When a patient develops colorectal cancer within a few

CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2013;11:768 773 Avoiding and Defending Malpractice Suits for Postcolonoscopy Cancer: Advice From an Expert Witness DOUGLAS K. REX Division of Gastroenterology/Hepatology, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana When a patient develops colorectal cancer within a few years of colonoscopy it sometimes results in a malpractice action against the colonoscopist. 1 This often results from an impression on the part of the patient, the patient s attorney, and some expert witnesses that colonoscopy is a guarantee of protection against colorectal cancer. Although it is always troubling to be sued, and some doctors are emotionally devastated by the process, malpractice suits alleging missed cancer are (in my experience) very difficult for the plaintiff to win, and a series of measures can further greatly increase the chance of a defense verdict. Colonoscopy is generally a poorly documented procedure in the absence of video recording, and no one involved in the medical-legal case can be certain that the colonoscopist performed a careful examination. Therefore, the case usually revolves around other documentation (or the absence of it) that supports a careful examination, the size of the tumor at diagnosis and the interval since the baseline colonoscopy, and the knowledge and performance of the defending doctor and the expert witnesses. In this article I review issues commonly encountered in malpractice suits centered on this issue, make recommendations for avoiding these suits, and discuss medical evidence that can be used by the defense when a suit proceeds. These recommendations represent both my understanding of the medical literature on colonoscopy and missed cancers, my own experience in performing colonoscopy, and my experience as an expert witness. Avoiding Malpractice Suits Alleging Missed Cancer Informed Consent The key risks to include in the informed consent discussion for colonoscopy are perforation and missed cancer or missed lesion. Other elements such as postpolypectomy bleeding and medication reaction typically also are discussed, and consideration should be given to including aspiration pneumonia and splenic injury. 2 A doctor who knows their adenoma detection rate (ADR) might present it to the patient during the process, although my own practice is to provide it only when the patient asks. Another approach is to say the general chance of a missed cancer, but this chance will depend greatly on the patient s age, sex, presence of risk factors, and the indication for the procedure. 3 For example, the risk of a missed cancer is higher when colonoscopy is performed for the indication of a positive fecal occult blood test (FOBT) 3 because the prevalence of cancer and advanced adenomas are both higher in patients with a positive FOBT than screening patients, and therefore the opportunity for missing is greater with a positive FOBT. The miss rates of colonoscopy for polyps of various sizes have been best defined by tandem studies, 4 and computerized tomographic colonography (CTC) studies that combine good CTC performance with segmental unblinding. 5,6 For polyps 1 cm or greater in size, the miss rates in tandem colonoscopy studies are 2% to 6%, 4 and in CTC studies are 12% to 17%. 5,6 My own approach is not quantitative with regard to missing, as in this test is the best available to examine the colon but it is not perfect, and rarely it can miss a significant growth. Bowel Preparation Issues Three guidelines have now endorsed split-dosing of preparations for colonoscopy. 7 9 The evidence that split-dosing improves the efficacy of preparation is overwhelming. 10,11 A reasonable question is whether the standard of medical care requires the use of split dosing. The answer would be that split-dosing is the standard of care if we consider evidence and guideline recommendations, 7 11 but not if we consider that many practitioners still do not split dose. My own impression is that using split-dosing helps provide an impression of awareness of the state of the art by a colonoscopist, and systematically not split-dosing implies a lack of seriousness about polyp detection. However, the issue is to avoid and defend malpractice in individual cases, and therefore the key is the documentation of preparation quality 12 in individual cases in which cancer develops postcolonoscopy. Appropriate documentation of preparation quality is essential to the physician s defense. It is acceptable to use either simple term 4 scales ranging from excellent to poor, to rate the preparation as adequate or inadequate, or to use validated scoring systems such as the Boston Bowel Preparation score, 13 the Ottawa score, 14 or the Aronchick scale. 15 The US Multi-society Task Force on Colorectal Cancer recommended that an adequate preparation is one that allows detection of polyps 6 mm and larger. 12,16 By using this definition, an inadequate preparation is not one with scattered bits of adherent mucus and feces but one in which there are pools of solid and semisolid debris that cannot be removed and cannot be moved out of the way by patient rotation. One issue that warrants clarification is whether to use the scales noted earlier to describe the contents of the colon on insertion or before the inspection begins, or to describe the preparation after the colon has been prepared for inspection by washing and suctioning. In many Abbreviations used in this paper: ADR, adenoma detection rate; CTC, computerized tomographic colonography; FOBT, fecal occult blood test; ICV, ileocecal valve. 2013 by the AGA Institute 1542-3565/$36.00 http://dx.doi.org/10.1016/j.cgh.2013.01.027

