結(jié)腸鏡檢查腺瘤檢出率的影響因素

黃敏丹(綜述)，占 強(qiáng)(審校)

(南京醫(yī)科大學(xué)附屬無錫人民醫(yī)院消化內(nèi)科，江蘇 無錫 214000)

結(jié)直腸癌是人類高發(fā)惡性腫瘤，在全球惡性腫瘤發(fā)病率中已上升至第3位，其病死率居惡性腫瘤死因的第二位。我國結(jié)直腸癌發(fā)病率也逐年增高，已躍居至第3～5位，其病死率已位于惡性腫瘤病死率的第5位。目前研究均表明結(jié)腸鏡檢查是篩查和監(jiān)測(cè)結(jié)直腸癌的金標(biāo)準(zhǔn)。通過結(jié)腸鏡篩查使得結(jié)直腸癌的總發(fā)生率降低了近80%。結(jié)直腸腺瘤是結(jié)直腸癌最主要的癌前病變，Kaminski等[1]通過多變量Cox風(fēng)險(xiǎn)回歸模型，發(fā)現(xiàn)內(nèi)鏡醫(yī)師腺瘤檢出率(adenoma detection rates,ADR)與結(jié)直腸間歇期癌發(fā)生的危險(xiǎn)性顯著相關(guān)，ADR降低間歇期癌發(fā)生明顯升高，說明ADR是結(jié)腸鏡篩查后發(fā)生結(jié)直腸間歇期癌的一個(gè)獨(dú)立危險(xiǎn)因子?，F(xiàn)將結(jié)腸鏡檢查ADR的影響因素進(jìn)行綜述。

1 腸道準(zhǔn)備情況

良好的腸道準(zhǔn)備質(zhì)量是完成全結(jié)腸檢查和黏膜觀察的前提。腸道準(zhǔn)備差將增加進(jìn)鏡難度、延長進(jìn)鏡時(shí)間、縮短退鏡時(shí)間、降低腺瘤檢出、增加腺瘤漏診、增加結(jié)腸鏡操作風(fēng)險(xiǎn)、縮短患者復(fù)查結(jié)腸鏡的間期和增加醫(yī)療費(fèi)用等[2]。Thomas-Gibson等[3]發(fā)現(xiàn)，若腸道準(zhǔn)備充分，ADR明顯較高，并發(fā)現(xiàn)ADR較高的內(nèi)鏡醫(yī)師可能對(duì)腸道準(zhǔn)備質(zhì)量的要求更高，接受結(jié)腸鏡培訓(xùn)的內(nèi)鏡醫(yī)師對(duì)腸道準(zhǔn)備進(jìn)行正確判斷，以及不接受對(duì)腸道準(zhǔn)備不佳患者行結(jié)腸鏡檢查有利于提高ADR。重復(fù)結(jié)腸鏡檢查可以發(fā)現(xiàn)腸道準(zhǔn)備不充分的初次結(jié)腸鏡檢查未發(fā)現(xiàn)的腺瘤以及高危病變，也說明了腸道準(zhǔn)備不充分影響ADR[4]。一項(xiàng)歐洲多中心研究顯示，在年老患者、住院患者和合并多種疾病的患者腸道清潔準(zhǔn)備的質(zhì)量相對(duì)更差,其中結(jié)腸癌的檢出與腸道清潔程度無關(guān)，但是任何大小的息肉檢出都與腸道清潔的程度有關(guān)，腸道準(zhǔn)備質(zhì)量提高，息肉檢出率也隨之提高[5]。Sherer等[6]研究指出，腸道準(zhǔn)備質(zhì)量是否充分對(duì)微小腺瘤(直徑≤5 mm)和高危腺瘤的檢出存在差異，兩者微小ADR的比值為0.57，高危腺瘤的檢出率分別為3.3%、5.0%，腸道準(zhǔn)備充分有利于腺瘤的檢出。多因素分析表明，腸道準(zhǔn)備情況與息肉檢出有關(guān)(比值比=1.21)，尤其是直徑≤9 mm的息肉，但是對(duì)直徑>9 mm息肉的檢出可能影響不大，不過這項(xiàng)研究需要前瞻的研究進(jìn)一步證實(shí)[7]。此外，遵守腸道準(zhǔn)備操作指南、腸道清潔劑服用的時(shí)機(jī)以及用藥之后等待結(jié)腸鏡檢查的時(shí)間被認(rèn)為影響腸道清潔質(zhì)量[8]。由于腸道準(zhǔn)備藥物劑量大，影響患者的依從性，近期有研究提出分劑量的腸道準(zhǔn)備對(duì)腸道準(zhǔn)備質(zhì)量和患者耐受都有顯著提高，且顯著提高ADR[9]。

