386
Research paper
Prevalence of colorectal adenoma in an average-risk population aged 40–50 versus 50–60 years Gholamreza Hemmasi, Masoudreza Sohrabi, Farhad Zamani, Hossein Ajdarkosh, Naser Rakhshani, Mahmoodreza Khoonsari, Mitra Ameli and Khadijeh Hatami According to current guidelines, screening colonoscopy begins at 50 years for the average-risk population, although there are not enough data on the incidence of precancerous lesions of individuals in the preceding decades. To evaluate the prevalence of colorectal polyps including potentially premalignant lesions in asymptomatic, average-risk individuals aged 40–49 versus 50–59 years, we offered total colonoscopy screening to individuals without any lower gastrointestinal symptoms. The primary end point was the prevalence of colorectal adenoma in two age groups. Of a total of 737 studies, 333 participants were 40–49 years old and 407 participants were 50–59 years old. The overall prevalence of adenomas was 11.2 and 16.4% in the group of 40–49 and 50–59 year olds, respectively. Advanced adenoma was more common in 50–59 year olds (1.2 vs. 2.9%). Malignancy was not reported in these groups. Furthermore, 77.5 and 68.6% of adenomas were observed in the distal colon in the groups of 40–49 year olds and 50–59 year olds, whereas in the proximal colon, 22.2 and 57.1% of adenomas in the groups of 40–49 year olds and 50–59 year olds, respectively, were advanced adenomas.
In our study, male sex showed an association with adenoma. However, importantly, there was no significant association between age and colorectal adenoma. Although the prevalence of colorectal adenoma was similar in the two age groups investigated, the rate of advanced adenoma was higher in the group of individuals who were 50–59 years old, suggesting that colorectal cancer screening could be recommended at an age younger than 50 years. European Journal of Cancer Prevention 24:386–390 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
Rex et al., 2009). Despite these trends, recent studies have shown a similarity in the prevalence of colorectal polyps including potentially premalignant lesions when comparing groups of 40–49 year olds and 50–59 year olds (Rundle et al., 2008; Chung et al., 2010; Ahnen et al., 2014). These new data indicate a necessity for the initiation of screening earlier than usual to promote the detection and removal of precancerous lesions.
The burden of colorectal cancer (CRC) has been broadly acknowledged worldwide and is also a growing health concern in Iran (Jemal et al., 2010; Pourhoseingholi and Zali, 2012; Barouni et al., 2013; Somi et al., 2014). CRC is the third most prevalent cancer worldwide, but can also be readily diagnosed and prevented at an early stage with the use of appropriate screening methods (Jemal et al., 2010; Siegel et al., 2012). Colonoscopy is a known mainstay in the screening for CRC, and studies show that colonoscopy, in comparison with other screening modalities, has superior diagnostic and preventive value, leading to a reduction in the incidence and morbidity of CRC (Zauber et al., 2012; Stegeman et al., 2013; Young and Womeldorph, 2013). Recommendations made by professional medical societies prefer colonoscopic screening for the detection of precancerous lesions and CRC in its early stages in the average-risk population (Rundle et al., 2008; Yoo, 2010). According to current guidelines, colonoscopic screening begins at 50 years for the average-risk population; this consensus is based on evidence that the incidence of CRC is at its peak in the sixth decade (Rundle et al., 2008; 0959-8278 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
European Journal of Cancer Prevention 2015, 24:386–390 Keywords: adenoma, colonoscopy, colorectal cancer, polyp, screening GastroIntestinal and Liver Diseases Research Centre (GILDRC), Firoozgar Hospital, Iran University Medical Sciences (IUMS), Tehran, Iran Correspondence to Masoudreza Sohrabi, MD or Farhad Zamani, GastroIntestinal and Liver Diseases Research Centre (GILDRC), Firoozgar Hospital, Iran University Medical Sciences (IUMS), No. 74, Beh Afarin St., Karimkhan Ave., Valiasr Sq., Tehran, Iran Tel: + 98 21 82141633; fax: + 98 21 88941831; e-mails: [email protected], [email protected] Received 6 February 2014 Accepted 8 October 2014
As mentioned earlier, CRC is a growing health concern in Iran, and is among the top four cancers prevalent today (Kolahdoozan et al., 2010). However, there are scarce data specifically on average-risk groups in terms of the prevalence and related risk factors in this region. The aim of our study was to assess the prevalence of colorectal polyps, including potentially premalignant lesions, in asymptomatic average-risk individuals aged 40–49 and 50–59 years.
