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Preoperative Evaluation of Colorectal Cancer
Surg Oncol Clin N Am 15 (2006) 39–49
Preoperative Evaluation of Colorectal Cancer James T. McCormick, DOa,b, Sharon G. Gregorcyk, MDc,* a
Department of Surgery, The Western Pennsylvania Hospital, 4800 Friendship Avenue, Pittsburgh, PA 15224, USA b Temple University School of Medicine, 3420 North Broad Street, Philadelphia, PA 19140, USA c Division of Colon and Rectal Surgery, Medical City Dallas Hospital, 7777 Forest Lane C760, Dallas, TX 75320, USA
Surgery is a primary modality for the treatment of patients with colorectal cancer. Before any surgical therapy, patients diagnosed with colorectal cancer require an evaluation. A preoperative evaluation is necessary for multiple reasons, including the basic need to assess the patient’s risk associated with surgery and to allow them to be medically optimized for surgery. Beyond that, the preoperative evaluation is useful in planning the surgical resection and may be used to stage the patient’s cancer. With regards to rectal cancer, preoperative staging is essential to determine the possible need for preoperative adjuvant therapy. This article focuses on the elective surgical setting and the recommended preoperative evaluation of patients who have been diagnosed with colorectal cancer.
History and physical The surgeon should perform a thorough history and physical examination on all patients with colorectal cancer. First, the patient must be deemed fit for surgery. Guidelines have been established to assess the cardiovascular risk of any patient undergoing a non-cardiac surgery [1]. These guidelines can help to optimize patients for surgery and can help identify patients who are at such high risk for surgery that alternatives to standard surgical practices must be considered. In the extreme case, this might mean no * Corresponding author. E-mail address: [email protected] (S.G. Gregorcyk). 1055-3207/06/$ - see front matter Ó 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.soc.2005.10.002 surgonc.theclinics.com
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surgery at all. For a patient who has rectal cancer, chemoradiation alone might be considered. In other instances, it might mean a more limited resection to shorten operative time and stress on the patient. In addition to determining fitness for surgery, the history and physical exam can provide data that will guide therapy. Directed questions about symptoms of obstruction or weight loss can yield information about the extent of the tumor. A patient who has a partially obstructed bowel may not tolerate a standard bowel preparation and may require a slower preparation. Significant weight loss that is not attributable to obstruction may be caused by metastatic disease. These patients may have nutritional deficits, which if repleted, will aid in recovery from surgery. The surgeon should inquire about and document continence status. This is pertinent when dealing with low rectal cancers because an anastomosis low in the pelvis will worsen tenuous bowel control and should be avoided. Continence must also be considered if an extended resection, such as a total colectomy, is planned. If the patient has poor sphincter function, the diarrhea resulting from a total colectomy may have a profound impact on the patient’s quality of life and a segmental resection may be the better choice. The patient’s family history as well as the patient’s own personal history may lead to concerns for a hereditary syndrome. Hereditary non-polyposis colorectal cancer syndrome and familial adenomatous polyposis are important to recognize preoperatively because they require more extensive surgeries than sporadic colon cancers. In addition to assessing a patient’s fitness, a physical examination should focus on discovering metastases as well as revealing technical considerations that may alter surgical plans. For instance, a bulky fixed tumor mass may preclude a laparoscopic approach. Jaundice or a right upper quadrant mass may be signs of extensive metastatic liver disease. A digital rectal examination is critical when evaluating a patient with rectal cancer. For palpable tumors, it is necessary to assess whether the tumor is fixed or mobile and if it invades into other structures such as the vagina or prostate. Also, the surgeon needs to assess the distance of the tumor from the anal verge and whether there is sphincter involvement. Obviously the functional status of the sphincters is very important and tone and squeeze should be documented. All of these findings are essential to determine if the patient is a candidate for sphincter preserving surgery. In cases of colon cancer, the digital rectal exam assesses the sphincter function, but also may reveal signs of extensive disease such as a Blummer’s shelf. Age-appropriate cancer screening should be up-to-date for all patients. Females should have annual mammograms starting at age 40. Females in reproductive years who have been sexually active should have Pap smears at least every 3 years. Males over age 50 should receive prostate screening [2]. Discretionary imaging and laboratory testing based on history and physical exam findings is always appropriate; however, the remainder of this article will focus on the routine screening modalities. Colon cancer and rectal
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cancer require different preoperative evaluation strategies. Although the upper rectal cancers are typically treated the same as colon cancers, the mid and lower rectal cancers are not and may require preoperative chemoradiation and sphincter preservation when possible. For these reasons, the preoperative evaluation for rectal cancer is typically more extensive and differences will be highlighted. Colonoscopy Colonoscopy is routine in the preoperative evaluation of patients with colon or rectal cancer. The study provides valuable information about the tumor, including location and characteristics that might affect the patient’s treatment. For example, if the tumor is large, bulky, and nearly obstructing, more extensive evaluation might be needed to plan the patient’s surgery. In the case of rectal cancer, preoperative chemoradiation would be indicated. In addition to assessing the tumor, additional lesions in the colon must be ruled out. According to some literature, the incidence of synchronous polyps in patients who have colorectal cancer is 24%–57%, depending on the size and histology of the primary lesion [3–8]. Other, more conservative reports quote the incidence of synchronous polyps to be only 10% [9]. The incidence of synchronous cancers is reported to be about 4% [7,10,11]. In one prospective study, findings on preoperative colonic evaluation resulted in a change of management in 3% of their patients [7]. Given these statistics, complete evaluation of the colon in all patients with colonic neoplasm is indicated. If the size and bulk of the tumor prevents proximal evaluation of the colon, a contrast study or CT colography may be an alternate option. Otherwise, the remainder of the colon can be evaluated intraoperatively with an on-table colonoscopy, or postoperatively within 6 months of surgery. When considering a laparoscopic approach to colon cancer surgery, accurate localization of the tumor is imperative to avoid removal of the wrong segment of intestine [12]. Colonoscopic localization simply by noting the proximity of the tumor to an unmistakable landmark is only accurate when dealing with the rectum or cecum. Otherwise, localization can be accomplished by endoscopic injection of India ink in three quadrants of bowel adjacent and distal to, but not through, the tumor, or by endoscopic placement of clips and subsequent plain film of the abdomen. Alternatively, barium enema or CT colography can be used. Rigid proctoscopy Because of the flexible nature of the colonoscope, the distance of the tumor from the anal verge cannot be accurately measured on colonoscopy. When the tumor is obviously within the colon or is palpable within the rectum, this limitation of the colonoscope is not an issue. Commonly, a tumor