2 退鏡時(shí)間

內(nèi)鏡醫(yī)師在退鏡過程中完成對(duì)結(jié)腸的觀察，因此充分的退鏡時(shí)間能保證對(duì)結(jié)腸黏膜的仔細(xì)觀察。結(jié)腸鏡檢查平均退鏡時(shí)間與ADR存在相關(guān)性。Millan等[10]研究發(fā)現(xiàn)，對(duì)于有經(jīng)驗(yàn)的內(nèi)鏡醫(yī)師，其盲腸到達(dá)率差異不大，但醫(yī)師之間的ADR相差很大，從14.2%～27.4%不等，主要原因是醫(yī)師之間退鏡時(shí)間差異大，退鏡時(shí)間增加，ADR提高。Benson等[11]亦發(fā)現(xiàn)退鏡時(shí)間的長短與ADR呈正相關(guān)，并且發(fā)現(xiàn)進(jìn)境時(shí)間與退鏡時(shí)間的比值與ADR呈負(fù)相關(guān)，比值<1者ADR較比值≥1者高。內(nèi)鏡醫(yī)師平均退鏡時(shí)間≥6 min者較<6 min者ADR(包括高危腺瘤的檢出率)更高，兩者間有顯著差異，而退鏡時(shí)間在6～11 min之間時(shí)，ADR高低與退鏡時(shí)間的長短無關(guān)[12-13]。Lee等[14]研究發(fā)現(xiàn)，退鏡時(shí)間延長主要是與小腺瘤和右半結(jié)腸腺瘤的檢出增加相關(guān)，然而退鏡時(shí)間>10 min ADR的提高不明顯，平均退鏡時(shí)間>6 min則與高危腺瘤的檢出無相關(guān)性。2002年美國大腸癌篩查學(xué)會(huì)意見要求篩查結(jié)腸鏡退鏡時(shí)間≥6 min。但是，也有人認(rèn)為這種規(guī)定很大程度是建立在專家觀點(diǎn)的基礎(chǔ)上，而且對(duì)于腺瘤的一些特殊觀察手段沒有評(píng)估，因此認(rèn)為定義最短退鏡時(shí)間為6 min可能不夠[11]。有人認(rèn)為除外活檢和息肉切除的時(shí)間，退鏡時(shí)間至少應(yīng)有6～10 min[15]。Simmons等[16]認(rèn)為，退鏡時(shí)間至少應(yīng)該為7 min才能保證較高的息肉檢出率，<7 min和≥7 min的息肉檢出率分別為76%、44%。也有研究發(fā)現(xiàn)，在要求內(nèi)鏡醫(yī)師退鏡時(shí)間≥8 min后，總體ADR和高危腺瘤ADR均顯著提高[17]。但對(duì)于經(jīng)驗(yàn)不足的培訓(xùn)醫(yī)師，其退鏡時(shí)間延長至10 min，ADR才明顯提高，退鏡時(shí)間≥10 min與<10 min的ADR分別為32.3%、9.5%[18]。