Methods Patients
We proposed a screening total colonoscopy for patients who visited various departments of Firoozgar Hospital DOI: 10.1097/CEJ.0000000000000097
Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
Colorectal adenoma in 40–60 year olds Hemmasi et al. 387
with symptoms not related to the lower gastrointestinal tract. Volunteers among these patients underwent a physical examination by three trained general practitioners, and in the case of any important findings, they were referred to a specialist. All those aged 40 years and older were enrolled from the years 2009 to 2012. Exclusion criteria were as follows: patients at an increased risk for CRC such as those with a personal or a family history of CRC, inflammatory bowel disease, recent involuntary weight loss, recent anemia, rectal bleeding, and altered bowel habits.
was assessed using the χ2-test. A P value of up to 0.05 was considered significant. Ethics
The study was approved by the ethics committee of Firoozgar hospital in accordance with the declaration of Helsinki. There was no cost for participants. The procedure of colonoscopy was explained to the patients and written informed consent was obtained from all the participants.
Results
Endoscopy
Colonoscopy was performed by three mentor gastroenterologists with at least 10 years of experience of colonoscopy in university hospitals where annually more than 4000 colonoscopies are performed. Patients were prepared for colonoscopy by self-administration of polyethylene glycol 24 h before the procedure along with a low-residue diet. During the procedure, participants were sedated with midazolam; petedine was also used when necessary. The procedures were performed using the Fujinon colonoscopy device (EPX-4400HD electronic video endoscopy System; Fujinon, Saitama, Japan). The endoscope was advanced to the cecum and confirmed by a photograph of the ileocecal valve or the appendiceal orifice. Successful endoscopy was defined as cecal intubation. Bowel preparation was classified as good, fair, or poor. Individuals with poor bowel preparation were invited to undergo a second colonoscopy procedure. Those with good or fair bowel preparation were included in the final analysis and the sizes of polyps were determined objectively by open biopsy forceps 1 cm in size. All polypoid lesions were removed for further histopathological evaluation. All samples were examined by a mentor gastrointestinal pathologist who had been part of many research projects. Data collection
Patient basic information and colonoscopy results were recorded. The data on the size, number, and location of polyps were extracted from colonoscopy reports. Furthermore, histopathological data were collected from pathology reports. Advanced adenomas were defined as lesion of at least 1 cm, with villous features and high-grade dysplasia. In case of multiple polyps, we took into account the most advanced one. Hyperplasic or inflammatory polyps were considered as nonneoplastic polyps and any type of adenoma or adenocarcinoma was defined as a neoplastic lesion. The distal colon was defined as the rectum, sigmoid and descending colon. Statistical analysis
The result was analyzed using the SPSS, version 16.0 for Windows, software (SPSS Inc., Chicago, Illinois, USA). Descriptive analysis was carried out for the prevalence of lesions, sex, and age. The correlation between demographic data and pathology findings and their prevalence
A total of 1380 colonoscopies were performed, with a success rate of 99%, without significant complications. The average withdrawal time was 15 min. A total of 737 individuals were enrolled in the study. The mean age of the participants was 50.1 ± 5.6 years. Of these, 389 (52.6%) were women. Normal colonoscopy was reported in 557 (75.4%) participants. A total of 124 polyps were detected, among which 106 adenomas were diagnosed. Nonadvanced and advanced adenomas were found in 90 (12.2%) and 16 (2.2%) participants (Table 1). Of all participants, 333 were 40–49 years old and 407 were 50–59 years old, mean age 44.6 ± 3.2 and 54.4 ± 2.7 years, respectively. Table 2 shows the findings in the two age groups. There were a higher number of women in both groups. Technical difficulties were reported in 7 and 10% of participants aged 40–49 and 50–59 years, respectively. The total number of polyps in the 40–49 and 50–59 year age groups was 50 (15.0%) and 78 (19.1%), respectively, whereas the number of colorectal adenomas was 11.7 and 16.4% in these two age groups, respectively. Advanced adenoma was common in the 50–59 years group (1.2 vs. 2.9%) (P = 0.01). Almost all of the advanced adenomas had a size less than 1 cm (Table 1). Malignancy was not detected in these groups. Interestingly, in these two age groups, 77.5 and 68.6% of all detected adenomas, respectively, were detected in the distal colon, that is the younger age group had a higher percentage of adenomas in the distal colon. Furthermore, 22.2 and 57.1% of proximal adenomas in the 40–49 and 50–59 year groups, respectively, were advanced adenomas. Table 3 shows the distribution of adenomas between the two groups according to the pathological features. Male sex was associated with the presence of adenoma (P = 0.01) and the presence of adenoma in the distal colon (P = 0.04). Furthermore, age showed an association with the presence of adenoma and the presence of adenoma in the distal colon, P = 0.04 and P = 0.01, respectively. Also, the number of polypoid lesions was associated with age (P = 0.04). Regression analyses showed male sex to be a risk factor for adenoma [odds ratio (OR) = 1.57; 95% confidence interval (CI) = 1.06–2.45] and advanced adenoma
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European Journal of Cancer Prevention 2015, Vol 24 No 5
Table 1
a nonsignificant association (OR = 1.37; 95% CI = 0.64–2.94). Furthermore, the analysis did not show a significant association between age and detection of adenoma in the 40–49 (OR = 1.36; 95% CI = 0.86–2.13) and 50–59 (OR = 2.51; 95% CI = 0.82–8.13) year groups. Age was a risk factor for the number of polypoid lesions, but this was not statistically significant (OR = 1.37; 95% CI =0.92–2.0).
