Skip to content

Advertisement

Open Access
Open Peer Review

This article has Open Peer Review reports available.

How does Open Peer Review work?

High prevalence of advanced colorectal neoplasia in the Thai population: a prospective screening colonoscopy of 1,404 cases

  • Bunchorn Siripongpreeda1Email author,
  • Chulabhorn Mahidol1, 2, 3,
  • Navara Dusitanond1,
  • Tassanee Sriprayoon1,
  • Bunlung Muyphuag1,
  • Thaniya Sricharunrat1,
  • Narongchai Teerayatanakul1,
  • Watanya Chaiwong1,
  • Wipra Worasawate1,
  • Prassanee Sattayarungsee1,
  • Juthamas Sangthongdee1,
  • Jirapa Prarom1,
  • Gaidganok Sornsamdang1,
  • Kamonwan Soonklang1,
  • Kasiruck Wittayasak1 and
  • Chirayu U. Auewarakul1, 3
BMC GastroenterologyBMC series – open, inclusive and trusted201616:101

https://doi.org/10.1186/s12876-016-0526-0

Received: 1 November 2015

Accepted: 18 August 2016

Published: 23 August 2016

Abstract

Background

Increasing morbidity and mortality from colorectal cancer is evident in recent years in the developing Asian nations. Particularly in Thailand and most neighbouring low-income countries, screening colonoscopy is not yet recommended nor implemented at the national policy level.

Methods

Screening colonoscopy was offered to 1,500 healthy volunteers aged 50–65 years old who were registered into the program between July 2009 and June 2010. Biopsy and surgery was performed depending on the identified lesions. Fecal immunochemical tests (FIT) were additionally performed for comparison with colonoscopy.

Results

There were 1,404 participants who underwent colonoscopy. The mean age of the cohort was 56.9 ± 4.2 years and 69.4 % were females. About 30 % (411 cases) of all colonoscopies had abnormal colonoscopic findings, and of these, 256 cases had adenomatous polyps. High risk adenomas (villous or tubulovillous or high grade dysplasia or size > 1 cm or > 3 adenomatous polyps) were found in 98 cases (7 %), low risk adenoma in 158 cases (11.3 %), and hyperplastic polyps in 119 cases (8.5 %). Eighteen cases (1.3 %) had colorectal cancer and 90 % of them (16 cases) were non-metastatic including five stage 0 cases, seven stage I cases, and four stage IIA cases. Only two cases had metastasis: one to regional lymph nodes (stage IIIB) and another to other organs (stage IVA). The most common cancer site was the distal intestine including rectum (7 cases, 38.9 %) and sigmoid colon (7 cases, 38.9 %). Ten colorectal cancer cases had positive FIT whereas 8 colorectal cancer cases were FIT-negative. The sensitivity and specificity of FIT was 55.6 % and 96.2 %, respectively, while the positive predictive value was 16.4 % and negative predictive value was 99.4 %. The overall survival of colorectal cancer cases at 5-year was 83.3 %.

Conclusion

High prevalence of colorectal cancer and high-risk adenoma was found in the Thai population aged 50–65 years old by screening colonoscopy. FIT was not sensitive enough to detect colorectal cancer in this asymptomatic cohort. Integration of screening colonoscopy into the national cancer screening program should be implemented to detect early cases of advanced colorectal neoplasia and improve survival of colorectal cancer patients in Thailand.

Keywords

Colorectal cancerAdenomaAdvanced colorectal neoplasiaScreening colonoscopyFecal immunochemical testNational policy

Background

Colorectal cancer is one of the most common causes of cancer death globally each year, along with lung, liver, prostate, and breast cancer [1]. Disease incidence of economically developed countries in Asia such as Japan, Korea and Singapore abruptly approached the level of the Western countries. Data from the National Cancer Institute of Thailand Cancer Registry also showed a gradual increase in the number of new colorectal cancer patients in recent years with increased advance stage cases identified [2]. Colorectal cancer screening can diagnose cases in early stages, decrease cancer mortality and potentially prevent this disease [3, 4]. Detection and proper management of advanced colorectal neoplasia which included malignant and some high risk colorectal lesions that need therapeutic interventions should prevent progression and worse outcomes in the affected cases.

