ORIGINAL ARTICLE

Five-year risk of colorectal neoplasia after normal baselinecolonoscopy in asymptomatic Chinese Mongolianover 50 years of age

Yinglong Huang & Xiaohua Li & Zhaoyang Wang &

Bingzhong Su

Accepted: 29 May 2012 /Published online: 5 July 2012# Springer-Verlag 2012

AbstractBackground After normal colonoscopy, the 5-year risk ofcolorectal neoplasia is sufficiently low for asymptomaticpeople over 50 years of age. In China, the incidence ofcolorectal carcinoma of Mongolian people is higher thanthat of Han people. The aim of this study was to assess the5-year risk of colorectal neoplasia after normal colonoscopyin asymptomatic Chinese Mongolian population.Patients and methods A cohort of asymptomatic ChineseMongolian people (≥50 years old) were recruited and fol-lowed up with colonoscopy 5 years after colonoscopy.Baseline colonoscopy and follow-up colonoscopy findingswere categorized based on the most advanced lesions: noadenoma, nonadvanced adenoma, and advanced adenoma.Five-year risk of colorectal neoplasia in these people wasassessed according to the rates of no baseline adenoma andadvanced adenoma at the end of 5 years.Results A total of 480 of the 538 recruited people under-went follow-up colonoscopy at the end of 5 years. In people

with no baseline adenoma, 27.3 % (82/301) was found tohave any adenoma, and 1.7 % had advanced adenoma atfollow-up colonoscopy. The risk of an advanced adenomadid not differ significantly between people with no ade-noma at baseline and those with nonadvanced adenoma(relative risk (RR), 1.06; 95 % confidence interval (CI),0.19–6.07). Advanced adenoma at baseline colonoscopywas the independent risk factor for advanced adenomarecurrence, compared with no adenoma at baseline (RR, 8.25;95 % CI, 1.90–35.77).Conclusion The risk of advanced adenoma is low 5 yearsafter the normal baseline colonoscopy, even in asymptom-atic Chinese Mongolian population over 50 years of age.

Keywords Colorectal neoplasia . Colonoscopy .

Surveillance . ChineseMongolian

Introduction

Colorectal neoplasia screening and removal with colono-scopy are associated with a significant reduction in the riskof colorectal cancer (CRC) [1–3]. The risk of metachronouscancer still exists after colonoscopy [4–9], so the surveil-lance is evitable for further reducing the incidence of CRC.It is recommended in the current guidelines that a repeatcolonoscopy is necessary: after 3 years for patients with anadvanced adenoma or more than two nonadvanced adeno-mas at baseline colonoscopy, 5 to 10 years for patients withnonadvanced adenomas, and 10 years for patients with nobaseline adenoma [10]. Several prospective studies suggestthat it is safe to repeat colonoscopy at 3 years for patientswith an advanced adenoma or more than two nonadvancedadenomas and 5 years for patients with nonadvanced ade-nomas at baseline colonoscopy [5, 11, 12] . Surveillance at a

Y. Huang (*) : B. Su (*)Department of Gastroenterology, Affiliated Hospital of InnerMongolia Medical College,Huhhot, Inner Mongolia Autonomous Region 010050,People’s Republic of Chinae-mail: hylmr@163.come-mail: shubz@sina.com

X. LiPediatrics Department,Affiliated Hospital of Inner Mongolia Medical College,Huhhot 010050, People’s Republic of China

Z. WangDepartment of General Surgery,Affiliated Hospital of Inner Mongolia Medical College,Huhhot 010050, People’s Republic of China

Int J Colorectal Dis (2012) 27:1651–1656DOI 10.1007/s00384-012-1516-5

10-year interval for patients with no baseline adenoma hasnot been proved by prospective study, expected for severalretrospective observational studies [1, 13–15]. Recently, ithas been reported in two studies that the rate of advancedneoplasia is extremely low, 5 years after normal colono-scopy for asymptomatic people over 50 years of age [16,17], but the incidence of colorectal adenoma and cancervaries in different races and territories. In China, the inci-dence of CRC in Mongolian people is higher than that ofHan people. Whether western surveillance guidelines andpractices can be directly applied to the Chinese Mongolianpopulation needs to be studied. In addition, people over50 years of age are high-risk population of CRC, especiallyfor Chinese Mongolian. Therefore, in order to further en-hance the quality of colonoscopy and develop reasonableguidelines of colonoscopic surveillance for Chinese popula-tion, we designed this program and aimed to assess 5-yearrisk of colorectal neoplasia after normal colonoscopy inasymptomatic Chinese Mongolian over 50 years of age.