Basic characteristics of the participants
Age (Mean ± SD) 40–49 (N = 333) 50–59 (N = 407) Total (N = 740)l Sex N (%) Male Female Endoscopic Findings N (%) Normal Polyps Diverticulum Solitary Ulcer IBD schema Morphology of polyps N (%) Sessile Pedanculated < 1 cm > 1 cm Location of polyps N (%) Distal Proximal Both sides Pathological Features N (%) Not adenoma Nonadvanced adenoma Advanced Adenoma
44.6 ± 3.2 54.4 ± 2.7 50.1 ± 5.6 389 (52.6) 351 (47.4) 557 (75.3) 128 (17.3) 43 (5.8) 4 (0.6) 11 (1.5)
Discussion According to the widely accepted model of sequential progression from adenoma to CRC, which is estimated to take at least 10 years, guidelines recommend the initiation of screening at least at the age of 50 years in the average-risk population (Mehran et al., 2003; Grau et al., 2010; Young and Womeldorph, 2013). In fact, it is worth noting the decrease in the incidence of CRC attributable to these screening programs in western countries (Heitman et al., 2009; Grau et al., 2010). Eastern countries have reported an increase in CRC, which could be attributed to changes in lifestyle brought about by industrialization (Lau and Sung, 2004; Leung et al., 2006; Chung et al., 2010; Ferlay et al., 2010; Yang et al., 2014). Despite these new developments in the region, adequate efforts have not been made to explore colorectal adenoma in the average-risk population, especially in those younger than 50 years of age. The majority of studies in this respect have been carried out in North America or developed Asian countries. In previous studies, Rundle et al. (2008), Thomas et al. (2011), and Imperiale et al. (2002), respectively, have reported the prevalence of adenoma in the average-risk population, aged 40–49 years, to be 14, 12.1, and 11% (Imperiale et al., 2002; Rundle et al., 2008; Thoma et al., 2011). Our findings are comparable with their results. However, the incidence reported here (Table 2) is lower than that from Asian developing countries (Liu et al., 2005; Chung et al., 2010). At present, no adequate data are available from the Middle East region, and to the best of our knowledge, this study is the first of its kind on CRC screening in the area. Furthermore, because of the similarities in various characteristics of individuals in this region, the results of this study could be considered a reliable estimate for the region as well. The prevalence of advanced adenoma in the present study is lower than that in previous studies (Liu et al., 2005; Rundle et al., 2008; Chung et al., 2010). This difference could be because of the study design, lifestyle, and number of participants. Moreover, it might
14 (1.9) 114 (15.4) 120 (93.7) 8 (6.3) 94 (73.4) 28 (21.9) 6 (4.7) 12 (9.4) 90 (12.2) 16 (2.2)
Prevalence of adenoma in relation to age, number, size, and location
Table 2
N (%)
Total number of patients Sex Male Female Adenoma Nonadvanced adenoma Advanced adenoma Number of adenomas 1 2 ≥3 Size of adenomas (cm) 1 Location of adenomas Distal Proximal Distal and proximal
Age 40–49
Age 50–59
333 (45)
407 (55)
156 (46.8) 177 (53.2)
195 (47.9) 212 (52.1)
35 (10.5) 4 (1.2)
55 (13.5) 12 (2.9)
34 (10.2) 4 (1.2) 2 (0.6)
50 (12.2) 13 (3.2) 4 (1.0)
38 (11.4) 2 (0.6)
64 (15.7) 3 (0.7)
30 (9.3) 8(2.4) 2 (0.6)
46 (11.3) 17 (4.17) 4 (0.9)
(OR = 3.60; 95% CI = 1.15–11.29) and also for adenoma in the distal colon (OR = 1.71; 95% CI = 1.12–2.63). For proximal colon adenoma, male sex was a risk factor with
Table 3
Pathological features of adenomas in relation to sex and age Pathological findings
Age group 40–49 50–59
Sex
Tubular
Serrated
Villous
Tubulovillous
High-grade dysplasia
Male Female Male Female
19 16 31 23
1 2 1 1
0 1 1 1
0 1 6 2
0 1 1 0
Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
Total [N (%)] 20 19 40 27
(51.2) (47.5) (59.7) (40.3)
Colorectal adenoma in 40–60 year olds Hemmasi et al. 389