Colonoscopy is one of the cancer screening tests that achieves goals of premalignant and early stage cancer detection and when it is coupled with polypectomy, it can prevent and reduce the incidence of disease, and finally of all results, decrease mortality from colorectal cancer [35]. Therefore, colonoscopy is recommended in colorectal cancer screening guideline since 1997 [6]. However, screening colonoscopy is presently not included in the national colorectal cancer screening policy in Thailand nor widely recommended for the Thai population. Most previous studies utilized fecal immunochemical test (FIT) as a first screening tool although the majority of the Thai population do not undergo such testing on a regular basis [79]. This study aimed to provide essential information on consideration of implementation of a nation-wide colorectal cancer screening program in Thailand and developing countries. Screening colonoscopy was performed as a first screening tool in all cases while FIT was done as a comparison.

Methods

Study participants

After the study protocol had been approved by the Human Research Ethical Committee of Chulabhorn Research Institute, we enrolled participants between 50 and 65 years of age with no past medical history of colorectal cancer or poorly controlled underlying diseases in July 2009. In total, 1,612 applicants expressed their willingness to participate in this project. All participants were educated about colorectal cancer and screening methods that were to be used in this study as well as study objectives, details of each procedure including possible complications, and usage of data from the study. Some patients were excluded based on age, poor medical problem control, or the inability to be followed over a long-term period. Finally, 1,404 participants underwent colonoscopy between July 2009 and June 2010 after they provided informed consent. Their demographic data, medical history, physical examination, and pre-operative management were collected.

Screening colonoscopy and pathological diagnosis

Bowel preparation before colonoscopy was established by using 90 mL of sodium phosphate after a low fiber diet for 2 days. All participants underwent colonoscopy under intravenous anaesthesia. The colonoscopic findings in each colonic section were recorded. If abnormal mucosal findings or polyps were found, the removed tissue was sent for pathological diagnosis. We categorized abnormal tissue from colonoscopic findings and pathological reports into malignant, high-risk adenoma, low risk adenoma, and non-adenomatous polyps, for which each group underwent different appropriate management according to National Comprehensive Cancer Network (NCCN) guidelines for colorectal cancer screening. High-risk adenoma cases recommended to have repeat colonoscopy earlier than low risk adenoma cases included one of the following colonoscopic and pathological criteria: size ≥1 cm, ≥3 adenomas, or tubulovillous or villous adenoma or high grade dysplasia. All malignant cases were diagnosed by pathological staging using the Seventh edition of the Union for International Cancer Control (UICC) TNM Classification of Malignant Tumours [10]. Patients with colorectal cancer were treated according to the NCCN Guidelines [11]. Participants without malignancy were seen annually in the clinic for general evaluation, and FIT and follow-up colonoscopy was to be performed based on clinical findings and colorectal cancer risks. The second screening colonoscopy was respectively performed at 3, 4, and 5 years follow-up for high risk adenoma cases, low risk adenoma/hyperplastic polyp cases, and normal colonoscopy cases.

Screening fecal immunochemical test (FIT)

FIT was performed in parallel to screening colonoscopy by fecal occult blood (FOB) one-step test device, a rapid chromatographic immunoassay (Abon Biopharm Hangzhou, China) with relative sensitivity of 93.6 % and relative specificity of 99.1 % [12, 13]. The FOB one-step test can detect fecal blood as low as 50 ng/mL or 6 μg/g feces and is specific for human hemoglobin at a concentration of 1.0 mg/mL. Fecal specimens were self-collected from the first bowel movement in the morning of the appointed date for FIT test which occurred before the start of bowel preparation for screening colonoscopy. The specimens were stored in a clean and dry container and brought in to the hospital by the participants at environmental temperature. The participants were instructed to hand in the samples to the laboratory within 6 h of collection.

Statistical analysis

Statistical analyses were performed with STATA version 12.1. Data of the participants were reported as means and standard deviation for continuous variables and as proportions and absolute counts for categorical variables. We also estimated FIT sensitivity, specificity and predictive values in detecting colorectal cancer.