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reported to be in the sigmoid colon by colonoscopy is actually much lower and represents rectal cancer. A rigid proctoscope is very useful for accurately measuring the distance of the tumor from the anal verge which not only helps in planning surgery, but also determines if the tumor is in a location where it might warrant preoperative neoadjuvant therapy. Chest radiography Whether performed as part of the evaluation for determining operative risk or to screen for lung metastases, which occur in 10%–20% of patients, chest radiography has become a standard part of the preoperative evaluation for colorectal cancer. CT scan of the chest offers no apparent benefit over a chest radiograph even in patients with known extracolonic metastases [13]. Laboratory Elevated serum carcinoembryonic antigen (CEA) levels O 5.0 ng/mL have been shown to have an adverse impact on survival, independent of tumor stage [14–22]. Despite the fact that a CEA level will not alter initial therapy, many doctors recommend that this test be performed for prognostic purposes and as a baseline for postoperative surveillance [23,24]. It is reasonable to obtain a preoperative baseline CEA in patients who will undergo postoperative surveillance. Patients with an elevated level of the protein CA19-9 in stage II of colorectal cancer have been shown to have a significantly poorer prognosis than those with normal levels, which leads some doctors to recommend this test for prognostic purposes [25,26]. Preoperative hypoalbuminema, defined as levels ! 3.5 g/dL, has been shown to be an independent predictor of surgical morbidity and mortality in general, and colorectal surgical populations more specifically [27,28]. Debilitated patients and those at risk for protein-calorie malnutrition or depleted visceral protein stores may benefit from nutritional assessment and enteral or parenteral nutritional supplementation before elective surgery. Basic hematology, liver function, and chemistry panels are used as appropriate for age and preexisting medical conditions. Liver function tests have poor sensitivity and specificity for detecting liver metastasis and are not routinely indicated. Serum potassium and hemoglobin levels are clinically relevant values in the postoperative period [29]. A preoperative baseline for these values may therefore prove helpful. In addition, because colorectal cancer can cause anemia, a preoperative hemoglobin screen can help plan for a possible need for blood products. Abdominal CT scan CT scan of the abdomen and pelvis in patients with colorectal cancer has been used with varying degrees of success to determine the extent of the
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primary tumor, the presence of lymph node involvement, and presence of liver metastases. It is important to obtain this information preoperatively for patients who have rectal cancer. Locally advanced stage II and stage III rectal cancers are candidates for neoadjuvant chemoradiation before surgery. CT scanning can be helpful with this staging. The highest reported sensitivity of a CT scan in imaging lymphadenopathy is 73%; specifity is 58% [30,31]. CT scans have been reported to correctly classify the T (tumor size) and N (node involvement) categories of cancer in 81% and 67.6% of cases respectively [32]. Endorectal ultrasound [33] and MRI with endorectal coil (discussed hereafter) are both more sensitive and specific than CT scan for detecting mesenteric lymphadenopathy in rectal cancer. In addition to local staging, the CT scan also assesses the liver. Although knowledge of liver disease does not usually alter the surgical approach for colon cancer, in patients who have rectal cancer, where the stakes of radical surgery are high, existence of liver metastases may influence management decisions. Furthermore, adequate staging mandates evaluation of the liver at the time of diagnosis and before neoadjuvant therapy. Contrast-enhanced CT scan of the abdomen is frequently used to evaluate the liver for metastatic disease in patients who have colorectal cancer. Sensitivity is between 73% and 79% for hepatic metastasis [29,34]. This sensitivity improves to 85% when CT scans are performed only when liver metastases are suspected based on laboratory or physical exam finding [35]. Sensitivities and specificities of 90% and 95% in detecting liver metastases O 1cm diameter have been reported [36]. Thus, the routine use of CT scan is advocated in the preoperative evaluation of patients with rectal cancer. The need for a CT scan preoperatively for colon cancer is not as compelling as that for rectal cancer. Lymphadenopathy does not change the need or timing of surgery. Liver metastases may result in a shorter segment of colon being resected but that is a decision that can be made intraoperatively after the metastases have been found on palpation or intraoperative ultrasound. Its use as a baseline scan is questionable because there will be changes on the scan after surgery, so future scans may be difficult to compare with a preoperative scan. Nevertheless, some doctors advocate a routine preoperative CT scan for colon cancer. Kerner and coworkers [37] evaluated 158 patients who had colon cancer, and found 120 otherwise unknown findings in 88 patients by using a preoperative CT scan. Thirty-five percent of those findings were believed to be clinically significant. McAndrew and Saba [32] reviewed their experience and found that CT scans resulted in an altered surgical approach for ! 2% of their patients. Thus, the need for a routine preoperative CT scan in cases of uncomplicated colon cancer remains controversial [38]. Although readily available and reasonably accurate, there is a paucity of evidence that supports this as a cost-effective screening modality [39]. The American Society of Colon and Rectal Surgeons Standards Practice Task Force does not promote routine preoperative CT scanning in colon cancer patients but does advocate it in selected patients [40].
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Most surgeons agree that adequate staging mandates evaluation of the liver either before or at the time of surgery. Intraoperative palpation of the liver satisfies this requirement. However, laparoscopy has made palpation of the liver a practical impossibility. An alternative to palpation is the use of intraoperative ultrasound [41]. If the surgeon is not proficient at laparoscopic ultrasound of the liver, then the liver should be assessed by other means and a preoperative CT scan is a reasonable choice. Palpable masses or near obstructing tumors on colonoscopy are concerning for advanced, bulky disease that may be invading other organs. A CT scan can help the surgeon delineate the extent of the tumor and plan the operative approach.
Ultrasound Intraoperative liver ultrasound performed either open or laparoscopically, is accurate in detecting liver metastasis [39,42]. It is, however, time consuming and operator dependent. Surgeon experience and preference determines the role of the imaging modality. Endorectal ultrasound has become the standard of care for staging rectal cancers. It is critical to accurately determine the T and N stage of rectal cancers so that patients with transmural disease (see Fig. 1) or nodal disease can be offered preoperative chemoradiation. The accuracy of endorectal ultrasound for staging rectal cancers is reported to be 75%–94%; the accuracy of the T stage is reported to be 69%–94.8% and the N stage is reported as 58%–83% [43–47]. Success of this technique is operator dependant [46,48] and may be limited by tumor or patient factors. Three-dimensional ultrasound is now available and although experience is limited, technical advantages over standard processing include the ability to review images in a ‘‘real-time’’ mode but at a later date.