be related to biological differences such as gene expression and genomic instability in the development of colorectal adenoma. In our study, we excluded patients with a family history of CRC or those who complained of a CRC-related symptom such as a change in bowel habit, rectal bleeding, anemia, or weight loss. The expertise of our endoscopists also needs to be acknowledged as the success rate of endoscopies was 99% and has contributed toward the strength of our study. Obviously, we need further studies on the biology and epidemiology of colorectal neoplasm in our region. In general, despite the higher prevalence of nonadvanced and advanced adenoma in the 50–60 year group, there was no significant difference in the prevalence of total colorectal adenoma between the two age groups, which in turn indicates the importance of screening of CRC at younger ages. In addition, we suggest that the nonsignificant discrepancy between the two groups might be a true aspect of the prevalence of colorectal adenoma among individuals with an age difference of about a decade, and the subsequent increase in malignancy in older groups. Of course, older age also means increased exposure to environmental factors as discussed in previous studies (Choe et al., 2007; Benson et al., 2008; Rundle et al., 2008; Boursi et al., 2009; Ahnen et al., 2014). It has been recognized that a family history of CRC is a predictive factor for sporadic CRC, and we excluded patients with a family history of CRC, which has not been a selection criterion in the majority of previous studies. The anatomical distribution of colorectal neoplastic lesions is another important issue that influences the selection of the modality of colorectal screening (Boursi et al., 2009; Chung et al., 2010; Aswakul et al., 2012). In the present study, about one-third of adenomas were located in the proximal colon, although the rate of proximal colon adenoma is higher among individuals older than 50 years. This finding highlights the role of colonoscopy as a preferred method for colon neoplastic lesion screening. Our findings also confirm that male sex has a significant association with the development of colorectal neoplastic lesions in both groups, as already reported in previous studies (Choe et al., 2007; Boursi et al., 2009; Heitman et al., 2009; Chung et al., 2010). In agreement with other studies, our results show that men older than 50 years of age tend to have more frequent polyp and adenoma formation. Thus, age and sex are factors influencing the development and progression of colonic polyps. The reasons for this are not clear, but we hypothesize that it could be because of the hormonal effects on the colorectal apparatus and that men are more exposed to environmental risk factors (Lieberman, 2005; Rundle et al., 2008). This result implies that sex needs to be given consideration. Studies have shown that sex itself is an independent risk factor and that colorectal screening should be sex specific (Chung et al., 2010; Corley et al.,
2013). Nonetheless, we do not make these recommendations for the initiation of screening. There are limitations that have to be taken into consideration for the interpretation of our results. As noted above, the sample size of this study was limited and there is a possibility of selection bias as the participants had knowledge beforehand about screening colonoscopy in an asymptomatic average-risk population. Moreover, although our participants were from different geographical areas, this study is not a multicenter study. Furthermore, data on the socioeconomic status, diet, and medication of the participants have not been taken into consideration. We also excluded those who had an indication for colonoscopy other than screening. Conclusion
Our study shows the prevalence of colorectal adenoma in individuals younger than 50 year of age as being notable. In the present study, male sex and age were found to be associated with the frequency of nonadvanced and advanced adenoma. Prospective multicentre studies are required to determine the benefits of colonoscopic screening of a younger population.
Acknowledgements The authors thank Dr Elham Ahmadnejad, Afsane Rahbari, Shakira Ghafor, Sima Aten, and all staff at GILDRC, Folad clinic, and Firoozgar Clinical Research Development Center. Conflicts of interest
There are no conflicts of interest.