Results

Demographic characteristics of the study cohort

Of the 1,404 participants, there were 429 males and 975 females, with a mean age of 56.9 ± 4.2 years. Most (81.8 %) of the participants lived in Bangkok Metropolitan and connective territorial provinces during the time of the colonoscopy. Overall, 96.1 % of participants had no lower gastrointestinal symptoms, i.e. bowel habit changes or lower gastrointestinal bleeding or decreased stool calibre or anemia, and the majority (91.7 %) did not have a family history of colorectal cancer, respectively (Table 1). Complete colonoscopy was accomplished in 99.6 % (1,399) of cases. In five incomplete colonoscopy cases, patients were further investigated by CT colonography, all of which produced normal findings.
Table 1

Demographic data of the study cohort (N = 1,404)

Variable

N (%)

Sex

 Male

429 (30.6)

 Female

975 (69.4)

Age

56.9 ± 4.2

BMI

  > 25

640 (45.6)

  ≤ 25

764 (54.4)

Area

 Bangkok and territories

1148 (81.8)

 Other

256 (18.2)

Lower gastrointestinal tract symptoms

 Yes

55 (3.9)

 No

1349 (96.1)

Family history of colorectal cancer

 Yes

117 (8.3)

 No

1287 (91.7)

Screening colonoscopy findings

About 30 % (411 cases) of all colonoscopies had abnormal colonoscopic findings. Malignancy was found in 1.3 % (18 cases) of all cases. Of all colonoscopies, 18.2 % (256 cases) had adenomatous polyps, of which 7 % (98 cases) were high risk adenoma. The other 9.8 % (137 cases) had abnormal tissue, of which 8.5 % (119 cases) were hyperplastic polyps (Fig. 1). The pathological diagnosis of malignant tissue in this study showed two cases of carcinoid tumor out of 18 cases. Others were adenocarcinoma with stages varying from stage 0 to stage 4 (Table 2). Nearly 90 % (16 cases) were non-metastatic colorectal cancer; five stage 0 cases, seven stage I cases, and four stage IIA cases. Only two cases from our study had metastasis: one to regional lymph nodes (stage IIIB) and another to other organs (stage IVA). Most abnormalities that required tissue diagnosis were found in the left side of the colon (Fig. 2). The most common cancer site was rectum (7 cases, 38.9 %) and sigmoid colon (7 cases, 38.9 %). Also, the most common site for high risk adenoma and low risk adenoma was sigmoid colon (30 % and 35 %, respectively) and the second most common sites were ascending and transverse colon. Most adenoma had only low grade dysplasia. Only one case of high grade dysplasia was detected in a tubulovillous adenoma case. The gender proportion in 256 cases of adenoma group was 117 males (45.7 %) and 139 females (54.3 %). For colorectal cancer cases, they were 8 males (44.4 %) and 10 females (55.6 %).
Fig. 1

Pathological diagnosis from screening colonoscopy; aincluding inflammatory polyp, colitis, lipoma and loss specimens; bincluding diverticulosis without biopsied tissues and hemorrhoids

Table 2

Staging and 5-year survival rates of 18 colorectal cancer cases diagnosed by screening colonoscopy

Variable

N (%)

Screening colonoscopy

 Cancer

18 (100)

Stage

 0

5 (27.8)

 I

7 (38.9)

 IIA

4 (22.2)

 IIIB

1 (5.6)

 IVA

1 (5.6)

 5-year survival rate

15 (83.3)a

aOne case died from unrelated hepatobiliarycancer

Fig. 2

Anatomical site distribution of abnormal colonic tissue from screening colonoscopy

Table 3 summarizes histopathology findings of 55 cases with complaining symptoms that may have suggested cancer at the outset of screening and 117 cases with a family history of colorectal cancer. Among 55 cases, 3 developed colorectal cancer (5.5 %) as compared with 15 cases in asymptomatic cases (1.1 %) (p = 0.031). Various types of adenomas and polyps were also found in symptomatic cases. If symptomatic cases were excluded, high risk adenoma and colorectal cancer accounted for 8.15 % (110/1,349 cases). Four colorectal cancer cases developed in participants with a family history of colorectal cancer (3.4 %) whereas 14 colorectal cancer cases (1.1 %) were found in a no family history group (p = 0.056). Hyperplastic polyps tended to be more common in participants with a family history of colorectal cancer.
Table 3

Histological comparison between cases with or without symptoms at screening day 0 visit and between cases with or without family history of colorectal cancer

 