Fig. 1. Endorectal ultrasound of rectal cancer, which is seen on the left side of the picture. The tumor invades through the muscularis propria into the perirectal fat and is a T3 lesion.
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MRI MRI of the liver is useful to better define suspicious liver lesions discovered by other imaging modalities. It is generally not used as a primary screening modality. MRI can be used for the local staging of rectal cancers. With the use of endorectal coils, MRI has a reported accuracy of 72%–100% in tumor staging [49–51]. When endorectal surface coil magnetic resonance imaging and endorectal ultrasound were compared head-to-head, there was no difference in T-staging between the two modalities, but MRI more accurately identified nodal involvement [52]. Whether this slight advantage justifies the increased cost and inconvenience is not well defined. The authors prefer endorectal ultrasound as a primary modality and use of MRI when ultrasound cannot be performed, is limited because of patient or tumor factors, or when invasion of other structures needs to be further defined. Positron emission tomography Positron Emission Tomography (PET) takes advantage of increased metabolic activity associated with malignancy or inflammation by detecting increased uptake of radiolabeled flourodeoxyglucose (FDG). Although highly sensitive for detecting carcinoma and metastases, its low specificity (43%) [53,54] limits the use of FDG-PET as a primary tool for preoperative assessment. Hybrid PET-CT may improve staging accuracy. An evolving technology, FDG-PET is most promising in the postoperative arena for primary surveillance or as a secondary imaging technique, accuracy is reported to be 93% [55]. There is not a reported indication for PET scan in the routine preoperative assessment of colorectal cancer. Bowel preparation Although mechanical bowel preparation (MBP) is recommended by most experts [56], a number of published studies challenge this approach. Prospective randomized trials comparing MBP and no MBP have demonstrated no difference in rate of wound infection, anastomotic leak, or development of intra-abdominal abscess [57–61]. Some authors have even demonstrated higher wound infection rates in patients who had MBP [62]. One explanation for this phenomenon is that liquid stool remaining after MBP is more susceptible to spillage than solid stool [63]. Additionally, extra-abdominal morbidity may be less without MBP because of the complications associated with preparation [64]. Despite this evidence, surgeons have been reluctant to adopt the protocol of colon resection without mechanical cleansing of the bowel. Most cite technical considerations and obvious distaste for manipulating stool, and point out that all of the aforementioned studies lack statistical power.
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Table 1 Recommendations for preoperative evaluation of patients with colorectal cancer Cancer Evaluation method History and physical Family history Colonoscopy Proctoscopy Basic lab Liver function tests CEA Chest radiography Abdominal CT scan Endoscopic ultrasound MRI PET scan a b c
Colon a
Yes Yes Yes Nob Yes Selectivec Yes Yes Selective No No No
Rectal Yes Yes Yes Yes Yes Selective Yes Yes Yes Yes Selective No
Comments Genetic counseling and testing as appropriate
As indicated from history or physical Baseline for follow-up if desired Evaluate liver prior to laparoscopy Clarification of other findings Major role is follow-up
Yes: the preponderance of data or expert opinion support routine use of these modalities. No: studies are not indicated. Selective: use of method is discretionary, based on individual clinical scenario.
Technical considerations of laparoscopic colon surgery make extrapolation of these data to the laparoscopic arena difficult. Laparoscopically manipulating a colon that is filled with stool is more difficult than a prepped colon, and to our knowledge, no studies of bowel preparation have included patients undergoing laparoscopy. We feel omission of the routine MBP deserves serious consideration but further research is necessary to conclude it equal or superior to MBP. The authors employ laparoscopic techniques whenever possible and currently prescribe mechanical bowel preparation before elective surgery. The use of prophylactic perioperative antibiotics is scientifically well supported and recommended [65]. Conclusions The preoperative evaluation of patients who have colorectal cancer will vary based on the type of cancer and on results of the history and physical examination. Routine screening for all patients is summarized in Table 1 and should include evaluation of the entire colon, a chest radiograph, and standard labs including a CEA if postoperative surveillance is planned. For rectal cancer patients, endorectal ultrasound is the preferred method of preoperative local staging. MRI with an endorectal coil can be used when ultrasound cannot be performed, is limited because of patient or tumor factors, or when invasion of other structures needs further delineation. A CT scan is also recommended preoperatively in all rectal cancer patients to further assess the local disease and also to determine if metastases are present, because that finding could alter surgical plans.
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Evaluation of the liver is important for staging colon cancer but may be accomplished intraoperatively by palpation and inspection or by ultrasound. If these are not possible, then a CT scan preoperatively is recommended and is the most widely used imaging technique. MRI is a useful adjunct to better define suspicious lesions but is not routinely used in the preoperative setting. References [1] Mukherjee D, Eagle KA. Perioperative cardiac assessment for non-cardiac surgery: eight steps to the best possible outcome. Circulation 2003;107:2771–4. [2] Smith RA, Cokkinides V, Eyre HJ. American Cancer Society guidelines for the early detection of cancer, 2005. CA Cancer J Clin 2005;55(1):31–44. [3] Opelka FG, Timmcke AE, Gathright JB Jr, et al. Diminutive colonic polyps: an indication for colonoscopy. Dis Colon Rectum 1992;35:178–81. [4] Read TE, Read JD, Butterly LF. Importance of adenomas 5 mm or less in diameter that are detected by sigmoidoscopy. N Engl J Med 1997;336:8–12. [5] Demetriades H, Kanellos I, Blouhos K, et al. Synchronous polyps in patients with colorectal cancer. Tech Coloproctol 2004;8(Suppl 1):S72–5. [6] McGarrity TJ, Bhatti AM, Peters DJ, et al. Synchronous proximal polyps and cancer