3 醫(yī)師的經(jīng)驗(yàn)及專業(yè)背景

醫(yī)師是結(jié)腸鏡檢查的操作者，是控制結(jié)腸鏡檢查質(zhì)量的重要因素。不同結(jié)腸鏡檢查醫(yī)師之間ADR存在很大差異。在各國結(jié)腸鏡篩查質(zhì)量指南，即使對(duì)有經(jīng)驗(yàn)的醫(yī)師均要求每年保證200～300例篩查結(jié)腸鏡檢查，以確保醫(yī)師行篩查結(jié)腸鏡的質(zhì)量[13]。也有研究認(rèn)為醫(yī)師的操作經(jīng)驗(yàn)，在達(dá)到一定熟練程度后可能對(duì)結(jié)腸鏡檢查質(zhì)量的影響不大，把醫(yī)師經(jīng)驗(yàn)分為<5年、5～10年、>10年，他們之間的ADR沒有顯著性差異[1]。Adler等[13]認(rèn)為醫(yī)師之間ADR的差異主要受醫(yī)師的個(gè)人因素(如繼續(xù)醫(yī)學(xué)教育等)和設(shè)備因素影響，其他引起差異大的原因可能和醫(yī)師的技術(shù)水平有關(guān)，但這部分因素在目前的研究中無法評(píng)價(jià)。一項(xiàng)回顧性調(diào)查顯示，接受內(nèi)鏡培訓(xùn)醫(yī)師的培訓(xùn)時(shí)間不同，ADR差異大，培訓(xùn)時(shí)間越長，ADR越高[19]。有經(jīng)驗(yàn)醫(yī)師與內(nèi)鏡培訓(xùn)醫(yī)師相比，內(nèi)鏡培訓(xùn)醫(yī)師的ADR明顯偏低，包括對(duì)小腺瘤的檢出率也較低[20]。但在上級(jí)醫(yī)師監(jiān)督下，內(nèi)鏡培訓(xùn)醫(yī)師的ADR較高，尤其是小腺瘤(<5 mm)的檢出率(有上級(jí)醫(yī)師監(jiān)督的ADR為25%；無上級(jí)醫(yī)師監(jiān)督的ADR為17%)[21]。另有研究指出，有上級(jí)醫(yī)師在旁指導(dǎo)內(nèi)鏡培訓(xùn)醫(yī)師的ADR比單獨(dú)由上級(jí)醫(yī)師完成的ADR高(OR=1.32)[19]。也有研究發(fā)現(xiàn)，對(duì)于有經(jīng)驗(yàn)的醫(yī)師，培訓(xùn)醫(yī)師的參與對(duì)ADR影響不是很大[22]。Sanduleanu等[23]認(rèn)為胃腸專業(yè)醫(yī)師與胃腸專業(yè)培訓(xùn)醫(yī)師相比，兩者ADR比較沒有顯著差異，病變的檢出主要依賴于醫(yī)師的臨床意識(shí)。此外，內(nèi)鏡醫(yī)師的專業(yè)背景亦是影響結(jié)腸鏡檢查質(zhì)量的重要因素，其對(duì)ADR的影響比患者年齡和性別因素影響更大[24]。有研究指出，消化專業(yè)結(jié)腸鏡醫(yī)師比非消化專業(yè)結(jié)腸鏡醫(yī)師的ADR更高[25]。

