman endoscopist for colonoscopy. This is in contrast to studies from the United States in which 46% to 48% of women preferred a woman endoscopist.9,13 It is unclear why most women in this cohort drawn from the Australian population have no preference with respect to the gender of the endoscopist, whereas 45% preferred that a Pap smear be performed by a woman physician, a proportion similar to that for American women who prefer that endoscopy be performed by a woman physician. This result may indicate cultural differences between Australian and American women. However, it is essential to consider such preferences when tailoring a CRC prevention program to a broader local population. The interpretation of the results of the present study is limited because the participants were, in fact, compliant with CRC screening. Because they agreed to undergo the recommended procedure, there may be an inherent bias in their responses. Moreover, nearly 100% stated that they definitely would have the procedure again if recommended, which again indicates a high level of compliance. In addition, 95% also would provide good ‘‘word-ofmouth’’ information regarding these procedures to other people. Although this willingness to ‘‘advertise’’ CRC screening has not been widely or adequately studied, it may be a critical factor in improving the general perception of these procedures in the wider community. If the benefits of any CRC screening modality are to be maximized, it is essential to understand the barriers to participation. Most women found either FS or colonoscopy to be highly acceptable for CRC prevention. In the present study, women regarded colonoscopy as more comfortable and less embarrassing than a Pap smear or a mammography, and few expressed a preference for the gender of the endoscopist. Most stated they would have the procedure again and would recommend it to others. These findings suggest that compliance with CRC prevention is not impeded by a fear or a dislike of FS or colonoscopy. VOLUME 60, NO. 3, 2004
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F Nicholson, M Korman
ACKNOWLEDGMENT Assistance was provided by the Monash University Department of Statistics.
8.
REFERENCES 1. Muto T, Bussey H, Morson B. The evolution of cancer in the colon and rectum. Cancer 1975;36:2251-70. 2. Dickinson JA. Cervical screening: time to change the policy. Med J Aust 2002;176:547-50. 3. Barratt AL, Cockburn J, Redman S, Paul C, Perkins J. Mammographic screening: results from the 1996 National Breast Health Survey. Med J Aust 1997;167:521-4. 4. Australian Institute Health Welfare (AIHW), Australasian Association Cancer Registries (AACR). Cancer in Australia 1999. Canberra: AIHW; 2002. AIHW cat. no. CAN 10, Cancer Series no. 15. 5. Giles G. The cancer epidemic in Victoria. Vol 2.2. Melbourne: ACCV; 2002. p. 23-6. 6. Becker M. Understanding attitudes and predicting behaviour. Englewood Cliffs (NJ): Prentice-Hall; 1980. 7. Paspatis G, Manolaraki M, Xirouchakis G, Papanikolaou N, Chlouverakis G, Gritzali A. Synergistic sedation with midazolam and propofol versus midazolam and pethidine in
9.
10.
11.
12.
13.
colonoscopies: a prospective, randomized study. Am J Gastroenterol 2002;97:1963-7. Taylor SA, Halligan S, Saunders BP, Bassett P, Vance M, Bartram CI. Acceptance by patients of multidetector CT colonography compared with barium enema examinations, flexible sigmoidoscopy, and colonoscopy. AJR Am J Roentgenol 2003;181:913-21. Harewood GC, Wiersema MJ, Melton LJ. A prospective controlled assessment of factors influencing acceptance of screening colonoscopy. Am J Gastroenterol 2002;97:3186-94. Eloubeidi MA, Wallace MB, Desmond R, Farraye FA. Female gender and other factors predictive of a limited screening flexible sigmoidoscopy examination for colorectal cancer. Am J Gastroenterol 2003;98:1634-9. Zubarik R, Ganguly E, Benway D, Ferrentino N, Moses P, Vecchio J. Procedure related abdominal discomfort in patients undergoing colorectal cancer screening: a comparison of colonoscopy and flexible sigmoidoscopy. Am J Gastroenterol 2002;97:3056-61. Kerssens J, Bensing JM, Andela M. Patient preference for genders of health professionals. Soc Sci Med 1997;44: 1531-40. Fidler H, Hartnett A, Cheng Man KC, Derbyshire I, Sheil M. Sex and familiarity of colonoscopists: patient preferences. Endoscopy 2000;32:481-2.