July 2013 POSTCOLONOSCOPY CANCER MALPRACTICE 769 clinical trials reporting the results of bowel preparation regimens the scales describe residual fluid and solid material that can be washed off the mucosa and suctioned. To a certain extent this approach lacks meaning in everyday practice because the only issue of relevance to the patient is the appearance of the colon after suctioning and washing. Many, if not most, good and many fair preparations according to these scales can be made excellent and good, respectively, for the purposes of the examination. Any preparation that cannot be cleaned to be above a grade of fair should be followed by a recommendation to repeat the examination at an interval shorter than would otherwise be appropriate for the findings. In some cases very specific language might be used to describe an area with less than ideal preparation such as the ascending colon preparation was such that polyps less than 1 cm could not be ruled out. Such language removes the risk of the plaintiff s expert deciding what the colonoscopist meant by fair preparation, and more effectively could support an intermediate postpolypectomy interval. To summarize, the optimal defense requires a description of the preparation as excellent or good throughout the colon. Photography can be very useful in supporting the adequacy of the preparation. 17,18 Standard photographs should be taken of the cecum and the rectum (see later) and they should be taken after suctioning and washing off mucus and bubbles. I have seen plaintiffs experts argue that the preparation was not good enough because a photograph of the cecal base showed a small area of adherent mucus. In addition, capturing photographs of several segments of the colon showing excellent preparation provides support for the endoscopist s claim of an adequate preparation. Rectal Examination It is important to document the results of a rectal examination performed before a colonoscope insertion. A surprising number of postcolonoscopy cancers are diagnosed in the distal rectum. Sometimes the defendant s doctor will testify that they always perform a rectal examination and the endoscopy room nurses will support the claim. This is good, however, documentation is better. The rectal examination should be a full finger insertion and circumferential sweep of the distal rectal mucosa, and not just lubricating of the anal canal. Landmark Documentation Cecal intubation should be documented by notation of landmarks and photography. 12,16,17 If photography is lacking, the plaintiff s expert may claim that the cecum was not intubated. A key photograph is the appendiceal orifice, optimally taken with the colonoscope tip far enough away to see the cecal strap fold around the appendiceal orifice but still proximal to the ileocecal valve (ICV). A second key photograph is of the cecum from just distal to the ICV, and showing both the ICV and the lateral wall of the cecal pouch. If the terminal ileum is intubated, it should be photographed. These photographs provide powerful proof that the cecum was fully intubated. 18 Because the majority of interval cancers occur in the proximal colon, these photographs assume even greater importance. I frequently examine the right colon twice, especially if a careful first examination from the cecal caput to the hepatic flexure has shown 1 or more polyps. This examination can be performed either in the forward view or in retroflexion, 19 and if retroflexion is chosen, I invariably take a photograph of the right colon in retroflexion. Finally, if retroflexion is performed in the rectum, as it should be unless the rectum appears narrow, that photograph also is taken. 20,21 If retroflexion is not performed, a forward-viewing photograph can be taken from the dentate line. Withdrawal Time The first quality recommendations regarding mucosal inspection during colonoscopy came in 2002 from the US Multisociety Task Force on Colorectal Cancer, 16 and these were updated by a joint task force of the American Society for Gastrointestinal Endoscopy/American College of Gastroenterology in 2006. 17 Both documents recommended that the ADR should be the primary measure of mucosal inspection and that secondarily the average withdrawal time in colons in which no biopsies or polypectomies were performed should be at least 6 minutes. Both documents recommended that the withdrawal time not be applied to individual cases because colonic length and fold anatomy is quite variable, and some colons can be effectively and carefully examined much faster than others. Subsequently, the withdrawal time began to assume more importance than it deserves after a landmark study showed that withdrawal times longer than 6 minutes were associated strongly with a better ADR as well as better detection of large adenomas. 