4 輔助觀察及成像方法

除了提高傳統(tǒng)的結(jié)腸鏡檢查方法，應(yīng)用一些輔助手段，可能也有助于提高腺瘤的檢出率。高分辨率染色內(nèi)鏡檢查較傳統(tǒng)結(jié)腸鏡檢查更易發(fā)現(xiàn)扁平腺瘤和小腺瘤[26]。Pohl等[27]發(fā)現(xiàn)染色內(nèi)鏡檢查較常規(guī)結(jié)腸鏡檢查ADR增加，特別是扁平腺瘤和鋸齒狀腺瘤的檢出率增加，但對(duì)高危腺瘤的檢出率影響不大。也有研究指出，雖然染色內(nèi)鏡對(duì)總體ADR沒有影響，但能夠顯著提高扁平小腺瘤(<5 mm)的檢出率[28]。有研究包括薈萃分析認(rèn)為與常規(guī)腸鏡相比染色內(nèi)鏡并沒有提高ADR[29]。在結(jié)腸鏡的前端安裝透明帽，有助于折疊和皺襞口側(cè)部位的結(jié)腸黏膜充分展現(xiàn)觀察，因此使用透明帽輔助觀察，ADR(49.3%)要顯著高于常規(guī)結(jié)腸鏡檢查(39.1%)[30]。Horiuchi等[31]也證實(shí)使用透明帽與常規(guī)結(jié)腸鏡檢查相比，腺瘤檢出的數(shù)目明顯增多。但也有研究指出使用透明帽可以縮短盲腸到達(dá)的時(shí)間，尤其是可以縮短無經(jīng)驗(yàn)內(nèi)鏡醫(yī)師的結(jié)腸鏡檢查時(shí)間，降低腸鏡檢查期間患者的不適感，但不增加ADR[32-33]。反復(fù)腸道沖洗吸引可以清潔腸道廢物，使得總體ADR提高8%，近端結(jié)腸的ADR提高11%，近端結(jié)腸<10 mm的腺瘤的檢出率提高12%[34]。由于腸道沖洗會(huì)延長檢查時(shí)間，Yen等[35]便將腸道沖洗吸引與透明帽結(jié)合運(yùn)用，發(fā)現(xiàn)不僅可以縮短檢查時(shí)間，而且可以提高ADR。還有研究在結(jié)腸鏡檢查時(shí)應(yīng)用升結(jié)腸和直腸反轉(zhuǎn)技術(shù)，認(rèn)為能夠觀察到直視下觀察不到的黏膜，從而提高腺瘤檢出[36-37]。然而，輔助手段對(duì)結(jié)腸鏡檢查質(zhì)量的影響也存在爭(zhēng)議，一些研究包括隨機(jī)對(duì)照研究認(rèn)為這些方法作用均有限，與常規(guī)結(jié)腸鏡檢查相比，ADR并沒有顯著差異[38]。

5 盲腸到達(dá)情況

結(jié)腸鏡檢查時(shí)只有到達(dá)回盲部才能保證整個(gè)結(jié)腸的觀察，否則必定會(huì)因?yàn)橐徊糠帜c道黏膜未觀察，而減少腺瘤的檢出。未能完成全結(jié)腸檢查的乙狀結(jié)腸鏡篩查ADR為8.6%～15.9%，明顯低于全結(jié)腸檢查的ADR，也就意味著將出現(xiàn)很大的漏診量[39]。因此，盲腸到達(dá)是成功完成全結(jié)腸鏡檢查最基本和重要的要求[1]。20世紀(jì)90年代就有報(bào)道指出，有經(jīng)驗(yàn)內(nèi)鏡醫(yī)師盲腸插管率>90%[40]。目前結(jié)腸鏡篩查盲腸到達(dá)率要求≥95%[41]。結(jié)腸鏡檢查質(zhì)量的保證僅僅依靠盲腸到達(dá)是遠(yuǎn)遠(yuǎn)不足的，因?yàn)槠洳荒鼙ＷC結(jié)腸黏膜的觀察質(zhì)量[10]。

除以上相關(guān)技術(shù)因素影響結(jié)腸鏡檢查質(zhì)量外，結(jié)腸鏡操作單位(醫(yī)院)的規(guī)?；蛩讲町悓?duì)ADR也有顯著影響，de Jonge等[42]選擇了荷蘭的12家不同規(guī)模及水平的醫(yī)院(6家教學(xué)醫(yī)院和6家綜合性醫(yī)院)，發(fā)現(xiàn)其ADR在13%～31.5%之間。此外，一些客觀因素也影響腺瘤檢出。不同直徑腺瘤其漏檢率有明顯不同，≤5 mm的漏檢率為20%～30%，6～9 mm的漏檢率為10%～15%，≥10 mm的漏檢率為2%～12%，間接說明腺瘤直徑越大，越容易檢出[43]。高危腺瘤檢出的影響因素包括高齡、男性患者、第1次腸鏡檢查發(fā)現(xiàn)高危腺瘤以及患有高危腺瘤的病史等[44]。有研究指出，男性患者ADR顯著高于女性(25% vs 15%)[45]。也有研究發(fā)現(xiàn)女性患者與男性患者ADR的比例為0.56[6]。隨著年齡的增長，ADR升高，如30歲的患者ADR為14.6%，而70歲將達(dá)到35.2%[24]?；颊叩慕Y(jié)腸癌家族史，吸煙史也會(huì)影響ADR[46]。結(jié)腸鏡檢查ADR與檢查的時(shí)間也有相關(guān)性，上午比下午ADR高(29.3% vs 25.3%)，而其原因有待進(jìn)一步研究[47]。