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Background: This study compared the experiences of women who underwent endoscopic screening for colorectal cancer vs. their experiences with breast and cervical cancer screening by mammography and Pap smear, respectively. Methods: Women who had either flexible sigmoidoscopy or colonoscopy as a screening procedure for colorectal cancer were asked to return a questionnaire by mail. In the questionnaire, they were asked about the procedure they had just undergone and to compare it with recent mammograms and Pap smears. Flexible sigmoidoscopy was performed without sedating the patient; colonoscopy was performed with the patient under deep sedation (midazolam, fentanyl, and propofol administered by an anesthesiologist). Results: Responses were obtained from 258 women (88%). Of these, 152 had colonoscopy and 106 had flexible sigmoidoscopy. A total of 72% of respondents found colonoscopy to be a comfortable test. Only 26% found flexible sigmoidoscopy uncomfortable, which was similar to mammography and Pap smear, at 22%. In terms of the test considered to be the most embarrassing, the highest response rate (38%) was for the Pap smear. Most women had no preference as to the gender of the endoscopist, but 46% preferred a woman doctor for a Pap smear (p < 0.001). Preparation was regarded as the worst part of the colonoscopy procedure; for flexible sigmoidoscopy, the procedure itself and the preparation were equivalent. Conclusions: Women found flexible sigmoidoscopy or colonoscopy comfortable and less embarrassing than a Pap smear or a mammography. There was no preference with respect to the gender of the physician who performed the colorectal screening procedures, unlike the Pap smear. Most respondents would have the procedure again and would recommend it to others. (Gastrointest Endosc 2004;60:400-7.)
Colorectal cancer (CRC) is a common but potentially preventable disease. Most CRCs develop over a period of 5 to 10 years from a precursor adenoma.1 If screening or surveillance programs for the prevention of CRC are to be effective, individuals must undergo procedures over many years. Appropriate screening tests for CRC include fecal occult blood tests (FOBT), flexible sigmoidoscopy (FS), and colonoscopy. Compliance is critical to the success of
Received December 16, 2003. For revision March 10, 2004. Accepted May 7, 2004. Current affiliations: GE Unit, Monash Medical Centre, Clayton Victoria, Australia. Presented at Australian Gastroenterology Week, October 2002, Adelaide, Australia. Grant support: Monash Postgraduate Scholarship, Melbourne GI Research Foundation. Reprint requests: Assoc. Professor Melvyn G Korman, Director of Gastroenterology, Monash Medical Centre, 246 Clayton Rd., Clayton Victoria 3168 Australia. Copyright Ó 2004 by the American Society for Gastrointestinal Endoscopy 0016-5107/$30.00 PII: S0016-5107(04)01708-0 400
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screening programs and essentially depends on the acceptance and the tolerance of patients for the test used. Thus, it is necessary to know which features of the test patients consider important, as well as the barriers that prevent individuals from considering either screening or surveillance. For health care providers, knowledge of these factors may influence the choice of test and/or the way the test is conducted. There are well-established, federally funded screening programs for cervical and breast cancer in Australia. The national program for cervical cancer screening was started in 1990,2 and the breast cancer screening program started in 1991.3 However, compliance with these procedures also is an ongoing problem: in 1998 to 1999, 55.9% of eligible women had a mammogram and 64.8% had a Pap smear.4 Although the incidence of CRC is less in women than in men,4 the mortality rate for this disease in women is second only to that of breast cancer,5 making prevention of CRC an important health issue for women. The aims of this study were to compare endoscopic screening and surveillance for CRC in women with existing screening methods for cervical and breast cancer and to elucidate factors related to VOLUME 60, NO. 3, 2004
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endoscopic screening or surveillance that may influence compliance. PATIENTS AND METHODS Patients Women patients were recruited from an existing CRC screening program (The Bowel Cancer Prevention Program) that was developed over a decade ago by a group of Melbourne gastroenterologists to target community groups with an interest in CRC prevention. The program is based on the return of a mailed questionnaire that allows a medical panel to assess bowel-cancer risk. A written response is sent to individuals who submit a completed questionnaire. This written response recommends colonoscopy surveillance for those at increased risk (e.g., a family history of CRC) and includes a menu of screening options, mainly FS with or without FOBT, for those at average risk (age $50 years). Women who chose to undergo FS or colonoscopy form the basis of the study group. The enrollment period for the study was October 1, 2001 through March 31, 2002. Before the screening