22 This finding was interpreted incorrectly by many as evidence that simply lengthening withdrawal to more than 6 minutes would fix detection problems. Although withdrawal time is associated very strongly with ADR in retrospective studies, 22 26 insisting on longer withdrawal times will not necessarily increase the ADR, 27 probably because the longer times are not used to effectively examine the colon. On the other hand, colonoscopist education on lesion recognition combined with training in technique of examination has produced systematic increases in ADR. 28 Despite these caveats regarding the limitations of the withdrawal time as a quality indicator, there is no doubt that procedure times are reviewed and discussed in every malpractice suit involving missed cancer. Further, the 6-minute recommendation has, despite the attempts to avoid it, become a sort of medical-legal standard. Several years ago I defended a doctor in a missed cancer case involving a colonoscopy performed in 1998 (4 years before the first recommendations regarding withdrawal times) in which the doctor had photographed the cecum and then the rectum in retroflexion. The 2 photographs were both timed and the interval between the 2 photographs was exactly 4 minutes. The plaintiff s experts argued successfully that this could not have been enough time to carefully inspect the colon. Based on experiences of this type, I inspect for at least 6 minutes in almost all cases with intact colons. Parenthetically, I find that it almost always takes at least 6 minutes to carefully examine an intact colon, so this policy has little effect on my examination technique. In defense of a malpractice suit, having the withdrawal time documented and having it exceed 6 minutes has multiple advantages. First, documentation of the withdrawal time creates the impression that the colonoscopist is up to date on and takes current quality recommendations seriously. Second, documenting the withdrawal time prevents the plaintiff s expert from speculating on how long the withdrawal lasted. This is particularly important when the total procedure

770 DOUGLAS K. REX CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 7 time is relatively short (total procedure time is essentially always documented as the procedure start and stop time or the scope in to scope out time). For example, some experts will opine that a total procedural time of 10 to 15 minutes is evidence of rushing per se. However, if the cecal intubation time was 2 minutes, a total procedural time of 10 minutes could be quite reasonable. It is a mistake to assume that the plaintiff s expert will be sufficiently skilled at colonoscopy to recognize the possibility of a 2-minute cecal intubation time. 29 In our unit we measure ADR as the primary measure of colonoscopy quality, but we require measurement of withdrawal time in all colonoscopies so that it can be used to counsel a doctor with a low ADR. An additional benefit of documenting ADR and staying above 6 minutes withdrawal time is that it confers some degree of medical-legal protection as discussed earlier. Standardized Language Although not critical, it seems reasonable to include language describing careful technique. For example, as the colonoscope was withdrawn, care was taken to expose and inspect the proximal sides of the ICV, and of haustral folds, flexures, and rectal valves. By itself it has little impact, but in the context of adequate preparation, landmark notation and photography, and withdrawal time, the language helps to create an aura of a well-trained expert performing a careful examination. Adenoma Detection Rate It is highly likely that the plaintiff s attorney and her experts will become aware of recommendations for quality in the technical performance of colonoscopy and the primacy of the ADR. 12,16,17 There is nothing that speaks more to the overall skill of the colonoscopist and the quality of their examinations than evidence that the ADR was being measured during or before the period in which the colonoscopy in question occurred and that the ADR was greater than recommended thresholds. I have been surprised that plaintiffs experts are not challenged more by defense attorneys to provide evidence of their own ADRs. It is now more than 10 years since the first recommendation to measure the ADR. One could argue that by now a colonoscopist who is serious about detection would have measured the ADR. I have only taken one case of a missed cancer for a plaintiff. The case involved a 2-cm cecal cancer surrounding the appendiceal orifice that presented as ruptured appendicitis 2 months after the colonoscopy in question. There was no documentation of the appendiceal orifice as a landmark and no photograph. I reasoned that the appendiceal orifice is one site that we are supposed to see and document in every case and that given the time interval involved it was reasonable to conclude that seeing the orifice had not occurred. I have defended many missed cancer cases, and my personal bias in missed cancer cases is to take the side of the physician. However, in recent years I have declined to defend a few cases. The usual scenario in cases I have declined to defend has been that the records indicate having reached the cecum without notation of landmarks and with no photographs. The withdrawal time typically was not recorded. In this instance, I often ask the defense attorney if the doctor can produce evidence of an ADR and what the number is. In such a case, if the doctor has never measured the ADR, I will decline to defend the case. I reason that at this juncture in time