6 小 結(jié)

通過結(jié)腸鏡檢查，左半結(jié)腸癌的發(fā)生率顯著降低，右半結(jié)腸癌發(fā)生率降低50%，不同年齡段和臨床分期結(jié)直腸癌的發(fā)病均顯著降低。目前研究發(fā)現(xiàn)，結(jié)腸鏡檢查ADR的影響因素主要有腸道準(zhǔn)備情況、退鏡時(shí)間、檢查醫(yī)師的經(jīng)驗(yàn)和專業(yè)背景、結(jié)腸鏡檢查過程中的輔助觀察和成像方法、盲腸的到達(dá)情況、結(jié)腸鏡操作單位的規(guī)?；蛩?、腺瘤的特征等，但是大多研究都是針對(duì)上述因素之一的單因素研究，而未考慮因素與因素之間存在的相互影響，可以針對(duì)上述所有因素進(jìn)行多因素研究，進(jìn)一步分析結(jié)腸鏡檢查腺瘤檢出的獨(dú)立影響因素。

[1] Kaminski MF,Regula J,Kraszewska E,etal.Quality indicators for colonoscopy and the risk of interval cancer[J].N Engl J Med,2010,362(19):1795-1803.

[2] Calderwood AH,Lai EJ,Fix OK,etal.An endoscopist-blinded,randomized,controlled trial of a simple visual aid to improve bowel preparation for screening colonoscopy[J].Gastrointest Endosc,2011,73(2):307-314.

[3] Thomas-Gibson S,Rogers P,Cooper S,etal.Judgement of the quality of bowel preparation at screening flexible sigmoidoscopy is associated with variability in adenoma detection rates[J].Endoscopy,2006,38(5):456-460.

[4] Chokshi RV,Hovis CE,Hollander T,etal.Prevalence of missed adenomas in patients with inadequate bowel preparation on screening colonoscopy[J].Gastrointest Endosc,2012,75(6):1197-1203.

[5] Froehlich F,Wietlisbach V,Gonvers JJ,etal.Impact of colonic cleansing on quality and diagnostic yield of colonoscopy:the European Panel of Appropriateness of Gastrointestinal Endoscopy European multicenter study[J].Gastrointest Endosc,2005,61(3):378-384.

[6] Sherer EA,Imler TD,Imperiale TF.The effect of colonoscopy preparation quality on adenoma detection rates[J].Gastrointest Endosc,2012,75(3):545-553.

[7] Harewood GC,Sharma VK,de Garmo P.Impact of colonoscopy preparation quality on detection of suspected colonic neoplasia[J].Gastrointest Endosc,2003,58(1):76-79.

[8] Romero RV,Mahadeva S.Factors influencing quality of bowel preparation for colonoscopy[J].World J Gastrointest Endosc,2013,5(2):39-46.

[9] Gurudu SR,Ramirez FC,Harrison ME,etal.Increased adenoma detection rate with system-wide implementation of a split-dose preparation for colonoscopy[J].Gastrointest Endosc,2012,76(3):603-608.

[10] Millan MS,Gross P,Manilich E,etal.Adenoma detection rate:the real indicator of quality in colonoscopy[J].Dis Colon Rectum,2008,51(8):1217-1220.

