Time Trends and Disparities in Lymphadenectomy for Gastrointestinal Cancer in the United States: A Population-Based Analysis of 326,243 Patients

Journal of Gastrointestinal Surgery

Volumn 17, Issue 4, 2013, Pages 611-619

  Dubecz, A ^a   Solymosi, N ^b   Schweigert, M ^a   Stadlhuber, R J ^a   Peters, J H ^c   Ofner, D ^d   Stein, H J ^a  

^a KLINIKUM NÜRNBERG   (Germany)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^d PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Adequate lymph node dissection; Disparities; Gastrointestinal carcinoma; Lymph node counts; Population based data

Indexed keywords

EID: 84875050127     PISSN: 1091255X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11605-013-2146-0     Document Type: Article

References (56)

1. Ruol A, Castoro C, Portale G, Cavallin F, Sileni VC, Cagol M, Alfieri R, Corti L, Boso C, Zaninotto G, Peracchia A, Ancona E. Trends in management and prognosis for esophageal cancer surgery: twenty-five years of experience at a single institution. Arch Surg. 2009 Mar; 144(3): 247-54.
2. Riall TS, Nealon WH, Goodwin JS, Zhang D, Kuo YF, Townsend CM Jr, Freeman JL. Pancreatic cancer in the general population: improvements in survival over the last decade. J Gastrointest Surg. 2006; 10(9): 1212-1223; discussion 1223-1224.
3. SSAT Patient Care Guidelines: Surgical Treatment of Gastric Cancer (2004). http://ssat. org. Accessed 13 May 2012.
4. Siewert JR, Böttcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg. 1998 Oct; 228(4): 449-61.
5. Kim JP, Lee JH, Kim SJ, Yu HJ, Yang HK. Clinicopathologic characteristics and prognostic factors in 10 783 patients with gastric cancer. Gastric Cancer. 1998 Mar; 1(2): 125-133.
6. Yeo CJ, Cameron JL, Lillemoe KD, Sohn TA, Campbell KA, Sauter PK, Coleman J, Abrams RA, Hruban RH. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Ann Surg. 2002; 236(3): 355-366; discussion 366-368.
7. Brennan MF, Kattan MW, Klimstra D, Conlon K. Prognostic nomogram for patients undergoing resection for adenocarcinoma of the pancreas. Ann Surg. 2004 Aug; 240(2): 293-8.
8. Le A, Berger D, Lau M, El-Serag HB. Secular trends in the use, quality, and outcomes of gastrectomy for noncardia gastric cancer in the United States. Ann Surg Oncol. 2007 Sep; 14(9): 2519-27.
9. Hellan M, Sun CL, Artinyan A, Mojica-Manosa P, Bhatia S, Ellenhorn JD, Kim J. The impact of lymph node number on survival in patients with lymph node-negative pancreatic cancer. Pancreas. 2008 Jul; 37(1): 19-24.
10. Greenstein AJ, Litle VR, Swanson SJ, Divino CM, Packer S, Wisnivesky JP. Effect of the number of lymph nodes sampled on postoperative survival of lymph node-negative esophageal cancer. Cancer. 2008 Mar 15; 112(6): 1239-46.
11. Parsons HM, Tuttle TM, Kuntz KM, Begun JW, McGovern PM, Virnig BA. Association between lymph node evaluation for colon cancer and node positivity over the past 20 years. JAMA. 2011 Sep 14; 306(10): 1089-97.
12. Bilimoria KY, Talamonti MS, Wayne JD, Tomlinson JS, Stewart AK, Winchester DP, Ko CY, Bentrem DJ. Effect of hospital type and volume on lymph node evaluation for gastric and pancreatic cancer. Arch Surg. 2008; 143(7): 671-678; discussion 678.
13. Singal V, Singal AK, Kuo YF. Racial disparities in treatment for pancreatic cancer and impact on survival: a population-based analysis. J Cancer Res Clin Oncol. 2012 Apr; 138(4): 715-22.
14. Paulson EC, Ra J, Armstrong K, Wirtalla C, Spitz F, Kelz RR. Underuse of esophagectomy as treatment for resectable esophageal cancer. Arch Surg. 2008 Dec; 143(12): 1198-203.
15. Bilimoria KY, Bentrem DJ, Ko CY, Stewart AK, Winchester DP, Talamonti MS. National failure to operate on early stage pancreatic cancer. Ann Surg. 2007 Aug; 246(2): 173-80.
16. Dubecz A, Sepesi B, Salvador R, Polomsky M, Watson TJ, Raymond DP, Jones CE, Litle VR, Wisnivesky JP, Peters JH. Surgical resection for locoregional esophageal cancer is underutilized in the United States. J Am Coll Surg. 2010; 211(6): 754-761.
17. Overview of the SEER Program. http://seer. cancer. gov/about/overview. html. Accessed on 13 May 2012.
