Skip to main content
Log in

Limited resection vs. pancreaticoduodenectomy for primary duodenal adenocarcinoma: a systematic review and meta-analysis

  • Review Article
  • Published:
International Journal of Clinical Oncology Aims and scope Submit manuscript

Abstract

It is well known that surgery is the mainstay treatment for duodenal adenocarcinoma. However, the optimal extent of surgery is still under debate. We aimed to systematically review and perform a meta-analysis of limited resection (LR) and pancreatoduodenectomy for patients with duodenal adenocarcinoma. A systematic electronic database search of the literature was performed using PubMed and the Cochrane Library. All studies comparing LR and pancreatoduodenectomy for patients with duodenal adenocarcinoma were selected. Long-term overall survival was considered as the primary outcome, and perioperative morbidity and mortality as the secondary outcomes. Fifteen studies with a total of 3166 patients were analyzed; 995 and 1498 patients were treated with limited resection and pancreatoduodenectomy, respectively. Eight and 7 studies scored a low and intermediate risk of publication bias, respectively. The LR group had a more favorable result than the pancreatoduodenectomy group in overall morbidity (odd ratio [OR]: 0.33, 95% confidence interval [CI] 0.17–0.65) and postoperative pancreatic fistula (OR: 0.13, 95% CI 0.04–0.43). Mortality (OR: 0.96, 95% CI 0.70–1.33) and overall survival (OR: 0.61, 95% CI 0.33–1.13) were not significantly different between the two groups, although comparison of the two groups stratified by prognostic factors, such as T categories, was not possible due to a lack of detailed data. LR showed long-term outcomes equivalent to those of pancreatoduodenectomy, while the perioperative morbidity rates were lower. LR could be an option for selected duodenal adenocarcinoma patients with appropriate location or depth of invasion, although further studies are required.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Aparicio T, Zaanan A, Mary F et al (2016) Small Bowel Adenocarcinoma. Gastroenterol Clin North Am 45(3):447–457

    Article  PubMed  Google Scholar 

  2. Buchbjerg T, Fristrup C, Mortensen MB (2015) The incidence and prognosis of true duodenal carcinomas. Surg Oncol 24(2):110–116

    Article  CAS  PubMed  Google Scholar 

  3. Meijer LL, Alberga AJ, de Bakker JK et al (2018) Outcomes and treatment options for duodenal adenocarcinoma: a systematic review and meta-analysis. Ann Surg Oncol 25(9):2681–2692

    Article  PubMed  PubMed Central  Google Scholar 

  4. Alwmark A, Andersson A, Lasson A (1980) Primary carcinoma of the duodenum. Ann Surg 191(1):13–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hu JX, Miao XY, Zhong DW et al (2006) Surgical treatment of primary duodenal adenocarcinoma. Hepatogastroenterology 53(72):858–862

    PubMed  Google Scholar 

  6. Joesting DR, Beart RW Jr, van Heerden JA et al (1981) Improving survival in adenocarcinoma of the duodenum. Am J Surg 141(2):228–231

    Article  CAS  PubMed  Google Scholar 

  7. Rose DM, Hochwald SN, Klimstra DS et al (1996) Primary duodenal adenocarcinoma: a ten-year experience with 79 patients. J Am Coll Surg 183(2):89–96

    CAS  PubMed  Google Scholar 

  8. Barnes G Jr, Romero L, Hess KR et al (1994) Primary adenocarcinoma of the duodenum: management and survival in 67 patients. Ann Surg Oncol 1(1):73–78

    Article  PubMed  Google Scholar 

  9. Zhang S, Cui Y, Zhong B et al (2011) Clinicopathological characteristics and survival analysis of primary duodenal cancers: a 14-year experience in a tertiary centre in South China. Int J Colorectal Dis 26(2):219–226

    Article  PubMed  Google Scholar 

  10. Chung WC, Paik CN, Jung SH et al (2011) Prognostic factors associated with survival in patients with primary duodenal adenocarcinoma. Korean J Intern Med 26(1):34–40

    Article  PubMed  PubMed Central  Google Scholar 

  11. Santoro E, Sacchi M, Scutari F et al (1997) Primary adenocarcinoma of the duodenum: treatment and survival in 89 patients. Hepatogastroenterology 44(16):1157–1163

    CAS  PubMed  Google Scholar 

  12. Sohn TA, Lillemoe KD, Cameron JL et al (1998) Adenocarcinoma of the duodenum: factors influencing long-term survival. J Gastrointest Surg 2(1):79–87