in patients with polyps detected at sigmoidoscopy: results of a single, rural-based sigmoidoscopy clinic. Dig Dis Sci 2002;47(2):309–16. [7] Arenas RB, Fichera A, Mhoon D, et al. Incidence and therapeutic implications of synchronous colonic pathology in colorectal adenocarcinoma. Surgery 1997;122(4):706–9. [8] Place RJ, Simmang CL. Hyperplastic-adenomatous polyposis syndrome. J Am Coll Surg 1999;188(5):503–7. [9] Northover JM. Staging and management of colorectal cancer. World J Surg 1997;21:672–7. [10] Papadopoulos V, Michalopoulos A, Basdanis G, et al. Synchronous and metachronous colorectal carcinoma. Tech Coloproctol 2004;8(Suppl 1):S97–100. [11] Oya M, Takahashi S, Okuyama T, et al. Synchronous colorectal carcinoma: clinico-pathological features and prognosis. Jpn J Clin Oncol 2003;33(1):38–43. [12] Larach SW, Patankar SK, Ferrara A, et al. Complications of laparoscopic colorectal surgery: analysis and comparison of early vs latter experience. Dis Colon Rectum 1997;40: 592–6. [13] Povoski SP, Fong Y, Sgouros SC, et al. Role of chest CT in patients with negative chest xrays referred for hepatic colorectal metastases. Ann Surg Oncol 1998;5(1):9–15. [14] Wanebo HJ, Rao B, Pinsky CM, et al. Preoperative carcinoembryonic antigen level as a prognostic indicator in colorectal cancer. N Engl J Med 1978;299:448–51. [15] Wolmark N, Fisher B, Wieand HS, et al. The significance of preoperative carcinoembryonic antigen levels in colorectal cancer. Ann Surg 1984;199:375–82. [16] Onetto M, Paganuzzi M, Secco GB, et al. Preoperative carcinoembryonic antigen and prognosis in patients with colorectal cancer. Biomed Pharmacother 1985;39:392–5. [17] Scott NA, Wieand HS, Moertel CG, et al. Colorectal cancer. Dukes’ stage, tumor site, preoperative plasma CEA level, and patient prognosis related to tumor DNA ploidy pattern. Arch Surg 1987;122:1375–9. [18] Wiggers T, Arends J, Volovics A. Regression analysis of prognostic factors in colorectal cancer after curative resections. Dis Colon Rectum 1988;31:33–41. [19] Meling GI, Rognum TO, Clausen OPF, et al. Serum carcinoembryonic antigen in relation to survival, DNA ploidy pattern, and recurrent disease in 406 colorectal carcinoma patients. Scand J Gastroenterol 1992;27:1061–8. [20] Slenz K, Senagore A, Hibbert J, et al. Can preoperative and postoperative CEA predict survival after colon cancer resection? Am Surg 1994;60:528–32.
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[21] Lindmark G, Bergstro¨m R, Pa˚hlman L, et al. The association of preoperative serum tumour markers with Dukes’ stage and survival in colorectal cancer. Br J Cancer 1995;71:1090–4. [22] Harrison LE, Guillem JG, Paty P, et al. Preoperative carcinoembryonic antigen predicts outcomes in node-negative colon cancer patients: a multivariate analysis of 572 patients. J Am Coll Surg 1997;185:55–9. [23] Compton C, Fenoglio-Preiser CM, Pettigrew N, et al. American joint committee on cancer prognostic factors consensus conference colorectal working group. Cancer 2000;88:1739. [24] Duffy MJ, van Dalen A, Haglund C, et al. Clinical utility of biochemical markers in colorectal cancer European group on tumour markers (EGTM) guidelines. Eur J Cancer 2003;39:718. [25] Chen CC, Yang SH, Lin JK, et al. Is it reasonable to add preoperative serum level of CEA and CA19–9 to staging for colorectal cancer? J Surg Res 2005;124(2):169–74. [26] Diez M, Cerdan FJ, Pollan M, et al. Prognostic significance of preoperative serum CA 19.9 assay in patients with colorectal carcinoma. Anticancer Res 1994;14(6B):2819–25. [27] Gibbs J, Cull W, Henderson W, et al. Preoperative serum albumin level as a predictor of operative mortality and morbidity: results from the national VA surgical risk study. Arch Surg 1999;134(1):36–42. [28] Alves A, Panis Y, Mathieu P, et al. Postoperative mortality and morbidity in French patients undergoing colorectal surgery results of a prospective multicenter study. Arch Surg 2005; 140:278–83. [29] Skenderis BS 2nd, Rodriguez-Bigas M, Weber TK, et al. Utility of routine postoperative laboratory studies in patients undergoing potentially curative resection for adenocarcinoma of the colon and rectum. Cancer Invest 1999;17(2):102–9. [30] Frenny PC, Marks WN, Ryan JA, et al. Colorectal carcinoma evaluation with CT: preoperative staging and detection of post-operative recurrence. Radiology 1986;158:347–53. [31] Balthazar EJ, Megibow AJ, Hulnick D, et al. Carcinoma of the colon: detection and preoperative staging by CT. AJR Am J Roentgenol 1988;150:301–6. [32] Hundt W, Braunschweig R, Reiser M. Evaluation of spiral CT in staging of colon and rectum carcinoma. Eur Radiol 1999;9:78–84. [33] Beynon J, Mortensen NJ, Foy DM, et al. Pre-operative assessment of local invasion in rectal cancer: digital examination, endoluminal sonography or computed tomography? Br J Surg 1986;73(12):1015–7. [34] McAndrew MR, Saba A. Efficacy of routine preoperative computed tomography scans in colon cancer. Am Surg 1999;65:205–8. [35] Valls C, Andia E, Sanchez A, et al. Hepatic metastases from colorectal cancer: preoperative detection and assessment of resectability with helical CT. Radiology 2001;218(1):55–60. [36] Ward J, Naik KS, Guthrie JA, et al. Hepatic lesion detection: comparison of MR imaging after the administration of superparamagnetic iron oxide with dual-phase CT by using alternative-free response receiver operating characteristic analysis. Radiology 1999;210:459–66. [37] Kerner BA, Oliver GC, Eisenstat TE, et al. Is preoperative computerized tomography useful in assessing patients with colorectal carcinoma? Dis Colon Rectum 1993;36(11):1050–3. [38] Cohen AM. Preoperative evaluation of patients with primary colorectal cancer. Cancer 1992;70(5 Suppl):1328–32. [39] Fisher KS, Zamboni WA, Ross DS. The efficacy of preoperative computed tomography in patients with colorectal carcinoma. Am Surg 1990;56(6):339–42. [40] Otchy D, Hyman NH, Simmang C, et al. Practice parameters for colon cancer. Dis Colon Rectum 2004;47:1268–84. [41] Milsom JW, Jerby BL, Kessler H, et al. Prospective, blinded comparison of laparoscopic ultrasonography vs. contrast-enhanced computerized tomography for liver assessment in patients undergoing colorectal carcinoma surgery. Dis Colon Rectum 2000;43(1):44–9. [42] Paul MA, Mulder LS, Cuesta MA, et al. Impact of intraoperative ultrasonography on treatment strategy for colorectal cancer. Br J Surg 1994;81(11):1660–3. [43] Glaser EF, Schlag P, Herfarth CH. Endorectal ultrasonography for the assessment of invasion of rectal tumors and lymph node involvement. Br J Surg 1990;77:883–7.