Patients and methods

Patients were recruited from the endoscopic center of Gas-troenterology Department at the Affiliated Hospital of InnerMongolia Medical College, Huhhot. The inclusion criteriafor the population are: (1) aged 50 years old or older, (2)without clinical symptoms, and (3) people who underwentthe first completed colonoscopy between January 2003 andAugust 2005, and the findings were normal or with anyadenoma. Patients with familial adenomatous polyposis,inflammatory bowel disease, or personal history of colorec-tal cancer and adenomatous polyps were excluded. Adeno-ma removal was performed after the first colonoscopy forpatients with any adenoma. All eligible patients underwentthe second colonoscopy 6 months after the initial colono-scopy in order to remove missed or incompletely resectedadenomas. The previous two colonoscopy findings wereregarded as baseline findings. The next colonoscopy wasgoing to be performed at the end of 5 years. Patientswith good bowel preparations and having undergonecomplete colonoscopy (colonoscope reach the cecum) atthe initial and follow-up colonoscopy could be recruitedin the present study. The 5-year follow-up was started forpatients with large adenoma removed by piecemeal re-section until the complete resection was confirmed. Theprotocol was approved by the institutional review boardof the Affiliated Hospital of Inner Mongolia MedicalCollege, and written and informed consent was obtainedfrom all eligible patients.

Patients were categorized into three groups based on find-ings at baseline colonoscopy: no adenoma, nonadvanced ad-enoma (tubular adenoma less than 10 mm in diameter), and

advanced adenoma. An advanced adenoma was defined asa tubular adenoma 10 mm or larger in diameter, villous ortubulovillous adenoma, or any adenoma with high-gradedysplasia.

All colonoscopy was performed by experienced colono-scopists using the Olympus CF-240I, CF-Q240I colono-scope. Polyethylene glycol lavage solution was used forbowel preparations. Characteristics of all adenomas detectedat baseline colonoscopy and repeated colonoscopy at theend of 5 years were recorded according to the size, location,shape, and number. The size of adenoma was measured withan opened biopsy forceps (6 mm), and the location wasestimated using anatomic landmarks and insertion distancesof withdrawal. The adenoma shape was identified accordingto the Paris classification [18]. All resected adenomas wereretrieved, and pathological specimens were evaluated by anexperienced gastrointestinal pathologist.

Bleeding complications occurred in 12 patients undergo-ing the adenoma removal. All bleeding complications weretreated successfully with the endoscopic clip or hot biopsytherapy. No perforation or other procedural related compli-cations were observed at either the baseline or follow-upcolonoscopy.

Statistical methods

Descriptive statistics were used to express 5-year risk of anyadenoma and of advanced adenoma. Multiple logisticregressions were used to evaluate the relative risk for thedifferent categories of baseline findings (no adenoma vs.nonadvanced adenoma and no adenoma vs. advanced ade-noma) and to adjust for differences in age, sex, and three ormore adenomas. Meanwhile, we assessed the risk factors ofadenoma recurrence 5 years after polypectomy in patientswith baseline adenomas by multiple logistic regressions.Statistical Package for the Social Sciences (SPSS) 13.0(SPSS Inc., Chicago, IL) was used for all statistical analysis.A two-sided P value less than 0.05 was regarded as statis-tically significant.

Results

Characteristics of eligible patients

Between January of 2003 and August of 2005, a total of 538patients, 50 years of age or older, were recruited according tobaseline colonoscopy findings. Among them, 332 (61.7 %)patients had no adenoma, and 206 (38.3 %) patients had atleast one adenoma (104 patients with nonadvanced adenomasand 102 patients with advanced adenomas). Of those who hadno adenomas on the baseline colonoscopy, 301 (90.7 %)underwent follow-up colonoscopy at the end of 5 years. The

1652 Int J Colorectal Dis (2012) 27:1651–1656

mean ± SD age was 56.5±9.2 years at baseline colonoscopy,and the mean ± SD follow-up interval was 5.1±0.2 years. Theratio of male to female was about 1.5 (199:133). Of those whohad any adenoma on the baseline colonoscopy, 179 patientsreturned for follow-up colonoscopy at 5 years. Ninety (50 %)patients were with nonadvanced adenomas, and 89 patients,with advanced adenomas at baseline colonoscopy. The mean± SD age was 52±6.4 years at baseline colonoscopy, and themean ± SD follow-up interval was 4.9±1.5 years (Table 1).