[11] Benson ME,Reichelderfer M,Said A,etal.Variation in colonoscopic technique and adenoma detection rates at an academic gastroenterology unit[J].Dig Dis Sci,2010,55(1):166-171.

[12] Rex DK,Bond JH,Winawer S,etal.Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy:recommendations of the U.S.Multi-Society Task Force on Colorectal Cancer[J].Am J Gastroenterol,2002,97(6):1296-1308.

[13] Adler A,Wegscheider K,Lieberman D,etal.Factors determining the quality of screening colonoscopy:a prospective study on adenoma detection rates,from 12,134 examinations(Berlin colonoscopy project 3,BECOP-3)[J].Gut,2013,62(2):236-241.

[14] Lee TJ,Blanks RG,Rees CJ,etal.Longer mean colonoscopy withdrawal time is associated with increased adenoma detection:evidence from the Bowel Cancer Screening Programme in England[J].Endoscopy,2013,45(1):20-26.

[15] Cutler CS,Rex DK,Hawes RH,etal.Does routine intravenous glucagon administration facilitate colonoscopy? A randomized trial[J].Gastrointest Endosc,1995,42(4):346-350.

[16] Simmons DT,Harewood GC,Baron TH,etal.Impact of endoscopist withdrawal speed on polyp yield:implications for optimal colonoscopy withdrawal time[J].Aliment Pharmacol Ther,2006,24(6):965-971.

[17] Barclay RL,Vicari JJ,Greenlaw RL.Effect of a time-dependent colonoscopic withdrawal protocol on adenoma detection during screening colonoscopy[J].Clin Gastroenterol Hepatol,2008,6(10):1091-1098.

[18] Gromski MA,Miller CA,Lee SH,etal.Trainees′ adenoma detection rate is higher if ≥10 minutes is spent on withdrawal during colonoscopy[J].Surg Endosc,2012,26(5):1337-1342.

[19] Peters SL,Hasan AG,Jacobson NB,etal.Level of fellowship training increases adenoma detection rates[J].Clin Gastroenterol Hepatol,2010,8(5):439-442.

[20] Nishizawa T,Suzuki H,Takahashi M,etal.Trainee participation during colonoscopy adversely affects polyp and adenoma detection rates[J].Digestion,2011,84(3):245-246.

[21] Buchner AM,Shahid MW,Heckman MG,etal.Trainee participation is associated with increased small adenoma detection[J].Gastrointest Endosc,2011,73(6):1223-1231.

[22] Eckardt AJ,Swales C,Bhattacharya K,etal.Does trainee participation during colonoscopy affect adenoma detection rates?[J].Dis Colon Rectum,2009,52(7):1337-1344.

[23] Sanduleanu S,Rondagh EJ,Masclee AA.Development of expertise in the detection and classification of non-polypoid colorectal neoplasia:Experience-based data at an academic GI unit[J].Gastrointest Endosc Clin N Am,2010,20(3):449-460.

[24] Chen SC,Rex DK.Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy[J].Am J Gastroenterol,2007,102(4):856-861.

[25] Ko CW,Dominitz JA,Green P,etal.Specialty differences in polyp detection,removal,and biopsy during colonoscopy[J].Am J Med,2010,123(6):528-535.

[26] Lecomte T,Cellier C,Meatchi T,etal.Chromoendoscopic colonoscopy for detecting preneoplastic lesions in hereditary nonpolyposis colorectal cancer syndrome[J].Clin Gastroenterol Hepatol,2005,3(9):897-902.

[27] Pohl J,Schneider A,Vogell H,etal.Pancolonic chromoendoscopy with indigo carmine versus standard colonoscopy for detection of neoplastic lesions:a randomised two-centre trial[J].Gut,2011,60(4):485-490.

[28] Cha JM,Lee JI,Joo KR,etal.A prospective randomized study on computed virtual chromoendoscopy versus conventional colonoscopy for the detection of small colorectal adenomas[J].Dig Dis Sci,2010,55(8):2357-2364.