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[44] Rifkin MD, Ehrlich SM, Marks G. Staging of rectal carcinoma: prospective comparison of endorectal US and CT. Radiology 1989;170:319–22. [45] Pappalardo G, Regio D, Grattaroli FM, et al. The value of endoluminal ultrasonography and computed tomography in the staging of rectal cancer: a preliminary study. J Surg Oncol 1990;43:219. [46] Orrom WJ, Wong WD, Rothenberger DA, et al. Endorectal ultrasound in the preoperative staging of rectal tumors. A learning experience. Dis Colon Rectum 1990;33(8):654–9. [47] Korkut MA, Killi R, Kara E, et al. Role of endorectal ultrasonography in preoperative evaluation of rectal cancer. Asian J Surg 1997;20:83–6. [48] Garcia-Aguilar J, Pollack J, Lee SH, et al. Accuracy of endorectal ultrasonography in preoperative staging of rectal tumors. Dis Colon Rectum 2002;45(1):10–5. [49] Murano A, Sasaki F, Kido C, et al. Endoscopic MRI using 3D-spoiled GRASS (SPGR) sequences for local staging of rectal carcinoma. J Comput Assisst Tomogr 1995;19:586. [50] Joosten FBM, Jansen JBMJ, Joosten HJM, et al. Staging of rectal carcinoma using MR double surface coil, MR endorectal coil, and intrarectal ultrasound: correlation with histopathologic findings. J Comput Assisst Tomogr 1995;19:52. [51] Blomqvist L, Machado M, Rubio C, et al. Rectal tumor staging: MR imaging using pelvic phased-array and endorectal coil vs endoscopic ultrasonography. Eur Radiol 2000;10: 653–60. [52] Maldjian C, Smith R, Kilger A, et al. Endorectal surface coil MR imaging as a staging technique for rectal carcinoma: a comparison study to rectal endosonography. Abdom Imaging 2000;25:75–80. [53] Falk PM, Gupta NC, Thorson AG, et al. Positron emission tomography for preoperative staging of colorectal carcinoma. Dis Colon Rectum 1994;37(2):153–6. [54] Abdel-Nabi H, Doerr RJ, Lamonica DM, et al. Staging of primary colorectal carcinomas with fluorine-18 fluorodeoxyglucose whole-body PET: correlation with histopathologic and CT findings. Radiology 1998;206(3):755–60. [55] Vitola JV, Delbeke D, Sandler MP, et al. Positron emission tomography to stage suspected metastatic colorectal carcinoma to the liver. Am J Surg 1996;171(1):21–6. [56] Otchy D, Hyman NH, Simmang C, et al. Practice parameters for colon cancer. Dis Colon Rectum 2004;47:1269–84. [57] Zmora O, Mahajna A, Bar-Zakai B, et al. Colon and rectal surgery without mechanical bowel preparation: a randomized prospective trial. Ann Surg 2003;237:363–7. [58] Miettinen RPJ, Laitinen ST, Makela JT, et al. Bowel preparation with oral polyethylene glycol electrolyte solution vs. no preparation in elective open colorectal surgery: prospective, randomized study. Dis Colon Rectum 2000;43:669–77. [59] Fa-Si-Oen P, Roumen R, Buitenweg J, et al. Mechanical bowel preparation or not? Outcome of a multicenter, randomized trial in elective open colon surgery. Dis Colon Rectum 2005; 48(8):1509–16. [60] Burke P, Mealy K, Gillen P, et al. Requirement for bowel preparation in colorectal surgery. Br J Surg 1994;81(6):907–10. [61] Ram E, Sherman Y, Weil R, et al. Is mechanical bowel preparation mandatory for elective colon surgery? A prospective randomized study. Arch Surg 2005;140(3):285–8. [62] Santos JC Jr, Batista J, Sirimarco MT, et al. Prospective randomized trial of mechanical bowel preparation in patients undergoing elective colorectal surgery. Br J Surg 1994; 81(11):1673–6. [63] Mahajna A, Krausz M, Rosin D, et al. Bowel preparation is associated with spillage of bowel contents in colorectal surgery. Dis Colon Rectum 2005;48(8):1626–31. [64] Bucher P, Gervaz P, Soravia C, et al. Randomized clinical trial of mechanical bowel preparation versus no preparation before elective left-sided colorectal surgery. Br J Surg 2005;92: 409–14. [65] Song F, Glenn AM. Antimicrobial prophylaxis in colorectal surgery: a systematic review of randomized controlled trials. Br J Surg 1998;85:1232–41.
Preoperative Evaluation of Colorectal Cancer James T. McCormick, DOa,b, Sharon G. Gregorcyk, MDc,* a
Department of Surgery, The Western Pennsylvania Hospital, 4800 Friendship Avenue, Pittsburgh, PA 15224, USA b Temple University School of Medicine, 3420 North Broad Street, Philadelphia, PA 19140, USA c Division of Colon and Rectal Surgery, Medical City Dallas Hospital, 7777 Forest Lane C760, Dallas, TX 75320, USA
Surgery is a primary modality for the treatment of patients with colorectal cancer. Before any surgical therapy, patients diagnosed with colorectal cancer require an evaluation. A preoperative evaluation is necessary for multiple reasons, including the basic need to assess the patient’s risk associated with surgery and to allow them to be medically optimized for surgery. Beyond that, the preoperative evaluation is useful in planning the surgical resection and may be used to stage the patient’s cancer. With regards to rectal cancer, preoperative staging is essential to determine the possible need for preoperative adjuvant therapy. This article focuses on the elective surgical setting and the recommended preoperative evaluation of patients who have been diagnosed with colorectal cancer.