Symptoms that may suggest colorectal cancer at the outset

Family history of colorectal cancer

Yes 55 cases

No 1,349 cases

P-value

Yes 117 cases

No 1,287 cases

P-value

Screening colonoscopy

 Colorectal cancer

3 (5.5)

15 (1.1)

0.031b

4 (3.4)

14 (1.1)

0.056b

Stage

      

 0

1

4

 

2

3

 

 I

0

6

 

0

6

 

 IIA

1

4

 

1

4

 

 IIIB

0

1

 

1

0

 

 IVA

1

0

 

0

1

 

 High risk adenoma

3 (5.5)

95 (7.0)

 

0 (0.0)

98 (7.6)

 

 Low risk adenoma

10 (18.2)

148 (11.0)

 

13 (11.1)

145 (11.3)

 

 Hyperplastic polyp

3 (5.5)

116 (8.6)

 

14 (12.0)

105 (8.2)

 

 Other pathological diagnosisa

0 (0.0)

18 (1.3)

 

2 (1.7)

16 (1.2)

 

 No colorectal tumor

36 (65.5)

957 (70.9)

 

84 (71.8)

909 (70.6)

 

aInflammatory polyp, colitis, and lipoma

bFisher Exact Test

Sensitivity and specificity of FIT in diagnosis of colorectal cancer

As shown in Table 4, 10/18 colorectal cancer cases had positive FIT whereas 8 colorectal cancer cases were FIT-negative. The sensitivity and specificity of FIT in detection of colorectal cancer was 55.6 % and 96.2 %, respectively, while the positive predictive value (PPV) was 16.4 % and the negative predictive value (NPV) was 99.4 %. Table 5 shows the distribution of FIT-positivity among participants with various histopathology findings. Most of adenoma cases were FIT-negative. FIT-positive non-cancer cases included6 high risk adenoma, 3 low risk adenoma, 8 hyperplastic polyps, and 33 cases with normal colonoscopy results.
Table 4

Diagnostic value of FIT in the diagnosis of colorectal cancer

FIT

Colonoscopy

Malignancy

No malignancya

Positive

10

51

Negative

8

1,295

Total

18

1,346

aFIT not done in 40 cases

Sensitivity (55.6 %), Specificity (96.2 %), PPV (16.4 %), NPV (99.4 %)

Table 5

Histopathology characteristics of cases with FIT-positive and FIT-negative results

Histopathology

FITa

Positive N (%)

Negative N (%)

Colorectal cancer

10 (16.4)

8 (0.6)

High risk adenoma

6 (9.8)

87 (6.7)

Low risk adenoma

3 (4.9)

152 (11.7)

Hyperplastic polyp

8 (13.1)

106 (8.1)

Other pathological diagnosisb

1 (1.6)

17 (1.3)

No colorectal tumor

33 (54.1)

933 (71.6)

aFIT not done in 40 cases

bInflammatory polyp, colitis, lipoma

Follow-up of study participants and survival of colorectal cancer cases

In the follow-up period after colonoscopic screening, there were three additional new cases of colorectal cancer. Two cases of intramucosal carcinoma of sigmoid colon and another case with stage 1 anal canal adenocarcinoma were found in the second year from the group previously identified as high risk adenoma, low risk adenoma and hyperplastic polyp, respectively. The mortality due to colorectal cancer cases in this study was 3/18 cases: 1 case with stage IV disease died in the first year, 1 case with stage IIA in the fourth year, and another case in stage I died from unrelated primary hepatobiliary cancer. The overall survival of colorectal cancer cases at 5 year was 83.3 % (88.9 % if excluded 1 death from unrelated cancer).

Discussion

The discovery rate of high risk adenoma and invasive colorectal cancer in this study (8.15 %) was nearly twice that of advanced colorectal neoplasia in the asymptomatic population (4.5 %) as reported from multiple studies in Asia but comparable to that of the symptomatic population (7.8 %) [14]. These patients should receive therapeutic intervention before progression to more advanced disease. When we excluded the amount criteria from the high risk adenoma group, the prevalence of advanced colorectal neoplasia in our study (3 %) and also adenocarcinoma (1.3 %) were still comparable to the country with a high incidence of colorectal cancer [14, 15]. Prior hospital-based reports and retrospective studies from Thailand also showedcancer detection rate by colonoscopy of 0.6–7.1 % in different studied population [79, 16, 17]. These previous studies utilized FIT as a first screening tool and were unlike our study whereby colonoscopy was performed as a first screening tool.