[29] Dinesen L,Chua TJ,Kaffes AJ.Meta-analysis of narrow-band imaging versus conventional colonoscopy for adenoma detection[J].Gastrointest Endosc,2012,75(3):604-611.

[30] Kondo S,Yamaji Y,Watabe H,etal.A randomized controlled trial evaluating the usefulness of a transparent hood attached to the tip of the colonoscope[J].Am J Gastroenterol,2007,102(1):75-81.

[31] Horiuchi A,Nakayama Y.Improved colorectal adenoma detection with a transparent retractable extension device[J].Am J Gastroenterol,2008,103(2):341-345.

[32] de Wijkerslooth TR,Stoop EM,Bossuyt PM,etal.Adenoma detection with cap-assisted colonoscopy versus regular colonoscopy:a randomised controlled trial[J].Gut,2012,61(10):1426-1434.

[33] Dai J,Feng N,Lu H,etal.Transparent cap improves patients′ tolerance of colonoscopy and shortens examination time by inexperienced endoscopists[J].J Dig Dis,2010,11(6):364-368.

[34] Leung F,Harker J,Leung J,etal.Removal of infused water predominantly during insertion(water exchange) is consistently associated with an increase in adenoma detection rate-review of data in randomized controlled trials(RCTs) of water-related methods[J].J Interv Gastroenterol,2011,1(3):121-126.

[35] Yen AW,Leung JW,Leung FW.A novel method with significant impact on adenoma detection:combined water-exchange and cap-assisted colonoscopy[J].Gastrointest Endosc,2013,77(6):944-948.

[36] Hewett DG,Rex DK.Miss rate of right-sided colon examination during colonoscopy defined by retroflexion:an observational study[J].Gastrointest Endosc,2011,74(2):246-252.

[37] Saad A,Rex DK.Routine rectal retroflexion during colonoscopy has a low yield for neoplasia[J].World J Gastroenterol,2008,14(42):6503-6505.

[38] Tee HP,Corte C,Al-Ghamdi H,etal.Prospective randomized controlled trial evaluating cap-assisted colonoscopy vs standard colonoscopy[J].World J Gastroenterol,2010,16(31):3905-3910.

[39] Atkin W,Rogers P,Cardwell C,etal.Wide variation in adenoma detection rates at screening flexible sigmoidoscopy[J].Gastroenterology,2004,126(5):1247-1256.

[40] Marshall JB,Barthel JS.The frequency of total colonoscopy and terminal ileal intubation in the 1990s[J].Gastrointest Endosc,1993,39(4):518-520.

[41] Lee TJ,Rutter MD,Blanks RG,etal.Colonoscopy quality measures:experience from the NHS Bowel Cancer Screening Programme[J].Gut,2012,61(7):1050-1057.

[42] de Jonge V,Sint Nicolaas J,Cahen DL,etal.Quality evaluation of colonoscopy reporting and colonoscopy performance in daily clinical practice[J].Gastrointest Endosc,2012,75(1):98-106.

[43] Pohl H,Robertson DJ.Colorectal cancers detected after colonoscopy frequently result from missed lesions[J].Clin Gastroenterol Hepatol,2010,8(10):858-864.

[44] Ferrández A,Navarro M,Díez M,etal.Risk factors for advanced lesions undetected at prior colonoscopy:not always poor preparation[J].Endoscopy,2010,42(12):1071-1076.

[45] Rex DK,Petrini JL,Baron TH,etal.Quality indicators for colonoscopy[J].Gastrointest Endosc,2006,63(4 Suppl):S16-S28.

[46] Rex DK,Lehman GA,Ulbright TM,etal.Colonic neoplasia in asymptomatic persons with negative fecal occult blood tests:influence of age,gender,and family history[J].Am J Gastroenterol,1993,88(6):825-831.

[47] Sanaka MR,Deepinder F,Thota PN,etal.Adenomas are detected more often in morning than in afternoon colonoscopy[J].Am J Gastroenterol,2009,104(7):1659-1664.