Annals of Surgical Oncology

, Volume 16, Issue 2, pp 254–265 | Cite as

How Good is Endoscopic Ultrasound in Differentiating Various T Stages of Rectal Cancer? Meta-Analysis and Systematic Review

  • Srinivas R. Puli
  • Matthew L. Bechtold
  • Jyotsna B. K. Reddy
  • Abhishek Choudhary
  • Mainor R. Antillon
  • William R. Brugge
Healthcare Policy and Outcomes


Published data on accuracy of endoscopic ultrasound (EUS) in differentiating T stages of rectal cancers is varied. Study selection criteria were to select only EUS studies confirmed with results of surgical pathology. Articles were searched in Medline and Pubmed. Pooling was conducted by both fixed and random effects models. Initial search identified 3,630 reference articles, of which 42 studies (N = 5,039) met the inclusion criteria and were included in this analysis. The pooled sensitivity and specificity of EUS to determine T1 stage was 87.8% [95% confidence interval (CI) 85.3–90.0%] and 98.3% (95% CI 97.8–98.7%), respectively. For T2 stage, EUS had a pooled sensitivity and specificity of 80.5% (95% CI 77.9–82.9%) and 95.6% (95% CI 94.9–96.3%), respectively. To stage T3 stage, EUS had a pooled sensitivity and specificity of 96.4% (95% CI 95.4–97.2%) and 90.6% (95% CI 89.5–91.7%), respectively. In determining the T4 stage, EUS had a pooled sensitivity of 95.4% (95% CI 92.4–97.5%) and specificity of 98.3% (95% CI 97.8–98.7%). The p value for chi-squared heterogeneity for all the pooled accuracy estimates was > 0.10. We conclude that, as a result of the demonstrated sensitivity and specificity, EUS should be the investigation of choice to T stage rectal cancers. The sensitivity of EUS is higher for advanced disease than for early disease. EUS should be strongly considered for T staging of rectal cancers.


Rectal Cancer Negative Likelihood Ratio Positive Likelihood Ratio Diagnostic Odds Ratio Pool Sensitivity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin. 2007;57(1):43–66.PubMedGoogle Scholar
  2. 2.
    National Cancer Institute. Surveillance epidemiology and end results (SEER). U.S. National Institutes of Health. Accessed June 2008.
  3. 3.
    Atkin WS, Morson BC, Cuzick J. Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med. 1992;326(10):658–62.PubMedGoogle Scholar
  4. 4.
    Larsson SC, Orsini N, Wolk A. Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst. 2005;97(22):1679–87.PubMedCrossRefGoogle Scholar
  5. 5.
    Giovannucci E, Ascherio A, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Physical activity, obesity, and risk for colon cancer and adenoma in men. Ann Intern Med. 1995;122(5):327–34.PubMedGoogle Scholar
  6. 6.
    Cho E, Smith-Warner SA, Ritz J, van den Brandt PA, Colditz GA, Folsom AR, et al. Alcohol intake and colorectal cancer: a pooled analysis of 8 cohort studies. Ann Intern Med. 2004;140(8):603–13.Google Scholar
  7. 7.
    Paskett ED, Reeves KW, Rohan TE, Allison MA, Williams CD, Messina CR, et al. Association between cigarette smoking and colorectal cancer in the Women’s Health Initiative. J Natl Cancer Inst. 2007;99(22):1729–35.PubMedCrossRefGoogle Scholar
  8. 8.
    Greene FL, Page DL, Fleming ID, Fritz A, Balch CM, Haller DG, et al. AJCC cancer staging manual (6th ed). New York: Springer-Verlag; 2002.Google Scholar
  9. 9.
    Rich T, Gunderson LL, Lew R, Galdibini JJ, Cohen AM, Donaldson G. Patterns of recurrence of rectal cancer after potentially curative surgery. Cancer. 1983;52(7):1317–29.PubMedCrossRefGoogle Scholar
  10. 10.