The abnormal colonic tissue (29.3 %) findings from our screening colonoscopy study are in the range of polyp detection rates (25–37 %) reported in other studies from within and outside Thailand [1620]. Both adenomatous polyp and hyperplastic polyposis can accumulate worse genetic changes and become malignant [21, 22]. Therefore, colorectal cancer screening would benefit this population. Although most abnormalities that required tissue diagnosis were found in the left side of the colon, complete colonoscopy should be done to include low and high risk adenomas in the second most common locations, the transverse and ascending colon.

There are some key differences in the selection of subjects for our study compared with others: our study included screening criteria for an age group at high risk of colorectal cancer [23], while others included data from a symptom-related group. Moreover, this result might not represent the incidence of colorectal cancer from all regions in Thailand because most (81.8 %) of the participants were from the Bangkok metropolitan region and territories. If this finding represented the real incidence of colorectal cancer in our population, or perhaps even in urban and suburban areas, launching a national colorectal cancer screening policy should be considered for specific groups. Other factors that might affect a high yield of colorectal cancer findings include public information that may stimulate awareness and access to reluctant cancer patients.

Problems related to colonoscopy screening include its invasiveness, complications, high financial cost, and need of specialized endoscopists; these reasons were reported as causes of low colorectal screening adherence in well developed countries [24, 25]. Therefore, other more practical screening methods were utilized instead of colonoscopy. The sensitivity of FIT for cancer detection in our study (55 %) was comparable to Guaiac fecal occult blood test (37–79 %) but somewhat lower than results of FIT in other studies (79 %) [26, 27]. In some resource-limited countries, fecal-based screening may play a major role in decreasing colorectal cancer mortality with high subject acceptance rates [28, 29]. However, in our study, the sensitivity of FIT of 55.6 % was deemed inadequate to detect colorectal cancer cases and 8/18 cancer cases had negative FITs.

There are no recommendations for any other surveillance procedure after screening colonoscopy, but endoscopic management after colonoscopic and pathologic findings have been suggested [3034]. However, in this study, cases of colorectal cancer were found before the recommended period of surveillance colonoscopy, which were similar to the findings of other studies [5, 24, 3539]. Moreover, some cases also suffered from unrelated types of cancer. Thus, some individual risk criteria such as smoking, a family history of biliary tract cancer which are common in Thailand should be concerned for improvement of screening benefits in specific groups of patients [40, 41]. Quality indices [42, 43], technology of colonoscopy [44] and other predictors [4548] should be included for detection of these interval cancers. Particularly, with the aging population in Thailand, proper screening and surveillance programsneed to be further evaluated [3].

The mortality caused by colorectal cancer in our study after monitoring for 5 years was only two cases from colorectal cancer. Another case died from unrelated hepatobiliary cancer. So the 5-yearsurvival rate after screening colonoscopy and standard treatment of detected colorectal cancer cases in this study, even including five cases (27.8 %) with stage IIA and IIIB, was excellent at 88.9 %. This survival rate was comparable to survival of stage I colorectal cancer (87–92 %) after standard staging and treatment [49].

Conclusions

In our study population aged 50–65 years old, 30 % of colonoscopically screened cases had abnormal colonic lesions that needed further pathological diagnosis. The colorectal cancer detection rate was 1.3 % and the overall prevalence of advanced colorectal neoplasia was 3 % by screening colonoscopy. Tissue abnormalities were found more in the distal part than the proximal part of the large intestine. The overall survival of colorectal cancer patients diagnosed by colonoscopic screening was 83 %. FIT was inadequate to detect advanced colorectal neoplasia and missed almost half of the colorectal cases. We suggest that screening colonoscopy should be implemented as part of the National Colorectal Cancer Screening Program in Thailand.

Abbreviations

BMI: 

Body mass index

CT colonography: 

Comperized tomographic colonography

FIT: 

Fecal immunochemical tests

FOB: 

Fecal occult blood

NCCN: 

National Comprehensive Cancer Network

NPV: 

Negative predictive value

PPV: 

Positive predictive value

UICC: 

The Union for International Cancer Control

Declarations

Acknowledgements

We appreciated all volunteer participants and Chulabhorn Hospital staff, particularly the Colorectal Cancer Care Team, the Nursing Division and the Data Management Unit, who generously spared their time for the accomplishment and fulfillment of this project.