there has been enough discussion of quality that any reasonable and careful practitioner of colonoscopy would be doing a better job of documentation and measuring quality than this scenario represents. Explain Hematochezia and Ensure Follow-up Evaluation In postcolonoscopy cancer cases in which the procedure indication was rectal bleeding, it is surprising how often the patient persists in having rectal bleeding for a year or more before they seek additional attention. This behavior results from false reassurance supplied by a negative colonoscopy. Bleeding indications (hematochezia, positive FOBT, iron-deficiency anemia, melena with a negative upper endoscopy) have a substantially higher predictive value for cancer compared with nonbleeding symptoms such as diarrhea, constipation, and abdominal pain. 30 From a medical-legal perspective, hematochezia is of greatest importance because it is so specific for the colorectum/anus. Therefore, before a colonoscopy for hematochezia a careful history should be performed, and a detailed examination should identify a source of bleeding consistent with the history. Optimally, the identified source is photodocumented. If the source is anal, treatment should be instituted and clear instructions should be given and documented for the patient to follow up with the endoscopist or the referring physician until the symptoms are resolved. If no source can be identified during colonoscopy but the history suggests an anal source, it still may be appropriate to institute treatment for an anal source (eg, a course of anal steroid cream) and definitely appropriate to recommend follow-up evaluation. If the patient is told to follow up with the referring physician, it may be best to recommend to both the patient and the referring physician that the patient should return to me if the bleeding persists. Summary of Avoidance Measures Missed cancer cases are inherently difficult for plaintiffs to win because of the extensive evidence that colonoscopy misses polyps, including polyps 10 mm or greater in size, and evidence that colonoscopy protection against cancer is imperfect. The ideal situation to defend is listed Table 1. Defending an Allegation of Missed Cancer The Plaintiff s Burden The plaintiff must prove that the performance of the colonoscopy was below the standard of care and that this Table 1. Ideal Circumstances for Defense of a Medical- Legal Case Alleging Negligent Colonoscopy Resulting in Missed Cancer Bowel preparation is excellent, good, or adequate or the equivalent Bowel preparation quality supported by photography Digital rectal examination and results are recorded Cecal intubation is documented by landmark notation and photography Withdrawal time is noted and exceeds 6 minutes Any retroflexion performed is photographed Physician participates in a quality-improvement program, measures ADR, and ADR exceeds recommended thresholds

July 2013 POSTCOLONOSCOPY CANCER MALPRACTICE 771 resulted in harm to the patient. The issue of harm is referred to as causation. The level of harm the plaintiff must establish can vary according to state laws and regulations. For example, in one state the plaintiff might be required to establish that the harm was such that the patient was more likely than not (51% probability) to die or another outcome as a result of the negligence. In another state the plaintiff might be required only to show that the negligence resulted in a reduction in the chance for survival. For example, if the cancer was alleged to have been stage I at the time of the colonoscopy and was stage III with 2 positive lymph nodes at the time of diagnosis then the patient still would have a greater than 50% chance of survival with surgery and adjuvant chemotherapy, but the colonoscopist could be found responsible for a reduction in the chance of survival as well for the cost and suffering associated with adjuvant chemotherapy. The case can be won for the defense on causation alone. For example, the patient undergoes a negative colonoscopy and 12 months later presents with abdominal pain and weight loss and a CT scan showing large liver metastases throughout both lobes. The expert oncologist for the defense might argue successfully that metastases of this size had to have been present 12 months earlier, and would have resulted in the patient s death irrespective of the colonoscopy result. The Plaintiff s Paradox The plaintiff seeks to establish negligence and maximize the damages. Important elements for discussion are the size of the colon lesion at diagnosis, the interval of time between the negative colonoscopy and the diagnosis, and the alleged size and stage of the lesion at the time of the colonoscopy. These size estimates often are made by oncologists and are based on limited science. Further, there is little evidence that the primary tumor and the liver metastases would be expected to grow at the same rate. In my experience, an estimation of the tumor passing through one stage in about a year is not uncommon. Estimations of growth rates of the primary are more variable. The paradox for the plaintiff is that to credibly establish negligence they must conclude that the lesion in the colon was of a sufficient size that it should have been detected by a well-trained colonoscopist performing a careful examination. However, a larger lesion that is closer in size to the cancer s