    Minsky BD, Mies C, Recht A, Rich TA, Chaffey JT. Resectable adenocarcinoma of the rectosigmoid and rectum: patterns of failure and survival. Cancer. 1988;61(7):1408–16.PubMedCrossRefGoogle Scholar
  11. 11.
    Willett CG, Lewandrowski K, Donelly S, Shellito PC, Convery K, Eliseo R, et al. Are there patients with stage I rectal carcinoma at risk for failure after abdominoperineal resection? Cancer. 1992;69(7):1651–5.PubMedCrossRefGoogle Scholar
  12. 12.
    Bailey HR, Huval WV, Max E, Smith KW, Butts DR, Zamora LF. Local excision of carcinoma of the rectum for cure. Surgery. 1992;111(5):555–61.PubMedGoogle Scholar
  13. 13.
    Kodner IJ, Gilley MT, Shemesh EI, Fleshman JW, Fry RD, Myerson RJ. Radiation therapy as definitive treatment for selected invasive rectal cancer. Surgery. 1993;114(4):850–6.PubMedGoogle Scholar
  14. 14.
    Mendenhall WM, Rout WR, Vauthey JN, Haigh LS, Zlotecki RA, Copeland EM 3rd. Conservative treatment of rectal adenocarcinoma with endocavitary irradiation or wide local excision and postoperative irradiation. J Clin Oncol. 1997;15(10):3241–8.PubMedGoogle Scholar
  15. 15.
    Maingon P, Guerif S, Darsouni R, Salas S, Barillot I, d’Hombres A, et al. Conservative management of rectal adenocarcinoma by radiotherapy. Int J Radiat Oncol Biol Phys. 1998;40(5):1077–85.PubMedGoogle Scholar
  16. 16.
    Sleisenger & Fortran’s gastrointestinal and liver disease, 8th ed. Saunders, 2006.Google Scholar
  17. 17.
    Krook JE, Moertel CG, Gunderson LL, Wieand HS, Collins RT, Beart RW, et al. Effective adjuvant therapy for high-risk rectal carcinoma. N Engl J Med. 1991;324:709.PubMedGoogle Scholar
  18. 18.
    Videtic GM, Fisher BJ, Perera FE, et al. Preoperative radiation with concurrent 5-fluorouracil continuous infusion for locally advanced unresectable rectal cancer. Int J Radiat Oncol Biol Phys. 1998; 42:319.PubMedGoogle Scholar
  19. 19.
    Guinet C, Buy JN, Ghossain MA, Sezeur A, Mallet A, Bigot JM, et al. Comparison of magnetic resonance imaging and computed tomography in the preoperative staging of rectal cancer. Arch Surg. 1990;125(3):385–8.PubMedGoogle Scholar
  20. 20.
    Rifkin MD, Ehrlich SM, Marks G. Staging of rectal carcinoma: prospective comparison of endorectal US and CT. Radiology. 1989;170(2):319–22.PubMedGoogle Scholar
  21. 21.
    Hildebrandt U, Klein T, Feifel G, Schwarz HP, Koch B, Schmitt RM. Endosonography of pararectal lymph nodes In vitro and in vivo evaluation. Dis Colon Rectum. 1990;33(10):863–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Tio TL, Coene PP, van Delden OM, Tytgat GN. Colorectal carcinoma: preoperative TNM classification with endosonography. Radiology 1991;179(1):165–70.PubMedGoogle Scholar
  23. 23.
    Kwok H, Bissett IP, Hill GL. Preoperative staging of rectal cancer. Int J Colorectal Dis. 2000;15(1):9–20.PubMedCrossRefGoogle Scholar
  24. 24.
    Thaler W, Watzka S, Martin F, La Guardia G, Psenner K, Bonatti G, et al. Preoperative staging of rectal cancer by endoluminal ultrasound vs magnetic resonance imaging Preliminary results of a prospective, comparative study. Dis Colon Rectum. 1994;37(12):1189–93.PubMedCrossRefGoogle Scholar
  25. 25.