Funding

This study was funded by Chulabhorn Hospital Research Grant.

Availability of data and materials

We do not wish to share all the data at the present time as the project is still ongoing. The full data set will be available by 2019 when the whole project is completed. Researchers wishing to access the data for this study should contact the corresponding author.

Authors’ contributions

BS performed colonoscopy, data collection and manuscript drafting. CM was responsible for the initiation and execution of the entire project. ND, BM and TS performed colonoscopy. TSr and NT reviewed and reported pathological results. WC and WW were responsible for anesthesia of the participants. PS, JJ and JP helped coordinating the appointment and follow-ups of the participants and patients. GS was responsible for FIT analysis. KW and KS performed data collection, data management and statistical analysis. CA reviewed the study design, monitored the project, and critically revised the final manuscript. All authors approved to the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

This research had been approved by the Human Research Ethical Committee of Chulabhorn Research Institute (certificate no. 05/2556).

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Chulabhorn Hospital, Bangkok, Thailand
(2)
Chulabhorn Research Institute, Bangkok, Thailand
(3)
Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand

References

  1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–917.View ArticlePubMedGoogle Scholar
  2. Hospital based cancer registry National Cancer Institute of Thailand. 2002–2011. http://www.nci.go.th/en/cancer_record/cancer_rec1.html. Accessed 20 July 2012.
  3. Zauber AG, Winawer SJ, O’Brien MJ, Lansdorp-Vogelaar I, van Ballegooijen M, Hankey BF, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med. 2012;366(8):687–96.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Winawer SJ. The history of colorectal cancer screening: a personal perspective. Dig Dis Sci. 2015;60(3):596–608.View ArticlePubMedGoogle Scholar
  5. Friedrich K, Gruter L, Gotthardt D, Eisenbach C, Stremmel W, Scholl SG, et al. Survival in patients with colorectal cancer diagnosed by screening colonoscopy. Gastrointest Endosc. 2015;82(1):133–7.View ArticlePubMedGoogle Scholar
  6. Winawer SJ, Fletcher RH, Miller L, Godlee F, Stolar MH, Mulrow CD, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology. 1997;112(2):594–642.View ArticlePubMedGoogle Scholar
  7. Khuhaprema T, Sangrajrang S, Lalitwongsa S, Chokvanitphong V, Raunroadroong T, Ratanachu-ek T, et al. Organised colorectal cancer screening in Lampang Province, Thailand: preliminary results from a pilot implementation programme. BMJ Open. 2014;4(1):1–11.View ArticleGoogle Scholar
  8. Aniwan S, Rerknimitr R, Kongkam P, Wisedopas N, Ponuthai Y, Chaithongrat S, et al. A combination of clinical risk stratification and fecal immunochemical test results to prioritize colonoscopy screening in asymptomatic participants. Gastrointest Endosc. 2015;81(3):719–27.View ArticlePubMedGoogle Scholar
  9. Lohsiriwat V. Accuracy of self-checked fecal occult blood testing for colorectal cancer in Thai patients. Asian Pac J Cancer Prev. 2014;15(18):7981–4.View ArticlePubMedGoogle Scholar
  10. Sobin LH, Wittekind C, M. G. TNM classification of malignant tumours (UICC S.). 7th ed. New York: Wiley-Blackwell; 2009. p. 73–7.Google Scholar
  11. Network NCC. NCCN Guidelines, Colorectal Cancer, Version I 2010. 2010.Google Scholar
  12. Simon JB. Occult blood screening for colorectal carcinoma: a critical review. Gastroenterology. 1985;88(3):820–37.View ArticlePubMedGoogle Scholar
  13. Blebea J, McPherson RA. False-positive guaiac testing with iodine. Arch Pathol Lab Med. 1985;109(5):437–40.PubMedGoogle Scholar