    Article  CAS  PubMed  Google Scholar 

  13. Bakaeen FG, Murr MM, Sarr MG et al (2000) What prognostic factors are important in duodenal adenocarcinoma? Arch Surg. 135(6):635–641 ((discussion 41-2))

    Article  CAS  PubMed  Google Scholar 

  14. Kaklamanos IG, Bathe OF, Franceschi D et al (2000) Extent of resection in the management of duodenal adenocarcinoma. Am J Surg 179(1):37–41

    Article  CAS  PubMed  Google Scholar 

  15. Tocchi A, Mazzoni G, Puma F et al (2003) Adenocarcinoma of the third and fourth portions of the duodenum: results of surgical treatment. Arch Surg 138(1):80–85

    Article  PubMed  Google Scholar 

  16. Cecchini S, Correa-Gallego C, Desphande V et al (2012) Superior prognostic importance of perineural invasion vs. lymph node involvement after curative resection of duodenal adenocarcinoma. J Gastrointest Surg. 16(1):113–120 ((discussion 20))

    Article  PubMed  Google Scholar 

  17. Onkendi EO, Boostrom SY, Sarr MG et al (2012) 15-year experience with surgical treatment of duodenal carcinoma: a comparison of periampullary and extra-ampullary duodenal carcinomas. J Gastrointest Surg 16(4):682–691

    Article  PubMed  Google Scholar 

  18. Kato Y, Takahashi S, Kinoshita T et al (2014) Surgical procedure depending on the depth of tumor invasion in duodenal cancer. Jpn J Clin Oncol 44(3):224–231

    Article  PubMed  Google Scholar 

  19. Cloyd JM, Norton JA, Visser BC et al (2015) Does the extent of resection impact survival for duodenal adenocarcinoma? Analysis of 1,611 cases. Ann Surg Oncol 22(2):573–580

    Article  PubMed  Google Scholar 

  20. Jiang QL, Huang XH, Chen YT et al (2016) Prognostic factors and clinical characteristics of patients with primary duodenal adenocarcinoma: a single-center experience from China. Biomed Res Int 2016:6491049

    PubMed  PubMed Central  Google Scholar 

  21. Lee CHA, Shingler G, Mowbray NG et al (2018) Surgical outcomes for duodenal adenoma and adenocarcinoma: a multicentre study in Australia and the United Kingdom. ANZ J Surg 88(3):E157–E161

    Article  PubMed  Google Scholar 

  22. Rangelova E, Blomberg J, Ansorge C et al (2015) Pancreas-preserving duodenectomy is a safe alternative to high-risk pancreatoduodenectomy for premalignant duodenal lesions. J Gastrointest Surg 19(3):492–497

    Article  PubMed  Google Scholar 

  23. Kohga A, Yamamoto Y, Sano S et al (2017) Surgical strategy for T1 duodenal or ampullary carcinoma according to the depth of tumor invasion. Anticancer Res 37(9):5277–5283

    PubMed  Google Scholar 

  24. DeOliveira ML, Winter JM, Schafer M et al (2006) Assessment of complications after pancreatic surgery: a novel grading system applied to 633 patients undergoing pancreaticoduodenectomy. Ann Surg. 244(6):931–937 ((discussion 7-9))

    Article  PubMed  PubMed Central  Google Scholar 

  25. Perez A, Saltzman JR, Carr-Locke DL et al (2003) Benign nonampullary duodenal neoplasms. J Gastrointest Surg 7(4):536–541

    Article  PubMed  Google Scholar 

  26. Yan JQ, Peng CH, Yang WP et al (2010) Surgical management of benign duodenal tumours. ANZ J Surg 80(7–8):526–530

    Article  PubMed  Google Scholar 

  27. Moher D, Liberati A, Tetzlaff J et al (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–341

    Article  PubMed  Google Scholar 

  28. Higgins JP, Altman DG, Gotzsche PC et al (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:d5928

    Article  PubMed  PubMed Central  Google Scholar 

  29. Wells G, Shea B, O'Connell D, Peterson j, Welch V, Losos M, et al (2000) The Newcastle–Ottawa Scale (NOS) for Assessing the Quality of Non-Randomized Studies in Meta-Analysis2000.