size at diagnosis makes it more difficult to suggest a much earlier stage at the time of the negative colonoscopy. If multiple plaintiff experts give varying estimates of size and stage at the time of the negative colonoscopy, it can help to shed doubt on the entire process of determining the extent of harm. The Plaintiff s Experts The idea that plaintiffs experts have special expertise in the area of colonoscopy is generally incorrect. They are typically gastroenterologists or surgeons in general practice who may perform a lot of colonoscopies but who do not necessarily know the medical literature on missing during colonoscopy in detail. The defendant doctor and the defense attorney should learn the details of this literature. The plaintiff s expert must opine that missing a lesion greater than some particular size during colonoscopy is below the standard of medical care. If the size suggested by the expert is inconsistent with the medical literature, it provides an opportunity to attack the expert s knowledge and credibility. I have seen experts say that missing a lesion as small as 5 mm in size is below the standard of care. Even to suggest that a lesion 1 to 2 cm in size can never be missed is inconsistent with the results of tandem colonoscopy 4 and CTC studies with segmental unblinding. 5,6 Obviously, the risk of missing a particular lesion is a function not only of its largest diameter but also its shape and whether the lesion is located in clear view or on the proximal side of a fold or flexure. Both very old barium enema studies 31 and recent CTC studies 5 establish that these locations in the colon are associated with increased missing during colonoscopy. Thus, the credible plaintiff s expert either must admit that a small lesion could be missed by careful technique or hypothesize that the lesion was sufficiently large at the time of the negative colonoscopy that the damages are diminished, because the hypothesized lesion size (and likely the stage) then would be closer to the lesion size at the ultimate diagnosis. General Basis of the Defense The defense initially should establish that colonoscopy is not perfect. First, colonoscopy has been studied for its miss rate in both tandem colonoscopy studies and in CTC studies using segmental unblinding. In these studies, in which well-trained gastroenterologists were aware that their miss rate was being studied, even polyps 1 cm and larger were missed 6% of the time in tandem colonoscopy studies, and polyps 6 to 9 cm in size were missed nearly 15% of the time. 4 However, tandem colonoscopies are inherently flawed from the perspective of measuring the sensitivity of colonoscopy because a second colonoscopy is considered the gold standard, and the same technical issues that impaired the sensitivity of the first colonoscopy also affect the second colonoscopy. Therefore, CTC studies using segmental unblinding from centers of excellence are of greater relevance. These studies show that the miss rate of colonoscopy for polyps 1 cm or larger is 12% to 17%. 5,6 These studies cannot be used to measure the sensitivity of colonoscopy for polyps less than 1 cm in size because the sensitivity of CTC is less than colonoscopy for polyps in that size range. Juries are very understanding of the concept that no medical test is perfect, and if a test misses 12% to 17% of polyps greater than 1 cm in size, they can understand that this is a sufficient frequency that missing a polyp could have come into play in the individual case, even in the face of a careful examination. The literature is increasingly replete with evidence that colonoscopy is imperfect with regard to overall protection against colorectal cancer, with studies showing protection in the proximal colon ranging from none to 56%, 32 35 and protection in the range of 80% to 85% in the left colon. Again, this evidence underscores for the jury that the event of postcolonoscopy cancer is not rare and is not per se evidence of negligence. Consideration can be given to having the tumor tested for microsatellite instability or immunostaining of the tumor for a mismatch repair gene products. Both in the setting of Lynch syndrome and in the case of hypermethylated tumors with BRAF mutations, 36 there is general acceptance that microsatellite instability is associated with more rapid transition through the polyp/cancer sequence. Poor tumor differentiation also generally is accepted as being associated with faster growth. These

772 DOUGLAS K. REX CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 7 arguments will assist the defense only if the tumor has these characteristics. Considerable attention will be placed on the specific facts of the case. To the extent that the examination generally presents a picture of high quality, that there is documentation of the digital rectal examination, notation of cecal landmarks and photography, description of adequate preparation, documentation of withdrawal time, and photography of retroflexion, it becomes much easier for the defense expert to argue that the colonoscopist was clearly aware of and attentive to recommendations regarding high-quality examinations. If the doctor participates in a colonoscopy quality program and is aware of their ADR and their ADR is adequate (the higher the better), the defense arguments begin to become overwhelming. Finally, the case is made easier