procedure, patients were given ‘‘explanatory information,’’ which included the informed consent process. At this time, they were asked by the admitting nurse whether they were interested in completing a questionnaire (Table 1). If so, the questionnaire was given to the patient when she was ready to be discharged from the recovery area. The patient was asked to fill in the questionnaire at home and to return it in the stamped, addressed envelope provided. All patients were contacted by telephone 3 days after the procedure and were reminded about the questionnaire. Exclusion criteria were refusal and a lack of English language skills sufficient to complete the questionnaire. Procedures Endoscopic procedures were performed in outpatient endoscopy centers by experienced gastroenterologists (at least 10 years’ experience in endoscopy). Patients were deeply sedated for colonoscopy by an anesthesiologist who administered midazolam, fentanyl, and propofol intravenously; FS was performed without sedation. The results of the procedures were not part of the study. For completion of the cervical cancer screening section (Pap smear) and the breast cancer screening section (mammography), women were asked about their memory of the most recent experience with these procedures. Questionnaire The questionnaire (Table 1) developed for the study was intended to elucidate factors relating to compliance with an endoscopy-based screening program. It was based on the ‘‘Health Belief Model,’’6 which was used as a reference for question development. The aim of the questionnaire was to assess perceived barriers to undergoing the procedures, including pain and embarrassment. Before the study, the performance of the questionnaire instrument was assessed in a small group of patients. The question methodology was based on other standard formats, such as the Likert scale and multiple-choice questions. VOLUME 60, NO. 3, 2004
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Statistical analysis The data obtained with the questionnaire were statistically analyzed by using a computer software program (SPSS, Chicago, Ill.), predominately with chi-square tests and the Yates correction for continuity when appropriate. Pain scores were compared by using techniques of analysis of variance (ANOVA). It is recognized that there was multiple testing of response data arising from individual respondents. The p values presented are without correction, but it is indicated wherever application of the method of Bonferroni would remove statistical significance from any results found to have nominal significance in a single test of hypothesis. The Southern Health Human Research Ethics Committee granted approval of the study. Return of the questionnaire was considered as consent to participation in the study.
RESULTS Questionnaires were given to 293 patients. The total number of replies received was 258, a response rate of 88%. The study group comprised 152 women (mean age 55 years, range 40-77 years) who had undergone colonoscopy and 106 women (mean age 54 years, range 50-75 years) who had FS. Of the 258 questionnaires received, the Pap smear section was completed for 248; 10 of the 258 women replied that they had undergone a hysterectomy and no longer had Pap smears. The mammogram section was complete on 237 questionnaires; 18 women replied that they had not had mammography (presumably because of age, because these women were <50 years old, the recommended age for initial mammography); 3 had refused mammography in the past. Number and timing of procedures All endoscopic procedures were performed just before the administration and the return of the questionnaire. The majority of the women who had FS underwent the procedure for the first time (mean number of FS per patient, 1.2). However, the majority of women who had colonoscopy had previously undergone the procedure (mean number of colonoscopies per patient, 2). For mammogram and Pap smear, the women were asked about their recollection of the most recent procedures. For mammography, 135/237 (57%) respondents had the procedure within the prior year, 28/237 (12%) within the last month, and 73/237 (31%) within 3 years. The average number of mammograms recalled per patient was 3.3. Similarly, for Pap smear, 118/248 (47%) responded that they had the test within the last year, 14/248 (6%) within the last month, 47/248 (19%) within the last 2 years, and GASTROINTESTINAL ENDOSCOPY
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Table 1. The questionnaire Breast Cancer Screening 1. Have you ever had a mammogram? If No, go to ‘Cervical cancer screeningÕ If yes, how recently? a. Within the last month b. Within the last year c. 2 years ago 2. Was the experience a. Comfortable b. Tolerable c. Uncomfortable d. Unbearable—would never have another one 3. Did you find it a. Embarrassing b. Humiliating c. Painful d. Don’t remember 4. If you found it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 5. Have you had more than one mammogram? If yes, how many? 1 2 3 >3 6. Would you recommend this procedure to other women? 7. Do you have any friends or family who have had breast cancer? 8. Will you have this procedure again when it is recommended in the future?