Of all patients, 31 patients with no adenoma and 22patients with any adenoma at baseline colonoscopy did notreturn for the follow-up colonoscopy at the end of 5 years.Three patients died from lung cancer, and three died fromcardiovascular and cerebrovascular diseases, respectively.Other patients refused reexamination or could not be con-tacted due to changes in the address and telephone numbers.

Colonoscopy findings of patients at the end of 5 years

Rates of nonadvanced and advanced adenomas at 5 years,based on different baseline colonoscopy findings, were shownin Table 2. Among the 480 follow-up patients, 147 (30.6 %)were found to have nonadvanced adenoma, and 30 (6.3 %)had advanced adenoma on the follow-up colonoscopy. Ofthose who had no baseline adenoma, 77 (25.6 %) patientshad nonadvanced adenoma, and 5 (1.7 %) had advancedadenomas. In patients with baseline nonadvanced adenoma,nonadvanced adenomas were found in 34 (37.8 %) patients,and advanced adenomas were found in 4 (4.4 %) patients. Ofthose who had baseline advanced adenomas, nonadvancedand advanced adenomas were found in 36 (40.4 %) and 21

(23.6 %) patients, respectively. One invasive cancer wasfound in one patient. No cancer was found in patients withno baseline and nonadvanced adenomas.

Factors related to any adenoma and advanced adenomaon the 5-year follow-up colonoscopy

Any adenoma were found in 38 of 90 patients (42.2 %), whohad nonadvanced adenoma at baseline, as compared with 82of 301 (27.3 %), who had no adenoma on baseline colono-scopy (relative risk, 1.79; 95 % CI, 1.04–3.10). Advancedadenoma were present in 21 of 89 (23.6 %), who hadadvanced adenoma at baseline, as compared with 5 of 301patients (1.7 %), who had no adenoma on baseline colono-scopy (relative risk, 4.48; 95 % CI, 2.55–7.86). Male sex,age, and three or more adenomas at baseline were indepen-dent risk factors for any adenoma on 5-year follow-upcolonoscopy (Table 3).

The factors associated with the development of advancedadenoma in all patients undergoing 5-year follow-up colo-noscopy were shown in Table 4. Advanced adenoma wereTable 1 Characteristic

of patients with follow-up colonoscopy

Characteristic Number ofpatients (480)

Patients with no adenoma 301

Mean age ± SD (year) 56.5±9.2

Follow-up interval (year) 5.07±0.23

Gender

Men 183

Women 118

Patients with adenoma 179

Mean age±SD (year) 59.2±6.4

Follow-up interval(year)

4.94±1.48

Gender

Men 118

Women 61

Adenoma stage

Nonadvanced adenoma 90

Advanced adenoma 89

Table 2 Rates of any adenoma and advanced adenoma for patientswith different baseline findings at the end of 5 years

Initial colonoscopyfindings

Nonadvancedadenoma

Advancedadenoma

n (%) n (%)

No neoplasia (301) 77 (25.6) 5 (1.7)

Any adenoma (179) 70 (39.1) 25 (14.0)

Nonadvanced adenoma (90) 34 (37.8) 4 (4.4)

Advanced adenoma (89) 36 (40.4) 21 (23.6)a

Total (480) 147 (30.6) 30 (6.3)

a Including one invasive cancer

Table 3 Risk of any adenomas at the end of 5 years, according tobaseline findings

Baseline findings Any adenomas(%)

Relative risk(95 % CI)

P value

No baseline adenoma(301)

82 (27.3)

Nonadvanced adenoma(90)

38 (42.2) 1.79 (1.04–3.10) 0.036

Advanced adenoma (89) 57 (64.0) 4.48 (2.55–7.86) <0.001

Age (year)

50–60 (304) 88 (28.9)

>60 (176) 89 (50.6) 2.90 (1.90–4.44) <0.001

Sex

Men (304) 126 (41.4) 1.60 (1.04–2.47) 0.034

Women (176) 51 (28.9)

Three or more adenoma(39)

29 (74.3) 1.70 (1.12–2.58) 0.013

Int J Colorectal Dis (2012) 27:1651–1656 1653

found in 21 of 89 patients (23.6 %), who had advancedadenoma at baseline, as compared with 5 of 301 (1.7 %),who had no adenoma on baseline colonoscopy (relative risk,14.11; 95 % CI, 4.51–44.12). Male sex, age, and numberof adenoma at baseline were also independent risk factorsfor any adenoma on 5-year follow-up colonoscopy;whereas, nonadvanced adenoma at baseline was not a riskfactor for advanced adenoma on 5-year follow-up colono-scopy compared with no baseline adenoma (relative risk,1.85; 95 % CI, 0.43–7.89).