History and physical The surgeon should perform a thorough history and physical examination on all patients with colorectal cancer. First, the patient must be deemed fit for surgery. Guidelines have been established to assess the cardiovascular risk of any patient undergoing a non-cardiac surgery [1]. These guidelines can help to optimize patients for surgery and can help identify patients who are at such high risk for surgery that alternatives to standard surgical practices must be considered. In the extreme case, this might mean no * Corresponding author. E-mail address: [email protected] (S.G. Gregorcyk). 1055-3207/06/$ - see front matter Ó 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.soc.2005.10.002 surgonc.theclinics.com
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surgery at all. For a patient who has rectal cancer, chemoradiation alone might be considered. In other instances, it might mean a more limited resection to shorten operative time and stress on the patient. In addition to determining fitness for surgery, the history and physical exam can provide data that will guide therapy. Directed questions about symptoms of obstruction or weight loss can yield information about the extent of the tumor. A patient who has a partially obstructed bowel may not tolerate a standard bowel preparation and may require a slower preparation. Significant weight loss that is not attributable to obstruction may be caused by metastatic disease. These patients may have nutritional deficits, which if repleted, will aid in recovery from surgery. The surgeon should inquire about and document continence status. This is pertinent when dealing with low rectal cancers because an anastomosis low in the pelvis will worsen tenuous bowel control and should be avoided. Continence must also be considered if an extended resection, such as a total colectomy, is planned. If the patient has poor sphincter function, the diarrhea resulting from a total colectomy may have a profound impact on the patient’s quality of life and a segmental resection may be the better choice. The patient’s family history as well as the patient’s own personal history may lead to concerns for a hereditary syndrome. Hereditary non-polyposis colorectal cancer syndrome and familial adenomatous polyposis are important to recognize preoperatively because they require more extensive surgeries than sporadic colon cancers. In addition to assessing a patient’s fitness, a physical examination should focus on discovering metastases as well as revealing technical considerations that may alter surgical plans. For instance, a bulky fixed tumor mass may preclude a laparoscopic approach. Jaundice or a right upper quadrant mass may be signs of extensive metastatic liver disease. A digital rectal examination is critical when evaluating a patient with rectal cancer. For palpable tumors, it is necessary to assess whether the tumor is fixed or mobile and if it invades into other structures such as the vagina or prostate. Also, the surgeon needs to assess the distance of the tumor from the anal verge and whether there is sphincter involvement. Obviously the functional status of the sphincters is very important and tone and squeeze should be documented. All of these findings are essential to determine if the patient is a candidate for sphincter preserving surgery. In cases of colon cancer, the digital rectal exam assesses the sphincter function, but also may reveal signs of extensive disease such as a Blummer’s shelf. Age-appropriate cancer screening should be up-to-date for all patients. Females should have annual mammograms starting at age 40. Females in reproductive years who have been sexually active should have Pap smears at least every 3 years. Males over age 50 should receive prostate screening [2]. Discretionary imaging and laboratory testing based on history and physical exam findings is always appropriate; however, the remainder of this article will focus on the routine screening modalities. Colon cancer and rectal
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cancer require different preoperative evaluation strategies. Although the upper rectal cancers are typically treated the same as colon cancers, the mid and lower rectal cancers are not and may require preoperative chemoradiation and sphincter preservation when possible. For these reasons, the preoperative evaluation for rectal cancer is typically more extensive and differences will be highlighted. Colonoscopy Colonoscopy is routine in the preoperative evaluation of patients with colon or rectal cancer. The study provides valuable information about the tumor, including location and characteristics that might affect the patient’s treatment. For example, if the tumor is large, bulky, and nearly obstructing, more extensive evaluation might be needed to plan the patient’s surgery. In the case of rectal cancer, preoperative chemoradiation would be indicated. In addition to assessing the tumor, additional lesions in the colon must be ruled out. According to some literature, the incidence of synchronous polyps in patients who have colorectal cancer is 24%–57%, depending on the size and histology of the primary lesion [3–8]. Other, more conservative reports quote the incidence of synchronous polyps to be only 10% [9]. The incidence of synchronous cancers is reported to be about 4% [7,10,11]. In one prospective study, findings on preoperative colonic evaluation resulted in a change of management in 3% of their patients [7]. Given these statistics, complete evaluation of the colon in all patients with colonic neoplasm is indicated. If the size and bulk of the tumor prevents proximal evaluation of the colon, a contrast study or CT colography may be an alternate option. Otherwise, the remainder of the colon can be evaluated intraoperatively with an on-table colonoscopy, or postoperatively within 6 months of surgery. When considering a laparoscopic approach to colon cancer surgery, accurate localization of the tumor is imperative to avoid removal of the wrong segment of intestine [12]. Colonoscopic localization simply by noting the proximity of the tumor to an unmistakable landmark is only accurate when dealing with the rectum or cecum. Otherwise, localization can be accomplished by endoscopic injection of India ink in three quadrants of bowel adjacent and distal to, but not through, the tumor, or by endoscopic placement of clips and subsequent plain film of the abdomen. Alternatively, barium enema or CT colography can be used. Rigid proctoscopy Because of the flexible nature of the colonoscope, the distance of the tumor from the anal verge cannot be accurately measured on colonoscopy. When the tumor is obviously within the colon or is palpable within the rectum, this limitation of the colonoscope is not an issue. Commonly, a tumor
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reported to be in the sigmoid colon by colonoscopy is actually much lower and represents rectal cancer. A rigid proctoscope is very useful for accurately measuring the distance of the tumor from the anal verge which not only helps in planning surgery, but also determines if the tumor is in a location where it might warrant preoperative neoadjuvant therapy. Chest radiography Whether performed as part of the evaluation for determining operative risk or to screen for lung metastases, which occur in 10%–20% of patients, chest radiography has become a standard part of the preoperative evaluation for colorectal cancer. CT scan of the chest offers no apparent benefit over a chest radiograph even in patients with known extracolonic metastases [13]. Laboratory Elevated serum carcinoembryonic antigen (CEA) levels O 5.0 ng/mL have been shown to have an adverse impact on survival, independent of tumor stage [14–22]. Despite the fact that a CEA level will not alter initial therapy, many doctors recommend that this test be performed for prognostic purposes and as a baseline for postoperative surveillance [23,24]. It is reasonable to obtain a preoperative baseline CEA in patients who will undergo postoperative surveillance. Patients with an elevated level of the protein CA19-9 in stage II of colorectal cancer have been shown to have a significantly poorer prognosis than those with normal levels, which leads some doctors to recommend this test for prognostic purposes [25,26]. Preoperative hypoalbuminema, defined as levels ! 3.5 g/dL, has been shown to be an independent predictor of surgical morbidity and mortality in general, and colorectal surgical populations more specifically [27,28]. Debilitated patients and those at risk for protein-calorie malnutrition or depleted visceral protein stores may benefit from nutritional assessment and enteral or parenteral nutritional supplementation before elective surgery. Basic hematology, liver function, and chemistry panels are used as appropriate for age and preexisting medical conditions. Liver function tests have poor sensitivity and specificity for detecting liver metastasis and are not routinely indicated. Serum potassium and hemoglobin levels are clinically relevant values in the postoperative period [29]. A preoperative baseline for these values may therefore prove helpful. In addition, because colorectal cancer can cause anemia, a preoperative hemoglobin screen can help plan for a possible need for blood products. Abdominal CT scan CT scan of the abdomen and pelvis in patients with colorectal cancer has been used with varying degrees of success to determine the extent of the