Yes
No
Yes Yes Yes Yes
No No No No
Yes Yes Yes Yes
No No No No
Yes
No
Yes Yes Yes
No No No
Cervical Cancer Screening 1. Have you ever had a pap smear? Yes No If yes, how recently? a. Within the last month b. Within the last year c. >2 years ago 2. Was the experience a. Comfortable Yes No b. Uncomfortable Yes No c. Tolerable Yes No d. Unbearable—would never have another one Yes No 3. Did you find it a. Embarrassing Yes No b. Humiliating Yes No c. Painful? Yes No d. Don’t remember Yes No 4. If you found it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 5. Have you had more than one? If yes, how many? 1 2 3 >3 6. Do you have a preference for the gender of the doctor doing the Yes No procedure? 7. If you would you prefer a FEMALE doctor, please give the MAIN reason why a. I am used to having a female doctor b. A female doctor would make me feel more comfortable c. A female doctor would respect my concerns about modesty/skin exposure d. A female doctor would be more understanding e. A female doctor would make me feel less embarrassed f. A female doctor would be more competent g. Other _____ 8. If you would prefer a MALE doctor, please give the MAIN reason why a. I am used to having a male doctor b. A male doctor would make me feel more comfortable
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Table 1. Continued c. A male doctor would be more understanding d. A male doctor would make me feel less embarrassed e. A male doctor would be more competent f. Other _____ 9. Would you recommend this procedure to other women? 10. Do you have any friends or family who have had cervical cancer? 11. Will you have this procedure again when it is recommended in the future?
Yes Yes Yes
No No No
Colon Cancer Flexible Sigmoidoscopy 1. Was the experience a. Comfortable Yes No b. Tolerable Yes No c. Uncomfortable Yes No d. Unbearable—would never have another one Yes No 2. Did you find it a. Embarrassing Yes No b. Humiliating Yes No c. Painful Yes No d. Don’t remember Yes No 3. If you find it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 4. What was the part of the procedure that concerned you most? (circle one only) a. Worry about the procedure b. Drinking the preparation/enema preparation c. The procedure itself d. Recovery after the procedure e. The embarrassment of having the procedure 5. Have you had more than one flexible sigmoidoscopy? Yes No If yes, how many? 1 2 3 >3 6. Do you have a preference for the gender of the doctor doing the Yes No procedure? 7. If you would you prefer a FEMALE doctor, please give the MAIN reason why a. I am used to having a female doctor b. A female doctor would make me feel more comfortable c. A female doctor would respect my concerns about modesty/skin exposure d. A female doctor would be more understanding e. A female doctor would make me feel less embarrassed f. A female doctor would be more competent g. Other _____ 8. If you would prefer a MALE doctor, please give the MAIN reason why a. I am used to having a male doctor b. A male doctor would make me feel more comfortable c. A male doctor would be more understanding d. A male doctor would make me feel less embarrassed e. A male doctor would be more competent f. Other______ 9. Do you have any friends or family who have had colon cancer? Yes No 10. Would you recommend this procedure to other women? Yes No 11. Will you have this procedure again when it is recommended in the Yes No future? Colon Cancer Colonoscopy 1. What was the reason that you had a colonoscopy? a. Rectal bleeding b. Diarrhoea or constipation c. Family history of bowel cancer/polyps d. Past history of polyps e. Age related screening for bowel cancer (continued on next page)