  14. Sung JJ, Lau JY, Young GP, Sano Y, Chiu HM, Byeon JS, et al. Asia Pacific consensus recommendations for colorectal cancer screening. Gut. 2008;57(8):1166–76.View ArticlePubMedGoogle Scholar
  15. Bae T, Ha Y, Kim C, Lee J, Ha K, Shin S, et al. Distribution of the colonoscopic adenoma detection rate according to age: is recommending colonoscopy screening for koreans over the age of 50 safe? Ann Coloproctol. 2015;31(2):46–51.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Rerknimitr R, Ratanapanich W, Kongkam P, Kullavanijaya P. Differences in characteristics of colorectal neoplasm between young and elderly Thais. World J Gastroenterol. 2006;12(47):7684–9.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Aswakul P, Prachayakul V, Lohsiriwat V, Bunyaarunnate T, Kachintorn U. Screening colonoscopy from a large single center of Thailand - something needs to be changed? Asian Pac J Cancer Prev. 2012;13(4):1361–4.View ArticlePubMedGoogle Scholar
  18. Wisedopas N, Thirabanjasak D, Taweevisit M. A retrospective study of colonic polyps in King Chulalongkorn Memorial Hospital. J Med Assoc Thai. 2005;88 Suppl 4:S36–41.PubMedGoogle Scholar
  19. Arayasakulwong N, Rojborwonwitaya J, Onnom K. Prevalence of colorectal adenomatous polyps in patients undergoing colonosopic examination at rajavithi hospital. Thai J Gastroenterol. 2009;10(1):9–15.Google Scholar
  20. Srichan P, Wasutit Y, Suwanthanma W, Euanorasetr C, Sornmayura P, Puanfoong O, et al. Characteristic of mixed hyperplastic-adenomatous polyps at ramathibodi hospital. Thai J Surg. 2009;30:17–21.Google Scholar
  21. Leggett BA, Devereaux B, Biden K, Searle J, Young J, Jass J. Hyperplastic polyposis: association with colorectal cancer. Am J Surg Pathol. 2001;25(2):177–84.View ArticlePubMedGoogle Scholar
  22. Hyman NH, Anderson P, Blasyk H. Hyperplastic polyposis and the risk of colorectal cancer. Dis Colon Rectum. 2004;47(12):2101–4.View ArticlePubMedGoogle Scholar
  23. SEER Cancer Statistics Review, National Cancer Institute. 1975–2010. http://seer.cancer.gov/archive/csr/1975_2010/. Accessed 20 July 2012.
  24. Young PE, Womeldorph CM. Colonoscopy for colorectal cancer screening. J Cancer. 2013;4(3):217–26.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Paskett ED, Khuri FR. Can we achieve an 80 % screening rate for colorectal cancer by 2018 in the United States? Cancer. 2015.Google Scholar
  26. Allison JE, Tekawa IS, Ransom LJ, Adrain AL. A comparison of fecal occult-blood tests for colorectal-cancer screening. N Engl J Med. 1996;334(3):155–9.View ArticlePubMedGoogle Scholar
  27. Lee JK, Liles EG, Bent S, Levin TR, Corley DA. Accuracy of fecal immunochemical tests for colorectal cancer: systematic review and meta-analysis. Ann Intern Med. 2014;160(3):171.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Giorgi Rossi P, Vicentini M, Sacchettini C, Di Felice E, Caroli S, Ferrari F, et al. Impact of screening program on incidence of colorectal cancer: a cohort study in Italy. Am J Gastroenterol. 2015;110(9):1359–66.View ArticlePubMedGoogle Scholar
  29. Saengow U, Chongsuwiwatvong V, Geater A, Birch S. Preferences and acceptance of colorectal cancer screening in Thailand. Asian Pac J Cancer Prev. 2015;16(6):2269–76.View ArticlePubMedGoogle Scholar
  30. Levin B, Lieberman DA, McFarland B, Andrews KS, Brooks D, Bond J, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology. 2008;134(5):1570–95.View ArticlePubMedGoogle Scholar
  31. Cairns SR, Scholefield JH, Steele RJ, Dunlop MG, Thomas HJ, Evans GD, et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut. 2010;59(5):666–89.View ArticlePubMedGoogle Scholar
  32. Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on colorectal cancer. Gastroenterology. 2012;143(3):844–57.View ArticlePubMedGoogle Scholar