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Heitman SJ, Ronksley PE, Hilsden RJ, Manns BJ, Rostom A, Hemmelgarn BR (2009). Prevalence of adenomas and colorectal cancer in average risk individuals: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 7:1272–1278. Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF (2002). Results of screening colonoscopy among persons 40 to 49 years of age. N Engl J Med 346:1781–1785. Jemal A, Siegel R, Xu J, Ward E (2010). Cancer statistics, 2010. CA Cancer J Clin 60:277–300. Kolahdoozan S, Sadjadi A, Radmard AR, Khademi H (2010). Five common cancers in Iran. Arch Iran Med 13:143–146. Lau P, Sung J (2004). Screening for colorectal cancer. Chin J Dig Dis 5:87–92. Leung WK, Ho KY, Kim WH, Lau JY, Ong E, Hilmi I, et al. Asia Pacific Working Group on Colorectal Cancer (2006). Colorectal neoplasia in Asia: a multicenter colonoscopy survey in symptomatic patients. Gastrointest Endosc 64:751–759. Lieberman D (2005). Race, gender, and colorectal cancer screening. Am J Gastroenterol 100:2756–2758. Liu HH, Wu MC, Peng Y, Wu MS (2005). Prevalence of advanced colonic polyps in asymptomatic Chinese. World J Gastroenterol 11:4731–4734. Mehran A, Jaffe P, Efron J, Vernava A, Liberman A (2003). Screening colonoscopy in the asymptomatic 50- to 59-year-old population. Surg Endosc 17:1974–1977. Pourhoseingholi MA, Zali MR (2012). Colorectal cancer screening: time for action in Iran. World J Gastrointest Oncol 4:82–83. Rex DK, Johnson DA, Anderson JC, Schoenfeld PS, Burke CA, Inadomi JM. American College of Gastroenterology (2009). American College of
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Research paper
Prevalence of colorectal adenoma in an average-risk population aged 40–50 versus 50–60 years Gholamreza Hemmasi, Masoudreza Sohrabi, Farhad Zamani, Hossein Ajdarkosh, Naser Rakhshani, Mahmoodreza Khoonsari, Mitra Ameli and Khadijeh Hatami According to current guidelines, screening colonoscopy begins at 50 years for the average-risk population, although there are not enough data on the incidence of precancerous lesions of individuals in the preceding decades. To evaluate the prevalence of colorectal polyps including potentially premalignant lesions in asymptomatic, average-risk individuals aged 40–49 versus 50–59 years, we offered total colonoscopy screening to individuals without any lower gastrointestinal symptoms. The primary end point was the prevalence of colorectal adenoma in two age groups. Of a total of 737 studies, 333 participants were 40–49 years old and 407 participants were 50–59 years old. The overall prevalence of adenomas was 11.2 and 16.4% in the group of 40–49 and 50–59 year olds, respectively. Advanced adenoma was more common in 50–59 year olds (1.2 vs. 2.9%). Malignancy was not reported in these groups. Furthermore, 77.5 and 68.6% of adenomas were observed in the distal colon in the groups of 40–49 year olds and 50–59 year olds, whereas in the proximal colon, 22.2 and 57.1% of adenomas in the groups of 40–49 year olds and 50–59 year olds, respectively, were advanced adenomas.
In our study, male sex showed an association with adenoma. However, importantly, there was no significant association between age and colorectal adenoma. Although the prevalence of colorectal adenoma was similar in the two age groups investigated, the rate of advanced adenoma was higher in the group of individuals who were 50–59 years old, suggesting that colorectal cancer screening could be recommended at an age younger than 50 years. European Journal of Cancer Prevention 24:386–390 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
Rex et al., 2009). Despite these trends, recent studies have shown a similarity in the prevalence of colorectal polyps including potentially premalignant lesions when comparing groups of 40–49 year olds and 50–59 year olds (Rundle et al., 2008; Chung et al., 2010; Ahnen et al., 2014). These new data indicate a necessity for the initiation of screening earlier than usual to promote the detection and removal of precancerous lesions.
The burden of colorectal cancer (CRC) has been broadly acknowledged worldwide and is also a growing health concern in Iran (Jemal et al., 2010; Pourhoseingholi and Zali, 2012; Barouni et al., 2013; Somi et al., 2014). CRC is the third most prevalent cancer worldwide, but can also be readily diagnosed and prevented at an early stage with the use of appropriate screening methods (Jemal et al., 2010; Siegel et al., 2012). Colonoscopy is a known mainstay in the screening for CRC, and studies show that colonoscopy, in comparison with other screening modalities, has superior diagnostic and preventive value, leading to a reduction in the incidence and morbidity of CRC (Zauber et al., 2012; Stegeman et al., 2013; Young and Womeldorph, 2013). Recommendations made by professional medical societies prefer colonoscopic screening for the detection of precancerous lesions and CRC in its early stages in the average-risk population (Rundle et al., 2008; Yoo, 2010). According to current guidelines, colonoscopic screening begins at 50 years for the average-risk population; this consensus is based on evidence that the incidence of CRC is at its peak in the sixth decade (Rundle et al., 2008; 0959-8278 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
European Journal of Cancer Prevention 2015, 24:386–390 Keywords: adenoma, colonoscopy, colorectal cancer, polyp, screening GastroIntestinal and Liver Diseases Research Centre (GILDRC), Firoozgar Hospital, Iran University Medical Sciences (IUMS), Tehran, Iran Correspondence to Masoudreza Sohrabi, MD or Farhad Zamani, GastroIntestinal and Liver Diseases Research Centre (GILDRC), Firoozgar Hospital, Iran University Medical Sciences (IUMS), No. 74, Beh Afarin St., Karimkhan Ave., Valiasr Sq., Tehran, Iran Tel: + 98 21 82141633; fax: + 98 21 88941831; e-mails: [email protected], [email protected] Received 6 February 2014 Accepted 8 October 2014
As mentioned earlier, CRC is a growing health concern in Iran, and is among the top four cancers prevalent today (Kolahdoozan et al., 2010). However, there are scarce data specifically on average-risk groups in terms of the prevalence and related risk factors in this region. The aim of our study was to assess the prevalence of colorectal polyps, including potentially premalignant lesions, in asymptomatic average-risk individuals aged 40–49 and 50–59 years.