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Table 1. Continued 2. Was the experience a. Comfortable Yes b. Tolerable Yes c. Uncomfortable Yes d. Unbearable—would never have another one Yes 3. Did you find it a. Embarrassing Yes b. Humiliating Yes c. Painful Yes d. Don’t remember Yes 4. If you found it painful, please score your pain on a score of zero for no pain to 10 for worst pain ever 0 1 2 3 4 5 6 7 8 9 10 5. What was the part of the procedure that concerned you most? (circle one only) a. Drinking the preparation b. Not eating or drinking before the procedure c. Worry about the procedure d. The procedure itself e. IV needle/sedation f. Recovery after the procedure g. Concern about the result of the procedure 6. Have you had more than one colonoscopy? If yes, how many? 1 2 3 >3 7. Do you have a preference for the gender of the doctor doing the Yes procedure? 8. If you would you prefer a FEMALE doctor, please give the MAIN reason why a. I am used to having a female doctor b. A female doctor would make me feel more comfortable c. A female doctor would respect my concerns about modesty/skin exposure d. A female doctor would be more understanding e. A female doctor would make me feel less embarrassed f. A female doctor would be more competent g. Other_____ 9. If you would prefer a MALE doctor, please give the MAIN reason why a. I am used to having a male doctor b. A male doctor would make me feel more comfortable c. A male doctor would be more understanding d. A male doctor would make me feel less embarrassed e. A male doctor would be more competent f. Other _____ 10. Would you recommend this procedure to other women? Yes 11. Do you have any friends or family who have had colon cancer? Yes 12. Will you have this procedure again when it is recommended Yes in the future?
No No No No No No No No
No
No No No
69/248 (28%) within 3 years. The average number of Pap smears recalled was 3.8.
Pap smear (p < 0.001) but not with the impression of the CRC screening procedures.
Overall experience with the procedure
Embarrassment
The majority of women 117/152 (77%) found the overall experience of colonoscopy more comfortable than all of the other screening procedures (Fig. 1). Most patients found FS more tolerable (60/106, 57%) than uncomfortable (28/106, 26%; p < 0.001). Flexible sigmoidoscopy compared favorably with the other screening procedures with respect to tolerability and discomfort, with no significant differences between them. There was a significant relationship between a positive impression of the mammogram and of the
Embarrassment associated with the procedures was tested with a yes/no question. Overall embarrassment was extremely low for the endoscopic procedures. Of those who had colonoscopy or FS, 11% and 5%, respectively, reported embarrassment. Of patients who had mammography, 9% reported embarrassment; 38% reported that they found the Pap smear to be embarrassing. There was no significant difference between colonoscopy and FS. However, significantly more women reported embarrassment
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Figure 1. Tolerability of screening procedures. Colon, Colonoscopy; FS, flexible sigmoidoscopy; Mamm, mammography; Pap, Pap smear.
during a Pap smear compared with FS, colonoscopy, and mammography ( p < 0.0001).
Figure 2. Likert scale scores for pain experienced during cancer screening procedures (shown as percentage of patients).
Pain
Compared with both FS and colonoscopy, this preference for performance of a Pap smear by a woman physician was significant (p < 0.0001). The major reason given was that the Pap smear was less embarrassing if performed by a woman. Patients were not asked whether they had a preference for the gender of the physician who performed mammography. The majority of mammograms actually are made by technicians and not medical doctors; the patient has limited direct contact with the radiologist. Thus, a comparison of gender preference for the doctor involved in mammography was not included.