As for patients with baseline adenomas, men older than60 years, three more adenomas were also risk factors ofadvanced and any adenomas recurrence 5 years afterpolypectomy, as were for piecemeal resection. The shapeand location of the baseline adenoma were not related tothe adenoma recurrence (Table 5). In addition, the numberof recurrent adenoma located in the right colon (49.4 %)was similar to that of baseline adenoma located in theright colon (43.1 %).

Discussion

This study provided valuable information on the 5-year riskof colorectal neoplasia among patients with no baselineadenoma or with baseline adenoma, who were asymptom-atic Chinese Mongolian 50 years of age or older. This cohortincluded 301 patients with no baseline adenoma, who hadlow rate (1.7 %) of advanced adenomas on the 5-yearfollow-up colonoscopy, and no cancer was found. However,any adenoma was found in nearly 27.3 % of these patients.These results provide support for the follow-up colonoscopyafter an interval of at least 5 years for asymptomatic ChineseMongolian with no baseline adenoma. It is suggested in

Imperiale's [16] study that the risk of advanced neoplasiain American screening population without baseline polyps is1.3 %. In Leung's [17] prospective study, the rate of ad-vanced adenomas after normal baseline colonoscopy wasonly 1.4 % for asymptomatic average-risk Chinese subjects(aged 55–75 years). In the present study, asymptomaticChinese Mongolian populations over 50 years old wereeligible subjects, and the rate of advanced adenomas wassimilar to those in previous two studies. It is revealed fromthese results that it is safe for asymptomatic Chinese Mon-golian over 50 years old to be reexamined 5 years after thenormal baseline colonoscopy.

It is reported in two studies that longer surveillanceinterval is necessary for subjects with no baseline adenoma.One was a retrospective cohort study in which the standard-ized incidence ratios (SIR) of colorectal cancer after normalbaseline colonoscopy were calculated in 32,203 subjects.SIRs were 0.66 at 1 year, 0.55 at 5 years, and 0.28 at10 years. The results suggest that the risk of developingcolorectal cancer remains decreased for more than 10 years,following the performance of normal colonoscopy [19]. Inanother case–control study, the risk of colorectal cancer wascompared between subjects with previous normal colono-scopy and those without previous colonoscopy. It is foundthat subjects with normal baseline colonoscopy are at verylow risk of developing colorectal cancer and might not needto undergo the repeat colonoscopy for 20 years [20], butthese two studies included subjects whose ages wereyounger than 50 years old, which might result in theextension of surveillance interval, as compared withsubjects in the present study.

In the present study, the other two surveillance popula-tions were included in the subjects except for those with nobaseline adenoma or with nonadvanced and advanced ade-nomas on baseline colonoscopy. On 5-year surveillancecolonoscopy, no baseline adenoma and advanced adenomawas found in 42.2 and 4.4 % of subjects with baselinenonadvanced adenoma, and 64 and 23.6 % of subjects withbaseline advanced adenoma, respectively. These resultswere similar to previous studies, in which the follow-upcolonoscopy was performed within 4 to 5.5 years, withreported any adenoma in 31.6–45.7 %, and advanced ade-noma in 4.6–4.9 % in subjects with baseline nonadvancedadenoma; whereas, in subjects with baseline advanced ade-noma, any adenoma was found in 39.5–62.1 %, and ad-vanced adenoma was found in 7.0–20.7 % [5, 12, 17, 21,22]. These results suggested that the 5-year risk of adenomaand advanced adenoma recurrences after polypectomy inasymptomatic Chinese Mongolian were similar to those ofasymptomatic subjects.

As have been indicated in previous studies, age, sex, andthree or more adenomas at the index colonoscopy were inde-pendent risk factors of no baseline adenoma and advanced

Table 4 Risk of advanced adenomas at the end of 5 years according tobaseline findings

Baseline findings Advancedadenomas (%)

Relative risk(95 % CI)

P value

No baselineadenoma (301)

5 (1.7)

Nonadvancedadenoma (90)

4 (4.4) 1.85 (0.43–7.89 ) 0.405

Advancedadenoma (89)

21 (23.6) 14.11 (4.51–44.12 ) <0.001

Age (year)

50–60 (304) 11 (3.6)

>60 (176) 19 (10.8) 3.44 (1.42–8.32) 0.006

Sex

Men (304) 25 (8.2) 3.06 (1.04–9.00) 0.043

Women (176) 5 (2.8)

Three or moreadenoma (39)