18. Small Area Income and Poverty Estimates. http://www. census. gov/did/www/saipe/index. html. Accessed 14 April 2012.
19. NCCN Guidelines For Treatment Of Cancer By Site. http://www. nccn. org/professionals/physician_gls/f_guidelines. asp. Accessed 14 April 2012.
20. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2012. ISBN 3-900051-07-0. http://www. R-project. org/.
21. Stiles BM, Nasar A, Mirza FA, Lee PC, Paul S, Port JL, Altorki NK. Worldwide oesophageal cancer collaboration guidelines for lymphadenectomy predict survival following neoadjuvant therapy. Eur J Cardiothorac Surg. 2012 Oct; 42(4): 659-64.
22. Tsujinaka T, Sasako M, Yamamoto S, Sano T, Kurokawa Y, Nashimoto A, Kurita A, Katai H, Shimizu T, Furukawa H, Inoue S, Hiratsuka M, Kinoshita T, Arai K, Yamamura Y; Gastric Cancer Surgery Study Group of Japan Clinical Oncology Group. Influence of overweight on surgical complications for gastric cancer: results from a randomized control trial comparing D2 and extended para-aortic D3 lymphadenectomy (JCOG9501). Ann Surg Oncol. 2007; 14(2): 355-361.
23. Kunisaki C, Akiyama H, Nomura M, Matsuda G, Otsuka Y, Ono H, Nagahori Y, Hosoi H, Takahashi M, Kito F, Shimada H. Comparison of surgical results of D2 versus D3 gastrectomy (para-aortic lymph node dissection) for advanced gastric carcinoma: a multi-institutional study. Ann Surg Oncol. 2006; 13(5): 659-667.
24. Nimura Y, Nagino M, Takao S, Takada T, Miyazaki K, Kawarada Y, Miyagawa S, Yamaguchi A, Ishiyama S, Takeda Y, Sakoda K, Kinoshita T, Yasui K, Shimada H, Katoh H. Standard versus extended lymphadenectomy in radical pancreatoduodenectomy for ductal adenocarcinoma of the head of the pancreas: long-term results of a Japanese multicenter randomized controlled trial. J Hepatobiliary Pancreat Sci. 2012; 19(3): 230-241.
25. Period life table for the Social Security area population in 2007. http://www. ssa. gov/oact/STATS/table4c6. html. Accessed 14 May 2012.
26. Pultrum BB, Bosch DJ, Nijsten MW, Rodgers MG, Groen H, Slaets JP, Plukker JT. Extended esophagectomy in elderly patients with esophageal cancer: minor effect of age alone in determining the postoperative course and survival. Ann Surg Oncol. 2010 Jun; 17(6): 1572-80.
27. Zehetner J, Lipham JC, Ayazi S, Banki F, Oezcelik A, DeMeester SR, Hagen JA, DeMeester TR. Esophagectomy for cancer in octogenarians. Dis Esophagus. 2010 Nov; 23(8): 666-9.
28. Barbas AS, Turley RS, Ceppa EP, Reddy SK, Blazer DG 3rd, Clary BM, Pappas TN, Tyler DS, White RR, Lagoo SA. Comparison of outcomes and the use of multimodality therapy in young and elderly people undergoing surgical resection of pancreatic cancer. J Am Geriatr Soc. 2012 Feb; 60(2): 344-50.
29. Riall TS. What is the effect of age on pancreatic resection? Adv Surg. 2009; 43: 233-49.
30. Ward E, Jemal A, Cokkinides V, Singh GK, Cardinez C, Ghafoor A, Thun M. Cancer disparities by race/ethnicity and socioeconomic status. CA Cancer J Clin. 2004; 54(2): 78-93.
31. Doubeni CA, Jambaulikar GD, Fouayzi H, Robinson SB, Gunter MJ, Field TS, Roblin DW, Fletcher RH. Neighborhood socioeconomic status and use of colonoscopy in an insured population - a retrospective cohort study. PLoS One. 2012; 7(5): e36392.
32. Launay L, Dejardin O, Pornet C, Morlais F, Guittet L, Launoy G, Bouvier V. Influence of socioeconomic environment on survival in patients diagnosed with esophageal cancer: a population-based study. Dis Esophagus. 2012; 25: 723-730.
33. Lee W, Nelson R, Mailey B, Duldulao MP, Garcia-Aguilar J, Kim J. Socioeconomic factors impact colon cancer outcomes in diverse patient populations. J Gastrointest Surg. 2012 Apr; 16(4): 692-704.
34. Stessin AM, Sherr DL. Demographic disparities in patterns of care and survival outcomes for patients with resected gastric adenocarcinoma. Cancer Epidemiol Biomarkers Prev. 2011 Feb; 20(2): 223-33.
35. Singal V, Singal AK, Kuo YF. Racial disparities in treatment for pancreatic cancer and impact on survival: a population-based analysis. J Cancer Res Clin Oncol. 2012 Apr; 138(4): 715-22.
36. Robbins AS, Siegel RL, Jemal A. Racial disparities in stage-specific colorectal cancer mortality rates from 1985 to 2008. J Clin Oncol. 2012 Feb 1; 30(4): 401-5.