Individuals were asked to rate pain experienced during each procedure on a Likert scale of 0 to 10 (Fig. 2). There essentially was no pain associated with colonoscopy; this was expected because all of these procedures were performed with the patient under deep sedation. Flexible sigmoidoscopy was well tolerated; the pain score was less than 3 in a majority of cases (58/106, 55%). Mean pain scores for the procedures were the following: FS, 2.7; mammogram, 1.8; Pap smear, 0.8; colonoscopy, 0.3. The ANOVA showed a significant difference between the mean pain scores of all of the procedures (p < 0.001). Gender preference Patients were asked whether they had a preference for the gender of the endoscopist who performed the procedure. If they answered yes, a multiplechoice question asked for the reason. The most common reason given was that they were less embarrassed if the procedure was performed by a woman endoscopist. Most women did not have a preference with respect to the gender of the endoscopist. Overall, 11% preferred a woman (16% for FS, 7% for colonoscopy; p = 0.03 in a single test hypothesis; but, Bonferroni correction for multiple testing removes this significance). Patients also were asked whether they had a preference for the gender of the physician who performed their Pap smear. A significant number (114/248, 46%) preferred a woman doctor. VOLUME 60, NO. 3, 2004
Worst part of the procedure A multiple-choice question was asked about the worst part of the endoscopic procedures. For colonoscopy, the majority of women (114/152 [75%]) found the preparation to be the worst aspect (p < 0.001). However, for FS, the procedure itself (25/106 [24%]) and the preparation (21%) were not significantly different. General compliance The women participants were asked a yes/no question whether they would have the procedure again if advised to do so. The vast majority would have colonoscopy or FS again (Table 2). Similarly, they were asked whether they would recommend the procedure to other women. The willingness to recommend FS and colonoscopy also was extremely high. GASTROINTESTINAL ENDOSCOPY
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Table 2. General compliance for colorectal cancer screening or surveillance
Willingness to have procedure again Recommend procedure to others
Colonoscopy
Flexible sigmoidoscopy
99%
96%
95%
95%
DISCUSSION This novel study compared the experiences of women who have undergone either colonoscopy or FS for CRC prevention with their experience with accepted tests for breast and cervical cancer screening. The best, most acceptable method for screening for CRC is controversial. Acceptance by the patient of whatever test is chosen is critical to ongoing compliance with any screening or surveillance program for CRC prevention. Colonoscopy in this study was the most comfortable and the least painful of all the screening/ surveillance tests. This was expected because colonoscopy was performed with the patient under deep sedation with propofol, which has been shown to significantly decrease the discomfort of the procedure.7 However, participants found FS, which was performed without sedating the patient, to be only slightly more painful than a mammography and a Pap smear. This finding suggests that both FS and colonoscopy are comparable with existing screening procedures that have some level of discomfort. The worst part of the endoscopic procedures was clearly the preparation for colonoscopy, which also is the case for related imaging methodologies, including CT colonography.8 For FS, the procedure itself did not differ significantly from the preparation. This suggests that although FS is not more uncomfortable than the other screening modalities, it, nevertheless, is not pleasant, and this may influence compliance. Pain and embarrassment are powerful factors that motivate avoidance behavior. The majority of women in the present study who had all 4 screening procedures experienced minimal pain with each. It is interesting that more women gave mammography a higher overall pain score than FS. However, the distribution of the results showed that the mean pain score for FS was higher than that for mammography. Other studies have found the pain associated with FS to be significant9,10 and a possible deterrent to CRC screening. In the study by Zubarik et al.,11 a significant number of patients experienced greater pain with FS compared with colonoscopy, with pain being a factor that influences the likelihood of future compliance with CRC screening. Women rated the 406