    Meyenberger C, Huch Boni RA, Bertschinger P, Zala GF, Klotz HP, Krestin GP. Endoscopic ultrasound and endorectal magnetic resonance imaging: a prospective, comparative study for preoperative staging and follow-up of rectal cancer. Endoscopy. 1995;27(7):469–79.PubMedCrossRefGoogle Scholar
  26. 26.
    Harewood GC, Wiersema MJ, Nelson H, Maccarty RL, Olson JE, Clain JE, et al. A prospective, blinded assessment of the impact of preoperative staging on the management of rectal cancer. Gastroenterology. 2002;123(1):24–32.PubMedCrossRefGoogle Scholar
  27. 27.
    Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF, for the QUOROM Group. Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Lancet. 1999;354:1896–1900.Google Scholar
  28. 28.
    Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, et al. Standards for reporting of diagnostic accuracy group Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative The Standards for Reporting of Diagnostic Accuracy Group. Croatian Med J. 2003;44(5):635–8.Google Scholar
  29. 29.
    Brennan P, Silman A. Statistical methods for assessing observer variability in clinical measures. BMJ. 1992;304:1491–4.PubMedCrossRefGoogle Scholar
  30. 30.
    Jadad AR, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Controlled Clin Trials. 1996;17:1–12.PubMedCrossRefGoogle Scholar
  31. 31.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting Meta-analysis of observational studies in Epidemiology (MOOSE) group. JAMA 2000;283(15):2008–12.PubMedCrossRefGoogle Scholar
  32. 32.
    Whiting P, Rutjes AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:25.PubMedCrossRefGoogle Scholar
  33. 33.
    Whiting PF, Weswood ME, Rutjes AW, et al. Evaluation of QUADAS, a tool for the quality assessment of diagnostic accuracy studies. BMC Med Res Methodol. 2006;6:9.PubMedCrossRefGoogle Scholar
  34. 34.
    Puli SR, Singh S, Hagedorn CH, Reddy J, Olyaee M. Diagnostic accuracy of EUS for vascular invasion in pancreatic and periampullary cancers: a meta-analysis and systematic review. Gastrointest Endosc. 2007;65(6):788–97.PubMedCrossRefGoogle Scholar
  35. 35.
    Puli SR, BK Reddy J, Bechtold ML, Antillon M, Ibdah JA. How good is endoscopic ultrasound for TNM staging of gastric cancers? A meta-analysis and systematic review. World J Gastroenterol. 2008;14(25):4011–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Puli SR, BK Reddy J, Bechtold ML, Ibdah JA, Antillon M. Staging accuracy of esophageal cancer by endoscopic ultrasound: a meta-analysis and systematic review. World J Gastroenterol. 2008;14(10):1479–90.PubMedCrossRefGoogle Scholar
  37. 37.
    Leemis LM, Trivedi KS. A comparison of approximate interval estimators for the Bernoulli parameter. Am Stat. 1996;50:63–8.CrossRefGoogle Scholar
  38. 38.
    Cox DR. The analysis of binary data. London: Methuen; 1970.Google Scholar
  39. 39.
    Agresti A. Analysis of ordinal categorical data. New York: Wiley; 1984.Google Scholar
  40. 40.
    Deeks JJ. Systematic reviews of evaluations of diagnostic and screening tests. In: Egger M, Smith GD, Altman DG, editors. Systematic Reviews in Health Care Meta-analysis in context. London: BMJ Books; 2001.Google Scholar
  41. 41.
    Harbord RM, Egger M, Sterne JAC. A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med. 2005;25(20):3443–57.CrossRefGoogle Scholar
  42. 42.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.PubMedCrossRefGoogle Scholar
  43. 43.
    Sterne JAC, Egger M, Davey-Smith G. Investigating and dealing with publication and other biases in meta-analysis. BMJ. 2001;323: 101–5.PubMedCrossRefGoogle Scholar
  44. 44.