  33. Fairley KJ, Li J, Komar M, Steigerwalt N, Erlich P. Predicting the risk of recurrent adenoma and incident colorectal cancer based on findings of the baseline colonoscopy. Clin Transl Gastroenterol. 2014;5:e64.View ArticlePubMedPubMed CentralGoogle Scholar
  34. Provenzale D, Jasperson K, Ahnen DJ, Aslanian H, Bray T, Cannon JA, et al. Colorectal cancer screening, version 1.2015. J Natl Compr Canc Netw. 2015;13(8):959–68.PubMedGoogle Scholar
  35. Imperiale TF, Glowinski EA, Lin-Cooper C, Larkin GN, Rogge JD, Ransohoff DF. Five-year risk of colorectal neoplasia after negative screening colonoscopy. N Engl J Med. 2008;359(12):1218–24.View ArticlePubMedGoogle Scholar
  36. Leung WK, Lau JY, Suen BY, Wong GL, Chow DK, Lai LH, et al. Repeat-screening colonoscopy 5 years after normal baseline-screening colonoscopy in average-risk Chinese: a prospective study. Am J Gastroenterol. 2009;104(8):2028–34.View ArticlePubMedGoogle Scholar
  37. Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Long-term risk of colorectal cancer after negative colonoscopy. J Clin Oncol. 2011;29(28):3761–7.View ArticlePubMedGoogle Scholar
  38. Chung SJ, Kim YS, Yang SY, Song JH, Kim D, Park MJ, et al. Five-year risk for advanced colorectal neoplasia after initial colonoscopy according to the baseline risk stratification: a prospective study in 2452 asymptomatic Koreans. Gut. 2011;60(11):1537–43.View ArticlePubMedGoogle Scholar
  39. Shergill AK, Conners EE, McQuaid KR, Epstein S, Ryan JC, Shah JN, et al. Protective association of colonoscopy against proximal and distal colon cancer and patterns in interval cancer. Gastrointest Endosc. 2015;82(3):529–37. e1.View ArticlePubMedGoogle Scholar
  40. Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Interval cancers after negative colonoscopy: population-based case–control study. Gut. 2012;61(11):1576–82.View ArticlePubMedGoogle Scholar
  41. Itatsu K, Yokoyama Y, Ebata T, Igami T, Sugawara G, Uehara K, et al. The value of preoperative screening colonoscopies in patients with biliary tract cancer. J Gastroenterol. 2016;51(2):138–43.View ArticlePubMedGoogle Scholar
  42. Robertson DJ, Kaminski MF, Bretthauer M. Effectiveness, training and quality assurance of colonoscopy screening for colorectal cancer. Gut. 2015;64(6):982–90.View ArticlePubMedGoogle Scholar
  43. Ross WA, Thirumurthi S, Lynch PM, Rashid A, Pande M, Shafi MA, et al. Detection rates of premalignant polyps during screening colonoscopy: time to revise quality standards? Gastrointest Endosc. 2015;81(3):567–74.View ArticlePubMedPubMed CentralGoogle Scholar
  44. Hassan C, Gralnek IM. Cost-effectiveness of “full spectrum endoscopy” colonoscopy for colorectal cancer screening. Dig Liver Dis. 2015;47(5):390–4.View ArticlePubMedGoogle Scholar
  45. Singh H, Turner D, Xue L, Targownik LE, Bernstein CN. Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. J Am Med Assoc. 2006;295(20):2366–73.View ArticleGoogle Scholar
  46. Bressler B, Paszat LF, Chen Z, Rothwell DM, Vinden C, Rabeneck L. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology. 2007;132(1):96–102.View ArticlePubMedGoogle Scholar
  47. Lakoff J, Paszat LF, Saskin R, Rabeneck L. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. Clin Gastroenterol Hepatol. 2008;6(10):1117–21. quiz 064.View ArticlePubMedGoogle Scholar
  48. Singh H, Nugent Z, Demers AA, Bernstein CN. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol. 2010;105(12):2588–96.View ArticlePubMedGoogle Scholar
  49. Colorectal Cancer Facts & Figures 2014–2016. American Cancer Society, Atlanta. 2014. http://www.cancer.org/acs/groups/content/documents/document/acspc-042280.pdf. Accessed 8 Oct 2015.

Copyright

© The Author(s). 2016

Advertisement