for the defense with a colonoscopist who shows in their deposition that they are personable, know the relevant literature and quality recommendations, and are committed to careful colonoscopy. The final element depends largely on the defense attorney. The defense attorney should become aware of the medical literature and the issues that surround these cases, through reading of the literature and direct consultation with defense experts. Although one approach to deposing the plaintiff s expert is to simply ask for their opinions, a more effective approach is to both get their opinions and thoroughly explore their understanding of the medical literature, so that errors that are made can be brought out later for the jury. There is no question that the case can be won or lost by the competence of the defense attorney and experts. The plaintiff oncologist and defense oncologist almost invariably will have differing opinions about growth rates and doubling times. The Future of Documentation As noted earlier, colonoscopies are poorly documented examinations, certainly relative to radiographic examinations. As systematic video recording becomes more feasible, it may be more difficult to resist systematic use of video recording. 37 My personal opinion is that video recordings of high-quality examinations would be a tremendous advantage to the defense of malpractice allegations of missed cancers, and essentially would eliminate cases in which a high-quality examination had been performed, just as the documentation already recommended previously greatly reduces the risk for colonoscopists. However, video recordings of poor-quality examinations certainly would provide evidence against physicians. In the future, willingness to video record, in combination with evidence of adequate ADR, could become a reasonable basis for patients and referring physicians to choose colonoscopists. Conclusions Malpractice cases alleging negligent performance of colonoscopy that resulted in failure to prevent cancer are difficult for plaintiffs to win, primarily because of extensive knowledge about detection rates for colonoscopy when the procedure is performed under optimal circumstances. Attention to appropriate documentation of several aspects of the procedure and participation in a quality program create an aura of a welltrained, careful colonoscopist. References 1. Rex DK, Bond JH, Feld AD. Medical-legal risks of incident cancers after clearing colonoscopy. Am J Gastroenterol 2001;96:952 957. 2. Cooper G, Kou TD, Rex DK. Complications following colonoscopy with anesthesia assistance: a population-based analysis. Arch Intern Med. In press. 3. Brenner H, Chang-Claude J, Seiler CM, et al. Interval cancers after negative colonoscopy: population-based case-control study. Gut 2012;61:1576 1582. 4. van Rijn JC, Reitsma JB, Stoker J, et al. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006;101:343 350. 5. Pickhardt PJ, Nugent PA, Mysliwiec PA, et al. Location of adenomas missed by optical colonoscopy. Ann Intern Med 2004;141: 352 359. 6. Van Gelder RE, Nio CY, Florie J, et al. Computed tomographic colonography compared with colonoscopy in patients at increased risk for colorectal cancer. Gastroenterology 2004;127: 41 48. 7. Lieberman DA, Rex DK, Winawer SJ, et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012;143:844 857. 8. Wexner SD, Beck DE, Baron TH, et al. A consensus document on bowel preparation before colonoscopy: prepared by a task force from the American Society of Colon and Rectal Surgeons (ASCRS), the American Society for Gastrointestinal Endoscopy (ASGE), and the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES). Gastrointest Endosc 2006;63:894 909. 9. Rex DK, Johnson DA, Anderson JC, et al. American College of Gastroenterology guidelines for colorectal cancer screening 2008. Am J Gastroenterol 2009;104:739 750. 10. Kilgore TW, Abdinoor AA, Szary NM, et al. Bowel preparation with split-dose polyethylene glycol before colonoscopy: a meta-analysis of randomized controlled trials. Gastrointest Endosc 2011; 73:1240 1245. 11. Cohen LB. Split dosing of bowel preparations for colonoscopy: an analysis of its efficacy, safety, and tolerability. Gastrointest Endosc 2010;72:406 412. 12. Lieberman D, Nadel M, Smith RA, et al. Standardized colonoscopy reporting and data system: report of the Quality Assurance Task Group of the National Colorectal Cancer Roundtable. Gastrointest Endosc 2007;65:757 766. 13. Lai EJ, Calderwood AH, Doros G, et al. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopyoriented research. Gastrointest Endosc 2009;69:620 625. 14. Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality. Gastrointest Endosc 2004; 59:482 486. 15. Choi YS, Suh JP, Kim JK, et al. Magnesium citrate with a single dose of sodium phosphate for colonoscopy bowel preparation. World J Gastroenterol 2011;17:242 248. 16. Rex DK, Bond JH, Winawer S, et al. 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. Am J Gastroenterol 2002;97:1296 1308. 17. Rex DK, Petrini JL, Baron TH, et al. Quality indicators for colonoscopy. Gastrointest Endosc 2006;63:S16 S28. 18. Rex DK. Still photography versus videotaping for documentation of cecal intubation: a prospective study. Gastrointest Endosc 2000;51:451 459. 19. Harrison M, Singh N, Rex DK. Impact of proximal colon retroflexion on adenoma miss rates. Am J Gastroenterol 2004;99:519 522.