    Sterne JAC, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol. 2001;54: 1046–55.PubMedCrossRefGoogle Scholar
  45. 45.
    Saitoh N, Okui K, Sarashina H, Suzuki M, et al. Evaluation of echographic diagnosis of rectal cancer using intrarectal ultrasonic examination. Dis Colon Rectum. 1986;29(4):234–42.PubMedCrossRefGoogle Scholar
  46. 46.
    Waizer A Zitron S, Ben-Baruch D, Baniel J, Wolloch Y, Dintsman M. Comparative study for preoperative staging of rectal cancer. Dis Colon Rectum. 1989;32(1):53–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Bali C, Nousias V, Fatouros M, Stefanou D, Kappas AM. Assessment of local stage in rectal cancer using endorectal ultrasonography (EUS). Tech Coloproctol. 2004;8(Suppl 1):S170–3.PubMedCrossRefGoogle Scholar
  48. 48.
    AP Zbar. Endorectal ultrasonography in rectal cancer: a preliminary Barbadian experience. West Indian Med J. 2006;55(5).Google Scholar
  49. 49.
    Sailer M, Leppert R, Kraemer M, et al. The value of endorectal ultrasound in the assessment of adenomas, T1- and T2-carcinomas. Int J Colorectal Dis. 1997;12(4):214–9. 10.1007/s003840050092.Google Scholar
  50. 50.
    Glaser F, Kuntz C, Schlag P, et al. Endorectal ultrasound for control of preoperative radiotherapy of rectal cancer. Ann Surg. 1993;217(1):64–71.PubMedCrossRefGoogle Scholar
  51. 51.
    Maor Y, Nadler M, Barshack I, et al. Endoscopic ultrasound staging of rectal cancer: diagnostic value before and following chemoradiation. J Gastroenterol Hepatol. 2006;21:454–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Kim JC, Kim HC, Yu CS, et al. Efficacy of 3-dimensional endorectal ultrasonography compared with conventional ultrasonography and computed tomography in preoperative rectal cancer staging. Am J Surg. 2006;192:89–97.PubMedCrossRefGoogle Scholar
  53. 53.
    AkasuT, KondoH, MoriyaY, et al. Endorectal ultrasonography and treatment of early stage rectal cancer. World J Surg. 2000;24(9):1061–8. 10.1007/s002680010151.Google Scholar
  54. 54.
    Norton SA, Thomas MG. Staging of rectosigmoid neoplasia with colonoscopic endoluminal ultrasonography. Brit J Surg. 1999;86(7):942–6.PubMedCrossRefGoogle Scholar
  55. 55.
    Kaneko K, Boku N, Hosokawa K, et al. Diagnostic utility of endoscopic ultrasonography for preoperative rectal cancer staging estimation. Japan J Clin Oncol. 1996;26(1):30–5.Google Scholar
  56. 56.
    Adams DR, Blatchford GJ, Lin KM, et al. Use of preoperative ultrasound staging for treatment of rectal cancer. Dis Colon Rectum. 1999;42(2):159–66.PubMedCrossRefGoogle Scholar
  57. 57.
    Gualdi GF, Casciani E, Guadalaxara A, et al. Local staging of rectal cancer with transrectal ultrasound and endorectal magnetic resonance imaging: comparison with histologic findings. Dis Colon Rectum. 2000;43(3):338–45.PubMedCrossRefGoogle Scholar
  58. 58.
    Hildebrandt U, Feifel G. Preoperative staging of rectal cancer by intrarectal ultrasound. Dis Colon Rectum. 1985;28(1):42–6.PubMedCrossRefGoogle Scholar
  59. 59.
    Mackay SG, Pager CK, Joseph D, et al. Assessment of the accuracy of transrectal ultrasonography in anorectal neoplasia. Br J Surg. 2003;90(3):346–50.PubMedCrossRefGoogle Scholar
  60. 60.