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Pap smear as the most embarrassing procedure, followed by FS, and colonoscopy as a distant last. This finding was surprising, because FS is as invasive as a Pap smear and was generally perceived to be an embarrassing procedure. A preference for the gender of the physician is thought to influence compliance with procedures that are perceived as intimate, such as gynecologic examination, although not for physicians who perform ‘‘instrumental’’ procedures, such as surgeons or anesthesiologists.12 Interestingly, only 16% of women preferred a woman endoscopist for FS and only 7% of women preferred a woman endoscopist for colonoscopy. This is in contrast to studies from the United States in which 46% to 48% of women preferred a woman endoscopist.9,13 It is unclear why most women in this cohort drawn from the Australian population have no preference with respect to the gender of the endoscopist, whereas 45% preferred that a Pap smear be performed by a woman physician, a proportion similar to that for American women who prefer that endoscopy be performed by a woman physician. This result may indicate cultural differences between Australian and American women. However, it is essential to consider such preferences when tailoring a CRC prevention program to a broader local population. The interpretation of the results of the present study is limited because the participants were, in fact, compliant with CRC screening. Because they agreed to undergo the recommended procedure, there may be an inherent bias in their responses. Moreover, nearly 100% stated that they definitely would have the procedure again if recommended, which again indicates a high level of compliance. In addition, 95% also would provide good ‘‘word-ofmouth’’ information regarding these procedures to other people. Although this willingness to ‘‘advertise’’ CRC screening has not been widely or adequately studied, it may be a critical factor in improving the general perception of these procedures in the wider community. If the benefits of any CRC screening modality are to be maximized, it is essential to understand the barriers to participation. Most women found either FS or colonoscopy to be highly acceptable for CRC prevention. In the present study, women regarded colonoscopy as more comfortable and less embarrassing than a Pap smear or a mammography, and few expressed a preference for the gender of the endoscopist. Most stated they would have the procedure again and would recommend it to others. These findings suggest that compliance with CRC prevention is not impeded by a fear or a dislike of FS or colonoscopy. VOLUME 60, NO. 3, 2004
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ACKNOWLEDGMENT Assistance was provided by the Monash University Department of Statistics.
8.
REFERENCES 1. Muto T, Bussey H, Morson B. The evolution of cancer in the colon and rectum. Cancer 1975;36:2251-70. 2. Dickinson JA. Cervical screening: time to change the policy. Med J Aust 2002;176:547-50. 3. Barratt AL, Cockburn J, Redman S, Paul C, Perkins J. Mammographic screening: results from the 1996 National Breast Health Survey. Med J Aust 1997;167:521-4. 4. Australian Institute Health Welfare (AIHW), Australasian Association Cancer Registries (AACR). Cancer in Australia 1999. Canberra: AIHW; 2002. AIHW cat. no. CAN 10, Cancer Series no. 15. 5. Giles G. The cancer epidemic in Victoria. Vol 2.2. Melbourne: ACCV; 2002. p. 23-6. 6. Becker M. Understanding attitudes and predicting behaviour. Englewood Cliffs (NJ): Prentice-Hall; 1980. 7. Paspatis G, Manolaraki M, Xirouchakis G, Papanikolaou N, Chlouverakis G, Gritzali A. Synergistic sedation with midazolam and propofol versus midazolam and pethidine in
9.
10.
11.
12.
13.
colonoscopies: a prospective, randomized study. Am J Gastroenterol 2002;97:1963-7. Taylor SA, Halligan S, Saunders BP, Bassett P, Vance M, Bartram CI. Acceptance by patients of multidetector CT colonography compared with barium enema examinations, flexible sigmoidoscopy, and colonoscopy. AJR Am J Roentgenol 2003;181:913-21. Harewood GC, Wiersema MJ, Melton LJ. A prospective controlled assessment of factors influencing acceptance of screening colonoscopy. Am J Gastroenterol 2002;97:3186-94. Eloubeidi MA, Wallace MB, Desmond R, Farraye FA. Female gender and other factors predictive of a limited screening flexible sigmoidoscopy examination for colorectal cancer. Am J Gastroenterol 2003;98:1634-9. Zubarik R, Ganguly E, Benway D, Ferrentino N, Moses P, Vecchio J. Procedure related abdominal discomfort in patients undergoing colorectal cancer screening: a comparison of colonoscopy and flexible sigmoidoscopy. Am J Gastroenterol 2002;97:3056-61. Kerssens J, Bensing JM, Andela M. Patient preference for genders of health professionals. Soc Sci Med 1997;44: 1531-40. Fidler H, Hartnett A, Cheng Man KC, Derbyshire I, Sheil M. Sex and familiarity of colonoscopists: patient preferences. Endoscopy 2000;32:481-2.
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