Methods Patients
We proposed a screening total colonoscopy for patients who visited various departments of Firoozgar Hospital DOI: 10.1097/CEJ.0000000000000097
Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
Colorectal adenoma in 40–60 year olds Hemmasi et al. 387
with symptoms not related to the lower gastrointestinal tract. Volunteers among these patients underwent a physical examination by three trained general practitioners, and in the case of any important findings, they were referred to a specialist. All those aged 40 years and older were enrolled from the years 2009 to 2012. Exclusion criteria were as follows: patients at an increased risk for CRC such as those with a personal or a family history of CRC, inflammatory bowel disease, recent involuntary weight loss, recent anemia, rectal bleeding, and altered bowel habits.
was assessed using the χ2-test. A P value of up to 0.05 was considered significant. Ethics
The study was approved by the ethics committee of Firoozgar hospital in accordance with the declaration of Helsinki. There was no cost for participants. The procedure of colonoscopy was explained to the patients and written informed consent was obtained from all the participants.
Results
Endoscopy
Colonoscopy was performed by three mentor gastroenterologists with at least 10 years of experience of colonoscopy in university hospitals where annually more than 4000 colonoscopies are performed. Patients were prepared for colonoscopy by self-administration of polyethylene glycol 24 h before the procedure along with a low-residue diet. During the procedure, participants were sedated with midazolam; petedine was also used when necessary. The procedures were performed using the Fujinon colonoscopy device (EPX-4400HD electronic video endoscopy System; Fujinon, Saitama, Japan). The endoscope was advanced to the cecum and confirmed by a photograph of the ileocecal valve or the appendiceal orifice. Successful endoscopy was defined as cecal intubation. Bowel preparation was classified as good, fair, or poor. Individuals with poor bowel preparation were invited to undergo a second colonoscopy procedure. Those with good or fair bowel preparation were included in the final analysis and the sizes of polyps were determined objectively by open biopsy forceps 1 cm in size. All polypoid lesions were removed for further histopathological evaluation. All samples were examined by a mentor gastrointestinal pathologist who had been part of many research projects. Data collection
Patient basic information and colonoscopy results were recorded. The data on the size, number, and location of polyps were extracted from colonoscopy reports. Furthermore, histopathological data were collected from pathology reports. Advanced adenomas were defined as lesion of at least 1 cm, with villous features and high-grade dysplasia. In case of multiple polyps, we took into account the most advanced one. Hyperplasic or inflammatory polyps were considered as nonneoplastic polyps and any type of adenoma or adenocarcinoma was defined as a neoplastic lesion. The distal colon was defined as the rectum, sigmoid and descending colon. Statistical analysis
The result was analyzed using the SPSS, version 16.0 for Windows, software (SPSS Inc., Chicago, Illinois, USA). Descriptive analysis was carried out for the prevalence of lesions, sex, and age. The correlation between demographic data and pathology findings and their prevalence
A total of 1380 colonoscopies were performed, with a success rate of 99%, without significant complications. The average withdrawal time was 15 min. A total of 737 individuals were enrolled in the study. The mean age of the participants was 50.1 ± 5.6 years. Of these, 389 (52.6%) were women. Normal colonoscopy was reported in 557 (75.4%) participants. A total of 124 polyps were detected, among which 106 adenomas were diagnosed. Nonadvanced and advanced adenomas were found in 90 (12.2%) and 16 (2.2%) participants (Table 1). Of all participants, 333 were 40–49 years old and 407 were 50–59 years old, mean age 44.6 ± 3.2 and 54.4 ± 2.7 years, respectively. Table 2 shows the findings in the two age groups. There were a higher number of women in both groups. Technical difficulties were reported in 7 and 10% of participants aged 40–49 and 50–59 years, respectively. The total number of polyps in the 40–49 and 50–59 year age groups was 50 (15.0%) and 78 (19.1%), respectively, whereas the number of colorectal adenomas was 11.7 and 16.4% in these two age groups, respectively. Advanced adenoma was common in the 50–59 years group (1.2 vs. 2.9%) (P = 0.01). Almost all of the advanced adenomas had a size less than 1 cm (Table 1). Malignancy was not detected in these groups. Interestingly, in these two age groups, 77.5 and 68.6% of all detected adenomas, respectively, were