    Nishimori H, Sasaki K, Hirata K, et al. The value of endoscopic ultrasonography in preoperative evaluation of rectal cancer. Int Surg. 1998;83(2):157–60.PubMedGoogle Scholar
  61. 61.
    Marone P, Petrulio F, de Bellis M, et al. Role of endoscopic ultrasonography in the staging of rectal cancer: a retrospective study of 63 patients. J Clin Gastroenterol. 2000;30(4):420–4.PubMedCrossRefGoogle Scholar
  62. 62.
    Hsieh PS, Changchien CR, Chen JS, et al. Comparing results of preoperative staging of rectal tumor using endorectal ultrasonography and histopathology. Chang Gung Medical J. 2003;26(7):474–8.Google Scholar
  63. 63.
    Kramann B, Hildebrandt U. Computed tomography versus endosonography in the staging of rectal carcinoma: a comparative study. Int J Colorectal Dis. 1986;1(4):216–8.PubMedCrossRefGoogle Scholar
  64. 64.
    Massari M, De Simone M, Cioffi U, et al. Value and limits of endorectal ultrasonography for preoperative staging of rectal carcinoma. Surg Laparosc Endosc. 1998;8(6):438–44.PubMedCrossRefGoogle Scholar
  65. 65.
    Boyce GA, Sivak MV, Jr., Lavery IC, et al. Endoscopic ultrasound in the pre-operative staging of rectal carcinoma. Gastrointest Endosc. 1992;38(4):468–71.PubMedCrossRefGoogle Scholar
  66. 66.
    Pappalardo G, Reggio D, Frattaroli 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(4):219–22.PubMedCrossRefGoogle Scholar
  67. 67.
    Akasu T, Sugihara K, Moriya Y, et al. Limitations and pitfalls of transrectal ultrasonography for staging of rectal cancer. Dis Colon Rectum. 1997;40(Suppl 10):S10–5.PubMedCrossRefGoogle Scholar
  68. 68.
    Feifel G, Hildebrandt U, Dhom G. Assessment of depth of invasion in rectal cancer by endosonography. Endoscopy. 1987;19(2):64–7.PubMedCrossRefGoogle Scholar
  69. 69.
    Giovannini M, Bories E, Pesenti C, Moutardier V et al. Three- dimensional endorectal ultrasound using a new freehand software program: results in 35 patients with rectal cancer. Endoscopy. 2006;38(4):339–43.PubMedCrossRefGoogle Scholar
  70. 70.
    Marusch F, Koch A, Schmidt U, et al. Routine use of transrectal ultrasound in rectal carcinoma: Results of a prospective multicenter study. Endoscopy. 2002;34(5):385–90.PubMedCrossRefGoogle Scholar
  71. 71.
    Meyenberger C, Huch Boni RA, Bertschinger P, et al. Endoscopic ultrasound and endorectal magnetic resonance imaging: a prospective, comparative study for preoperative staging and follow-up of rectal cancer. Endoscopy. 1995;27(7):469–79.PubMedCrossRefGoogle Scholar
  72. 72.
    Thaler W, Watzka S, Martin F, et al. Preoperative staging of rectal cancer by endoluminal ultrasound vs magnetic resonance imaging Preliminary results of a prospective, comparative study. Dis Colon Rectum. 1994;37(12):1189–93.PubMedCrossRefGoogle Scholar
  73. 73.
    Waizer A, Powsner E, Russo I, et al. Prospective comparative study of magnetic resonance imaging versus transrectal ultrasound for preoperative staging and follow-up of rectal cancer Preliminary report. Dis Colon Rectum. 1991;34(12):1068–72.PubMedCrossRefGoogle Scholar
  74. 74.
    Herzog U, von FM, Tondelli P, Schuppisser JP. How accurate is endorectal ultrasound in the preoperative staging of rectal cancer? Dis Colon Rectum. 1993;36:127–34.PubMedCrossRefGoogle Scholar
  75. 75.