37. Artinyan A, Mailey B, Sanchez-Luege N, Khalili J, Sun CL, Bhatia S, Wagman LD, Nissen N, Colquhoun SD, Kim J. Race, ethnicity, and socioeconomic status influence the survival of patients with hepatocellular carcinoma in the United States. Cancer. 2010 Mar 1; 116(5): 1367-77.
38. Riall TS, Townsend CM Jr, Kuo YF, Freeman JL, Goodwin JS. Dissecting racial disparities in the treatment of patients with locoregional pancreatic cancer: a 2-step process. Cancer. 2010 Feb 15; 116(4): 930-9.
39. Hill S, Sarfati D, Blakely T, Robson B, Purdie G, Dennett E, Cormack D, Dew K, Ayanian JZ, Kawachi I. Ethnicity and management of colon cancer in New Zealand: do indigenous patients get a worse deal? Cancer. 2010 Jul 1; 116(13): 3205-14.
40. Chen AY, Halpern MT, Schrag NM, Stewart A, Leitch M, Ward E. Disparities and trends in sentinel lymph node biopsy among early-stage breast cancer patients (1998-2005). J Natl Cancer Inst. 2008 Apr 2; 100(7): 462-74.
41. Hulscher JB, van Sandick JW, de Boer AG, Wijnhoven BP, Tijssen JG, Fockens P, Stalmeier PF, ten Kate FJ, van Dekken H, Obertop H, Tilanus HW, van Lanschot JJ. Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl J Med. 2002 Nov 21; 347(21): 1662-9.
42. Brar SS, Seevaratnam R, Cardoso R, Law C, Helyer L, Coburn N. A systematic review of spleen and pancreas preservation in extended lymphadenectomy for gastric cancer. Gastric Cancer. 2011 Sep 14.
43. Frist WH. Overcoming disparities in U. S. health care. Health Aff (Millwood). 2005; 24(2): 445-451.
44. Baxter NN. Is lymph node count an ideal quality indicator for cancer care? J Surg Oncol. 2009; 99(4): 265-268.
45. Nathan H, Shore AD, Anders RA et al. Variation in lymph node assessment after colon cancer resection: patient, surgeon, pathologist, or hospital? J Gastrointest Surg. 2011 Mar; 15(3): 471-9.
46. Fielding LP, Arsenault PA, Chapuis PH, Dent O, Gathright B, Hardcastle JD, Hermanek P, Jass JR, Newland RC. Clinicopathological staging for colorectal cancer: an International Documentation System (IDS) and an International Comprehensive Anatomical Terminology (ICAT). J Gastroenterol Hepatol. 1991; 6(4): 325-344.
47. Greene FL, Page DL, Fleming ID, et al. AJCC Cancer Staging Manual, 6th ed. New York: Springer-Verlag, 2002.
48. Compton CC, Fielding LP, Burgart LJ, Conley B, Cooper HS, Hamilton SR, Hammond ME, Henson DE, Hutter RV, Nagle RB, Nielsen ML, Sargent DJ, Taylor CR, Welton M, Willett C. Prognostic factors in colorectal cancer. College of American Pathologists Consensus Statement. Arch Pathol Lab Med. 2000 Jul; 124(7): 979-94.
49. Stitzenberg KB, Meropol NJ. Trends in centralization of cancer surgery. Ann Surg Oncol. 2010 Nov; 17(11): 2824-31.
50. Bilimoria KY, Talamonti MS, Wayne JD et al. Effect of hospital type and volume on lymph node evaluation for gastric and pancreatic cancer. Arch Surg. 2008 Jul; 143(7): 671-8.
51. Senthil M, Trisal V, Paz IB et al. Prediction of the adequacy of lymph node retrieval in colon cancer by hospital type. Arch Surg. 2010 Sep; 145(9): 840-3.
52. Wang H, Safar B, Wexner SD et al. The clinical significance of fat clearance lymph node harvest for invasive rectal adenocarcinoma following neoadjuvant therapy. Dis Colon Rectum. 2009 Oct; 52(10): 1767-73.
53. Shia J, Wang H, Nash GM et al. Lymph node staging in colorectal cancer: revisiting the benchmark of at least 12 lymph nodes in R0 resection. J Am Coll Surg. 2012 Mar; 214(3): 348-55.
54. Altorki NK, Zhou XK, Stiles B, Port JL, Paul S, Lee PC, Mazumdar M. Total number of resected lymph nodes predicts survival in esophageal cancer. Ann Surg. 2008; 248(2): 221-226.
55. Smith DD, Schwarz RR, Schwarz RE. Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol. 2005 Oct 1; 23(28): 7114-24.
56. Slidell MB, Chang DC, Cameron JL, Wolfgang C, Herman JM, Schulick RD, Choti MA, Pawlik TM. Impact of total lymph node count and lymph node ratio on staging and survival after pancreatectomy for pancreatic adenocarcinoma: a large, population-based analysis. Ann Surg Oncol. 2008 Jan; 15(1): 165-74.