detected in the distal colon, that is the younger age group had a higher percentage of adenomas in the distal colon. Furthermore, 22.2 and 57.1% of proximal adenomas in the 40–49 and 50–59 year groups, respectively, were advanced adenomas. Table 3 shows the distribution of adenomas between the two groups according to the pathological features. Male sex was associated with the presence of adenoma (P = 0.01) and the presence of adenoma in the distal colon (P = 0.04). Furthermore, age showed an association with the presence of adenoma and the presence of adenoma in the distal colon, P = 0.04 and P = 0.01, respectively. Also, the number of polypoid lesions was associated with age (P = 0.04). Regression analyses showed male sex to be a risk factor for adenoma [odds ratio (OR) = 1.57; 95% confidence interval (CI) = 1.06–2.45] and advanced adenoma
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European Journal of Cancer Prevention 2015, Vol 24 No 5
Table 1
a nonsignificant association (OR = 1.37; 95% CI = 0.64–2.94). Furthermore, the analysis did not show a significant association between age and detection of adenoma in the 40–49 (OR = 1.36; 95% CI = 0.86–2.13) and 50–59 (OR = 2.51; 95% CI = 0.82–8.13) year groups. Age was a risk factor for the number of polypoid lesions, but this was not statistically significant (OR = 1.37; 95% CI =0.92–2.0).
Basic characteristics of the participants
Age (Mean ± SD) 40–49 (N = 333) 50–59 (N = 407) Total (N = 740)l Sex N (%) Male Female Endoscopic Findings N (%) Normal Polyps Diverticulum Solitary Ulcer IBD schema Morphology of polyps N (%) Sessile Pedanculated < 1 cm > 1 cm Location of polyps N (%) Distal Proximal Both sides Pathological Features N (%) Not adenoma Nonadvanced adenoma Advanced Adenoma
44.6 ± 3.2 54.4 ± 2.7 50.1 ± 5.6 389 (52.6) 351 (47.4) 557 (75.3) 128 (17.3) 43 (5.8) 4 (0.6) 11 (1.5)
Discussion According to the widely accepted model of sequential progression from adenoma to CRC, which is estimated to take at least 10 years, guidelines recommend the initiation of screening at least at the age of 50 years in the average-risk population (Mehran et al., 2003; Grau et al., 2010; Young and Womeldorph, 2013). In fact, it is worth noting the decrease in the incidence of CRC attributable to these screening programs in western countries (Heitman et al., 2009; Grau et al., 2010). Eastern countries have reported an increase in CRC, which could be attributed to changes in lifestyle brought about by industrialization (Lau and Sung, 2004; Leung et al., 2006; Chung et al., 2010; Ferlay et al., 2010; Yang et al., 2014). Despite these new developments in the region, adequate efforts have not been made to explore colorectal adenoma in the average-risk population, especially in those younger than 50 years of age. The majority of studies in this respect have been carried out in North America or developed Asian countries. In previous studies, Rundle et al. (2008), Thomas et al. (2011), and Imperiale et al. (2002), respectively, have reported the prevalence of adenoma in the average-risk population, aged 40–49 years, to be 14, 12.1, and 11% (Imperiale et al., 2002; Rundle et al., 2008; Thoma et al., 2011). Our findings are comparable with their results. However, the incidence reported here (Table 2) is lower than that from Asian developing countries (Liu et al., 2005; Chung et al., 2010). At present, no adequate data are available from the Middle East region, and to the best of our knowledge, this study is the first of its kind on CRC screening in the area. Furthermore, because of the similarities in various characteristics of individuals in this region, the results of this study could be considered a reliable estimate for the region as well. The prevalence of advanced adenoma in the present study is lower than that in previous studies (Liu et al., 2005; Rundle et al., 2008; Chung et al., 2010). This difference could be because of the study design, lifestyle, and number of participants. Moreover, it might
14 (1.9) 114 (15.4) 120 (93.7) 8 (6.3) 94 (73.4) 28 (21.9) 6 (4.7) 12 (9.4) 90 (12.2) 16 (2.2)
Prevalence of adenoma in relation to age, number, size, and location
Table 2
N (%)
Total number of patients Sex Male Female Adenoma Nonadvanced adenoma Advanced adenoma Number of adenomas 1 2 ≥3 Size of adenomas (cm) 1 Location of adenomas Distal Proximal Distal and proximal
Age 40–49
Age 50–59
333 (45)
407 (55)
156 (46.8) 177 (53.2)
195 (47.9) 212 (52.1)
35 (10.5) 4 (1.2)
55 (13.5) 12 (2.9)
34 (10.2) 4 (1.2) 2 (0.6)
50 (12.2) 13 (3.2) 4 (1.0)
38 (11.4) 2 (0.6)
64 (15.7) 3 (0.7)
30 (9.3) 8(2.4) 2 (0.6)
46 (11.3) 17 (4.17) 4 (0.9)
(OR = 3.60; 95% CI = 1.15–11.29) and also for adenoma in the distal colon (OR = 1.71; 95% CI = 1.12–2.63). For proximal colon adenoma, male sex was a risk factor with
Table 3