    Nielsen MB, Qvitzau S, Pedersen JF, et al. Endosonography for preoperative staging of rectal tumours. Acta Radiologica. 1996;37(5):799–803.PubMedCrossRefGoogle Scholar
  76. 76.
    Sentovich SM, Blatchford GJ, Falk PM, et al. Transrectal ultrasound of rectal tumors. Am J Surg. 1993;166(6):638–41 discussion 641–2.PubMedCrossRefGoogle Scholar
  77. 77.
    Romano G, de Rosa P, Vallone G, et al. Intrarectal ultrasound and computed tomography in the pre- and postoperative assessment of patients with rectal cancer. Br J Surg. 1985;72(Suppl):S117–9.PubMedCrossRefGoogle Scholar
  78. 78.
    Bianchi P, Ceriani C, Palmisano A, Pompili G, Passoni GR, Rottoli M, et al. A prospective comparison of endorectal ultrasound and pelvic magnetic resonance in the preoperative staging of rectal cancer. Ann Ital Chir. 2006;77:41–6.PubMedGoogle Scholar
  79. 79.
    Ramana KN, Murthy PV, Rao KP, et al. Transrectal ultrasonography versus computed tomography in staging rectal carcinoma. Indian J Gastroenterol. 1997;16(4):142–3.PubMedGoogle Scholar
  80. 80.
    Garcia-Aguilar J, Pollack J, Lee SH, Hernandez de Anda E, Mellgren A, Wong WD, et al. Accuracy of endorectal ultrasonography in preoperative staging of rectal tumors. Dis Colon Rectum. 2002;45(1):10–5.PubMedCrossRefGoogle Scholar
  81. 81.
    Manger T, Stroh C. Accuracy of endorectal ultrasonography in the preoperative staging of rectal cancer. Tech Coloproctol. 2004;8(Suppl 1):s14–5.PubMedCrossRefGoogle Scholar
  82. 82.
    Starck M, Bohe M, Simanaitis M, Valentin L. Rectal endosonography can distinguish benign rectal lesions from invasive early rectal cancers. Colorectal Dis. 2003;5(3):246–50.PubMedCrossRefGoogle Scholar
  83. 83.
    Kim JC, Yu CS, Jung HY, Kim HC, Kim SY, Park SK, et al. Source of errors in the evaluation of early rectal cancer by endoluminal ultrasonography. Dis Colon Rectum. 2001;44(9):1302–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Osti MF, Padovan FS, Pirolli C, Sbarbati S, Tombolini V, Meli C, et al. Comparison between transrectal ultrasonography and computed tomography with rectal inflation of gas in preoperative staging of lower rectal cancer. Eur Radiol. 1997;7(1):26–30.PubMedCrossRefGoogle Scholar
  85. 85.
    Caseiro-Alves F, Goncalo M, Cruz L, Ilharco J, Leite J, Agostinho A, et al. Water enema computed tomography (WE-CT) in the local staging of low colorectal neoplasms: Comparison with transrectal ultrasound. Abdominal Imag. 1998;23(4):370–4.CrossRefGoogle Scholar
  86. 86.
    Norton SA, Thomas MG. Staging of rectosigmoid neoplasia with colonoscopic endoluminal ultrasonography.Br J Surg. 1999;86(7): 942–6.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2008

Authors and Affiliations

  • Srinivas R. Puli
    • 1
    • 2
  • Matthew L. Bechtold
    • 1
  • Jyotsna B. K. Reddy
    • 1
  • Abhishek Choudhary
    • 1
  • Mainor R. Antillon
    • 1
  • William R. Brugge
    • 3
  1. 1.Division of Gastroenterology and HepatologyUniversity of Missouri-ColumbiaColumbiaUSA
  2. 2.Division of GastroenterologyCE443 Clinical Support & Education Five Hospital DriveColumbiaUSA
  3. 3.GI UnitMassachusetts General HospitalBostonUSA

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