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primary tumor, the presence of lymph node involvement, and presence of liver metastases. It is important to obtain this information preoperatively for patients who have rectal cancer. Locally advanced stage II and stage III rectal cancers are candidates for neoadjuvant chemoradiation before surgery. CT scanning can be helpful with this staging. The highest reported sensitivity of a CT scan in imaging lymphadenopathy is 73%; specifity is 58% [30,31]. CT scans have been reported to correctly classify the T (tumor size) and N (node involvement) categories of cancer in 81% and 67.6% of cases respectively [32]. Endorectal ultrasound [33] and MRI with endorectal coil (discussed hereafter) are both more sensitive and specific than CT scan for detecting mesenteric lymphadenopathy in rectal cancer. In addition to local staging, the CT scan also assesses the liver. Although knowledge of liver disease does not usually alter the surgical approach for colon cancer, in patients who have rectal cancer, where the stakes of radical surgery are high, existence of liver metastases may influence management decisions. Furthermore, adequate staging mandates evaluation of the liver at the time of diagnosis and before neoadjuvant therapy. Contrast-enhanced CT scan of the abdomen is frequently used to evaluate the liver for metastatic disease in patients who have colorectal cancer. Sensitivity is between 73% and 79% for hepatic metastasis [29,34]. This sensitivity improves to 85% when CT scans are performed only when liver metastases are suspected based on laboratory or physical exam finding [35]. Sensitivities and specificities of 90% and 95% in detecting liver metastases O 1cm diameter have been reported [36]. Thus, the routine use of CT scan is advocated in the preoperative evaluation of patients with rectal cancer. The need for a CT scan preoperatively for colon cancer is not as compelling as that for rectal cancer. Lymphadenopathy does not change the need or timing of surgery. Liver metastases may result in a shorter segment of colon being resected but that is a decision that can be made intraoperatively after the metastases have been found on palpation or intraoperative ultrasound. Its use as a baseline scan is questionable because there will be changes on the scan after surgery, so future scans may be difficult to compare with a preoperative scan. Nevertheless, some doctors advocate a routine preoperative CT scan for colon cancer. Kerner and coworkers [37] evaluated 158 patients who had colon cancer, and found 120 otherwise unknown findings in 88 patients by using a preoperative CT scan. Thirty-five percent of those findings were believed to be clinically significant. McAndrew and Saba [32] reviewed their experience and found that CT scans resulted in an altered surgical approach for ! 2% of their patients. Thus, the need for a routine preoperative CT scan in cases of uncomplicated colon cancer remains controversial [38]. Although readily available and reasonably accurate, there is a paucity of evidence that supports this as a cost-effective screening modality [39]. The American Society of Colon and Rectal Surgeons Standards Practice Task Force does not promote routine preoperative CT scanning in colon cancer patients but does advocate it in selected patients [40].
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Most surgeons agree that adequate staging mandates evaluation of the liver either before or at the time of surgery. Intraoperative palpation of the liver satisfies this requirement. However, laparoscopy has made palpation of the liver a practical impossibility. An alternative to palpation is the use of intraoperative ultrasound [41]. If the surgeon is not proficient at laparoscopic ultrasound of the liver, then the liver should be assessed by other means and a preoperative CT scan is a reasonable choice. Palpable masses or near obstructing tumors on colonoscopy are concerning for advanced, bulky disease that may be invading other organs. A CT scan can help the surgeon delineate the extent of the tumor and plan the operative approach.
Ultrasound Intraoperative liver ultrasound performed either open or laparoscopically, is accurate in detecting liver metastasis [39,42]. It is, however, time consuming and operator dependent. Surgeon experience and preference determines the role of the imaging modality. Endorectal ultrasound has become the standard of care for staging rectal cancers. It is critical to accurately determine the T and N stage of rectal cancers so that patients with transmural disease (see Fig. 1) or nodal disease can be offered preoperative chemoradiation. The accuracy of endorectal ultrasound for staging rectal cancers is reported to be 75%–94%; the accuracy of the T stage is reported to be 69%–94.8% and the N stage is reported as 58%–83% [43–47]. Success of this technique is operator dependant [46,48] and may be limited by tumor or patient factors. Three-dimensional ultrasound is now available and although experience is limited, technical advantages over standard processing include the ability to review images in a ‘‘real-time’’ mode but at a later date.
Fig. 1. Endorectal ultrasound of rectal cancer, which is seen on the left side of the picture. The tumor invades through the muscularis propria into the perirectal fat and is a T3 lesion.
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MRI MRI of the liver is useful to better define suspicious liver lesions discovered by other imaging modalities. It is generally not used as a primary screening modality. MRI can be used for the local staging of rectal cancers. With the use of endorectal coils, MRI has a reported accuracy of 72%–100% in tumor staging [49–51]. When endorectal surface coil magnetic resonance imaging and endorectal ultrasound were compared head-to-head, there was no difference in T-staging between the two modalities, but MRI more accurately identified nodal involvement [52]. Whether this slight advantage justifies the increased cost and inconvenience is not well defined. The authors prefer endorectal ultrasound as a primary modality and use of MRI when ultrasound cannot be performed, is limited because of patient or tumor factors, or when invasion of other structures needs to be further defined. Positron emission tomography Positron Emission Tomography (PET) takes advantage of increased metabolic activity associated with malignancy or inflammation by detecting increased uptake of radiolabeled flourodeoxyglucose (FDG). Although highly sensitive for detecting carcinoma and metastases, its low specificity (43%) [53,54] limits the use of FDG-PET as a primary tool for preoperative assessment. Hybrid PET-CT may improve staging accuracy. An evolving technology, FDG-PET is most promising in the postoperative arena for primary surveillance or as a secondary imaging technique, accuracy is reported to be 93% [55]. There is not a reported indication for PET scan in the routine preoperative assessment of colorectal cancer. Bowel preparation Although mechanical bowel preparation (MBP) is recommended by most experts [56], a number of published studies challenge this approach. Prospective randomized trials comparing MBP and no MBP have demonstrated no difference in rate of wound infection, anastomotic leak, or development of intra-abdominal abscess [57–61]. Some authors have even demonstrated higher wound infection rates in patients who had MBP [62]. One explanation for this phenomenon is that liquid stool remaining after MBP is more susceptible to spillage than solid stool [63]. Additionally, extra-abdominal morbidity may be less without MBP because of the complications associated with preparation [64]. Despite this evidence, surgeons have been reluctant to adopt the protocol of colon resection without mechanical cleansing of the bowel. Most cite technical considerations and obvious distaste for manipulating stool, and point out that all of the aforementioned studies lack statistical power.