July 2013 POSTCOLONOSCOPY CANCER MALPRACTICE 773 20. Saad A, Rex DK. Routine rectal retroflexion during colonoscopy has a low yield for neoplasia. World J Gastroenterol 2008;14: 6503 6505. 21. Rex DK. Development of distal rectal cancer 5 years after a normal photograph of the distal rectum. Gastrointest Endosc 2011;74:728 729. 22. Barclay RL, Vicari JJ, Doughty AS, et al. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. N Engl J Med 2006;355:2533 2541. 23. Rex DK. Colonoscopic withdrawal technique is associated with adenoma miss rates. Gastrointest Endosc 2000;51:33 36. 24. Sanchez W, Harewood GC, Petersen BT. Evaluation of polyp detection in relation to procedure time of screening or surveillance colonoscopy. Am J Gastroenterol 2004;99:1941 1945. 25. Fatima H, Rex DK, Rothstein R, et al. Cecal insertion and withdrawal times with wide-angle versus standard colonoscopes: a randomized controlled trial. Clin Gastroenterol Hepatol 2008;6: 109 114. 26. Simmons DT, Harewood GC, Baron TH, et al. Impact of endoscopist withdrawal speed on polyp yield: implications for optimal colonoscopy withdrawal time. Aliment Pharmacol Ther 2006;24: 965 971. 27. Corley DA, Jensen CD, Marks AR. Can we improve adenoma detection rates? A systematic review of intervention studies. Gastrointest Endosc 2011;74:656 665. 28. Barclay RL, Vicari JJ, Greenlaw RL. Effect of a time-dependent colonoscopic withdrawal protocol on adenoma detection during screening colonoscopy. Clin Gastroenterol Hepatol 2008;6: 1091 1098. 29. Rex DK. Is splenic injury from colonoscopy malpractice? Am J Gastroenterol 2010;105:957 958. 30. Rex DK. Colonoscopy: a review of its yield for cancers and adenomas by indication. Am J Gastroenterol 1995;90:353 365. 31. Miller RE, Lehman G. Polypoid colonic lesions undetected by endoscopy. Radiology 1978;129:295 297. 32. Baxter NN, Goldwasser MA, Paszat LF, et al. Association of colonoscopy and death from colorectal cancer. Ann Intern Med 2009;150:1 8. 33. Lakoff J, Paszat LF, Saskin R, et al. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. Clin Gastroenterol Hepatol 2008;6: 1117 1121. 34. Singh H, Nugent Z, Demers AA, et al. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010;105:2588 2596. 35. Brenner H, Chang-Claude J, Seiler CM, et al. Protection from colorectal cancer after colonoscopy: a population-based, casecontrol study. Ann Intern Med 2011;154:22 30. 36. Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012;107:1315 1329. 37. Rex DK, Hewett DG, Raghavendra M, et al. The impact of videorecording on the quality of colonoscopy performance: a pilot study. Am J Gastroenterol 2010;105:2312 2317. Reprint requests Address requests for reprints to: Douglas K. Rex, MD, Indiana University Hospital, 550 N University Boulevard, #4100, Indianapolis, Indiana 46202. e-mail: drex@iupui.edu; fax: (317) 944-5449. Conflicts of interest The author discloses no conflicts.