Pathological features of adenomas in relation to sex and age Pathological findings
Age group 40–49 50–59
Sex
Tubular
Serrated
Villous
Tubulovillous
High-grade dysplasia
Male Female Male Female
19 16 31 23
1 2 1 1
0 1 1 1
0 1 6 2
0 1 1 0
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Total [N (%)] 20 19 40 27
(51.2) (47.5) (59.7) (40.3)
Colorectal adenoma in 40–60 year olds Hemmasi et al. 389
be related to biological differences such as gene expression and genomic instability in the development of colorectal adenoma. In our study, we excluded patients with a family history of CRC or those who complained of a CRC-related symptom such as a change in bowel habit, rectal bleeding, anemia, or weight loss. The expertise of our endoscopists also needs to be acknowledged as the success rate of endoscopies was 99% and has contributed toward the strength of our study. Obviously, we need further studies on the biology and epidemiology of colorectal neoplasm in our region. In general, despite the higher prevalence of nonadvanced and advanced adenoma in the 50–60 year group, there was no significant difference in the prevalence of total colorectal adenoma between the two age groups, which in turn indicates the importance of screening of CRC at younger ages. In addition, we suggest that the nonsignificant discrepancy between the two groups might be a true aspect of the prevalence of colorectal adenoma among individuals with an age difference of about a decade, and the subsequent increase in malignancy in older groups. Of course, older age also means increased exposure to environmental factors as discussed in previous studies (Choe et al., 2007; Benson et al., 2008; Rundle et al., 2008; Boursi et al., 2009; Ahnen et al., 2014). It has been recognized that a family history of CRC is a predictive factor for sporadic CRC, and we excluded patients with a family history of CRC, which has not been a selection criterion in the majority of previous studies. The anatomical distribution of colorectal neoplastic lesions is another important issue that influences the selection of the modality of colorectal screening (Boursi et al., 2009; Chung et al., 2010; Aswakul et al., 2012). In the present study, about one-third of adenomas were located in the proximal colon, although the rate of proximal colon adenoma is higher among individuals older than 50 years. This finding highlights the role of colonoscopy as a preferred method for colon neoplastic lesion screening. Our findings also confirm that male sex has a significant association with the development of colorectal neoplastic lesions in both groups, as already reported in previous studies (Choe et al., 2007; Boursi et al., 2009; Heitman et al., 2009; Chung et al., 2010). In agreement with other studies, our results show that men older than 50 years of age tend to have more frequent polyp and adenoma formation. Thus, age and sex are factors influencing the development and progression of colonic polyps. The reasons for this are not clear, but we hypothesize that it could be because of the hormonal effects on the colorectal apparatus and that men are more exposed to environmental risk factors (Lieberman, 2005; Rundle et al., 2008). This result implies that sex needs to be given consideration. Studies have shown that sex itself is an independent risk factor and that colorectal screening should be sex specific (Chung et al., 2010; Corley et al.,
2013). Nonetheless, we do not make these recommendations for the initiation of screening. There are limitations that have to be taken into consideration for the interpretation of our results. As noted above, the sample size of this study was limited and there is a possibility of selection bias as the participants had knowledge beforehand about screening colonoscopy in an asymptomatic average-risk population. Moreover, although our participants were from different geographical areas, this study is not a multicenter study. Furthermore, data on the socioeconomic status, diet, and medication of the participants have not been taken into consideration. We also excluded those who had an indication for colonoscopy other than screening. Conclusion
Our study shows the prevalence of colorectal adenoma in individuals younger than 50 year of age as being notable. In the present study, male sex and age were found to be associated with the frequency of nonadvanced and advanced adenoma. Prospective multicentre studies are required to determine the benefits of colonoscopic screening of a younger population.
Acknowledgements The authors thank Dr Elham Ahmadnejad, Afsane Rahbari, Shakira Ghafor, Sima Aten, and all staff at GILDRC, Folad clinic, and Firoozgar Clinical Research Development Center. Conflicts of interest
There are no conflicts of interest.
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