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Table 1 Recommendations for preoperative evaluation of patients with colorectal cancer Cancer Evaluation method History and physical Family history Colonoscopy Proctoscopy Basic lab Liver function tests CEA Chest radiography Abdominal CT scan Endoscopic ultrasound MRI PET scan a b c
Colon a
Yes Yes Yes Nob Yes Selectivec Yes Yes Selective No No No
Rectal Yes Yes Yes Yes Yes Selective Yes Yes Yes Yes Selective No
Comments Genetic counseling and testing as appropriate
As indicated from history or physical Baseline for follow-up if desired Evaluate liver prior to laparoscopy Clarification of other findings Major role is follow-up
Yes: the preponderance of data or expert opinion support routine use of these modalities. No: studies are not indicated. Selective: use of method is discretionary, based on individual clinical scenario.
Technical considerations of laparoscopic colon surgery make extrapolation of these data to the laparoscopic arena difficult. Laparoscopically manipulating a colon that is filled with stool is more difficult than a prepped colon, and to our knowledge, no studies of bowel preparation have included patients undergoing laparoscopy. We feel omission of the routine MBP deserves serious consideration but further research is necessary to conclude it equal or superior to MBP. The authors employ laparoscopic techniques whenever possible and currently prescribe mechanical bowel preparation before elective surgery. The use of prophylactic perioperative antibiotics is scientifically well supported and recommended [65]. Conclusions The preoperative evaluation of patients who have colorectal cancer will vary based on the type of cancer and on results of the history and physical examination. Routine screening for all patients is summarized in Table 1 and should include evaluation of the entire colon, a chest radiograph, and standard labs including a CEA if postoperative surveillance is planned. For rectal cancer patients, endorectal ultrasound is the preferred method of preoperative local staging. MRI with an endorectal coil can be used when ultrasound cannot be performed, is limited because of patient or tumor factors, or when invasion of other structures needs further delineation. A CT scan is also recommended preoperatively in all rectal cancer patients to further assess the local disease and also to determine if metastases are present, because that finding could alter surgical plans.
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Evaluation of the liver is important for staging colon cancer but may be accomplished intraoperatively by palpation and inspection or by ultrasound. If these are not possible, then a CT scan preoperatively is recommended and is the most widely used imaging technique. MRI is a useful adjunct to better define suspicious lesions but is not routinely used in the preoperative setting. References [1] Mukherjee D, Eagle KA. Perioperative cardiac assessment for non-cardiac surgery: eight steps to the best possible outcome. Circulation 2003;107:2771–4. [2] Smith RA, Cokkinides V, Eyre HJ. American Cancer Society guidelines for the early detection of cancer, 2005. CA Cancer J Clin 2005;55(1):31–44. [3] Opelka FG, Timmcke AE, Gathright JB Jr, et al. Diminutive colonic polyps: an indication for colonoscopy. Dis Colon Rectum 1992;35:178–81. [4] Read TE, Read JD, Butterly LF. Importance of adenomas 5 mm or less in diameter that are detected by sigmoidoscopy. N Engl J Med 1997;336:8–12. [5] Demetriades H, Kanellos I, Blouhos K, et al. Synchronous polyps in patients with colorectal cancer. Tech Coloproctol 2004;8(Suppl 1):S72–5. [6] McGarrity TJ, Bhatti AM, Peters DJ, et al. Synchronous proximal polyps and cancer in patients with polyps detected at sigmoidoscopy: results of a single, rural-based sigmoidoscopy clinic. Dig Dis Sci 2002;47(2):309–16. [7] Arenas RB, Fichera A, Mhoon D, et al. Incidence and therapeutic implications of synchronous colonic pathology in colorectal adenocarcinoma. Surgery 1997;122(4):706–9. [8] Place RJ, Simmang CL. Hyperplastic-adenomatous polyposis syndrome. J Am Coll Surg 1999;188(5):503–7. [9] Northover JM. Staging and management of colorectal cancer. World J Surg 1997;21:672–7. [10] Papadopoulos V, Michalopoulos A, Basdanis G, et al. Synchronous and metachronous colorectal carcinoma. Tech Coloproctol 2004;8(Suppl 1):S97–100. [11] Oya M, Takahashi S, Okuyama T, et al. Synchronous colorectal carcinoma: clinico-pathological features and prognosis. Jpn J Clin Oncol 2003;33(1):38–43. [12] Larach SW, Patankar SK, Ferrara A, et al. Complications of laparoscopic colorectal surgery: analysis and comparison of early vs latter experience. Dis Colon Rectum 1997;40: 592–6. [13] Povoski SP, Fong Y, Sgouros SC, et al. Role of chest CT in patients with negative chest xrays referred for hepatic colorectal metastases. Ann Surg Oncol 1998;5(1):9–15. [14] Wanebo HJ, Rao B, Pinsky CM, et al. Preoperative carcinoembryonic antigen level as a prognostic indicator in colorectal cancer. N Engl J Med 1978;299:448–51. [15] Wolmark N, Fisher B, Wieand HS, et al. The significance of preoperative carcinoembryonic antigen levels in colorectal cancer. Ann Surg 1984;199:375–82. [16] Onetto M, Paganuzzi M, Secco GB, et al. Preoperative carcinoembryonic antigen and prognosis in patients with colorectal cancer. Biomed Pharmacother 1985;39:392–5. [17] Scott NA, Wieand HS, Moertel CG, et al. Colorectal cancer. Dukes’ stage, tumor site, preoperative plasma CEA level, and patient prognosis related to tumor DNA ploidy pattern. Arch Surg 1987;122:1375–9. [18] Wiggers T, Arends J, Volovics A. Regression analysis of prognostic factors in colorectal cancer after curative resections. Dis Colon Rectum 1988;31:33–41. [19] Meling GI, Rognum TO, Clausen OPF, et al. Serum carcinoembryonic antigen in relation to survival, DNA ploidy pattern, and recurrent disease in 406 colorectal carcinoma patients. Scand J Gastroenterol 1992;27:1061–8. [20] Slenz K, Senagore A, Hibbert J, et al. Can preoperative and postoperative CEA predict survival after colon cancer resection? Am Surg 1994;60:528–32.
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