11 (28.2) 1.92 (1.16–3.16) 0.011

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adenoma recurrence [10, 12, 23–25]; our study also confirmedthis result. Meanwhile, we found that the 5-year follow-upcolonoscopy findings were significantly different in subjectswith different baseline colonoscopy findings. As comparedwith the baseline normal colonoscopic finding, nonadvancedand advanced adenomas on baseline colonoscopy were riskfactors of adenoma recurrence, and advanced adenoma onbaseline colonoscopy was an independent risk factor of ad-vanced adenoma at 5 years. These results add evidences forthe current guidelines of surveillance after polypectomy thatpatients with one or two nonadvanced adenomas should havesurveillance colonoscopy in 5 to 10 years (10). In subjectswith normal baseline colonoscopy, however, the recommen-dation of guidelines suggested that the interval before thesubsequent colonoscopy should be 10 years. At present, nodata of prospective study confirmed this recommendation, andonly three studies documented that it was safe for asymptom-atic subjects with no baseline adenoma to be followed up atthe end of 5 years after polypectomy. Our study provided thedata of the 5-year follow-up in asymptomatic Chinese Mon-golian over 50 years old, which complemented the suggestionthat the 5-year follow-up interval is safe for subjects with nobaseline adenoma. In addition, in our study, the rate of ade-noma recurrence in patients, who received piecemeal resec-tion at initial colonoscopy, was higher than that in patientsreceived en-bloc resection because bigger adenoma needed tobe resected by piecemeal usually was an advanced adenoma,

which was the most important risk factor for adenoma recur-rence. In our study, the location of recurrent adenoma wassimilar to that of baseline adenoma. Prior studies showed thatrecurrent adenoma was easily present on the right colon. Thisresult differed from that of prior studies, which might beassociated with different races.

Our study has several limitations. First, the sample sizewas small, which might bring about biased risk estimates.However, the follow-up information was obtained from89.2 % of all subjects in our study, which we assume couldpartially overcome this small sample size. Second, the pop-ulation in our study was mainly aged from 50 to 70 yearsold. There were few aged 70 years old or older. The distri-bution of ages has limited the generalizability of our find-ings. Third, in our study, we did not assess the risk ofcolorectal neoplasia after the normal baseline colonoscopyor polypectomy based on stratified patient-specific features,such as the family history of colorectal cancer or adenoma,diet, physical activity, smoking status, body mass index, andso on. These factors may affect the progression of adenomaformation and development [22, 26–28].

In conclusion, the risk of advanced adenoma 5 years after anormal baseline colonoscopy was low even if the follow-uppopulation was asymptomatic Chinese Mongolian over50 years of age. Follow-up interval of colonoscopy after thenormal baseline colonoscopy or polypectomy should be de-termined based on stratified baseline colonoscopic findings.

Table 5 Risk factors of adenoma recurrence at the end of 5 years in patients with baseline adenomas

Baseline findings Any adenomas (%) RR (95 % CI) P value Advanced adenomas (%) RR (95 % CI) P value

Type

Nonadvanced adenoma (90) 38 (42.2) 1 4 (4.4) 1

Advanced adenoma (89) 57 (64.0) 1.29 (1.02–1.76) 0.028 21 (23.6) 2.64 (1.34–4.72) 0.014

Age (year)

50–60 (121) 51 (42.15) 1 9 (7.4) 1

>60 (58) 44 (75.9) 2.86 (2.13–3.75) <0.001 16 (27.6) 3.91 (2.48–7.52) <0.001

Sex

Women (60) 26 (43.3) 1 4 (6.7) 1

Men (119) 69 (58.0) 1.15 (1.02–1.63) 0.041 21 (17.6) 2.18 (1.13–3.06) 0.003

Number

Two or less adenoma (140) 64 (45.7) 1 12 (8.6) 1

Three or more adenoma (39) 31 (79.5) 1.75 (1.29–2.34) <0.001 13 (33.3) 1.24 (1.22–5.10) 0.018

Morphology

Pedunculated (125) 67 (53.6) 1 20 (13.8) 1

Flat (54) 28 (51.9) 1.03 (0.81–1.27) 0.830 5 (14.7) 1.28 (0.95–2.26) 0.065

Location

Any proximal (77) 38 (49.4) 1 10 (13.5) 1

Distal only (102) 57 (55.9) 1.05 (0.84–1.29) 0.655 15 (14.3) 0.76 (0.45–1.24) 0.359

Resection method

En-bloc (158) 79 (50.0) 1 19 (12.0) 1

Piece meal resection (21) 16 (76.2) 1.39 (1.05–2.12) 0.034 6 (28.6) 2.45 (1.09–4.02) 0.021

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