  30. Zhang RC, Xu XW, Wu D et al (2013) Laparoscopic transduodenal local resection of periampullary neuroendocrine tumor: a case report. World J Gastroenterol 19(39):6693–6698

    Article  PubMed  PubMed Central  Google Scholar 

  31. Poves I, Burdio F, Alonso S et al (2011) Laparoscopic pancreas-sparing subtotal duodenectomy. JOP 12(1):62–65

    PubMed  Google Scholar 

  32. Cho A, Yamamoto H, Kainuma O et al (2012) Totally laparoscopic pancreas-sparing duodenectomy. Surg Today 42(10):1032–1035

    Article  PubMed  Google Scholar 

  33. Stauffer JA, Raimondo M, Woodward TA et al (2013) Laparoscopic partial sleeve duodenectomy (PSD) for nonampullary duodenal neoplasms: avoiding a whipple by separating the duodenum from the pancreatic head. Pancreas 42(3):461–466

    Article  PubMed  Google Scholar 

  34. Konishi M, Kinoshita T, Nakagohri T et al (2007) Pancreas-sparing duodenectomy for duodenal neoplasms including malignancies. Hepatogastroenterology 54(75):753–757

    PubMed  Google Scholar 

  35. Chung RS, Church JM, vanStolk R (1995) Pancreas-sparing duodenectomy: indications, surgical technique, and results. Surgery 117(3):254–259

    Article  CAS  PubMed  Google Scholar 

  36. Huttner FJ, Fitzmaurice C, Schwarzer G et al (2016) Pylorus-preserving pancreaticoduodenectomy (pp Whipple) versus pancreaticoduodenectomy (classic Whipple) for surgical treatment of periampullary and pancreatic carcinoma. Cochrane Database Syst Rev. 2:CD006053

    PubMed  Google Scholar 

  37. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213

    Article  PubMed  PubMed Central  Google Scholar 

  38. Bassi C, Dervenis C, Butturini G et al (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138(1):8–13

    Article  PubMed  Google Scholar 

  39. Wente MN, Bassi C, Dervenis C et al (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142(5):761–768

    Article  PubMed  Google Scholar 

  40. Wente MN, Veit JA, Bassi C et al (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142(1):20–25

    Article  PubMed  Google Scholar 

  41. Poultsides GA, Huang LC, Cameron JL et al (2012) Duodenal adenocarcinoma: clinicopathologic analysis and implications for treatment. Ann Surg Oncol 19(6):1928–1935

    Article  PubMed  Google Scholar 

  42. Kim MJ, Choi SB, Han HJ et al (2014) Clinicopathological analysis and survival outcome of duodenal adenocarcinoma. Kaohsiung J Med Sci 30(5):254–259

    Article  PubMed  Google Scholar 

  43. Lee HG, You DD, Paik KY et al (2008) Prognostic factors for primary duodenal adenocarcinoma. World J Surg 32(10):2246–2252

    Article  PubMed  Google Scholar 

  44. Liang TJ, Wang BW, Liu SI et al (2012) Number of involved lymph nodes is important in the prediction of prognosis for primary duodenal adenocarcinoma. J Chin Med Assoc 75(11):573–580

    Article  PubMed  Google Scholar 

  45. Sarela AI, Brennan MF, Karpeh MS et al (2004) Adenocarcinoma of the duodenum: importance of accurate lymph node staging and similarity in outcome to gastric cancer. Ann Surg Oncol 11(4):380–386

    Article  PubMed  Google Scholar 

  46. Hurtuk MG, Devata S, Brown KM et al (2007) Should all patients with duodenal adenocarcinoma be considered for aggressive surgical resection? Am J Surg. 193(3):319–324 ((discussion 24-5))

    Article  CAS  PubMed  Google Scholar 

  47. Solaini L, Jamieson NB, Metcalfe M et al (2015) Outcome after surgical resection for duodenal adenocarcinoma in the UK. Br J Surg 102(6):676–681

    Article  CAS  PubMed  Google Scholar 

  48. Rotman N, Pezet D, Fagniez PL et al (1994) Adenocarcinoma of the duodenum: factors influencing survival. French Association for Surgical Research. Br J Surg. 81(1):83–85

    Article  CAS  PubMed  Google Scholar 

  49. Struck A, Howard T, Chiorean EG et al (2009) Non-ampullary duodenal adenocarcinoma: factors important for relapse and survival. J Surg Oncol 100(2):144–148

    Article  PubMed  Google Scholar 

  50. Ryder NM, Ko CY, Hines OJ et al (2000) Primary duodenal adenocarcinoma: a 40-year experience. Arch Surg. 135(9):1070–1074 ((discussion 4-5))

    Article  CAS  PubMed  Google Scholar 

  51. Moss WM, McCart PM, Juler G et al (1974) Primary adenocarcinoma of the duodenum. Arch Surg 108(6):805–807

    Article  CAS  PubMed  Google Scholar 

  52. Jones BA, Langer B, Taylor BR et al (1985) Periampullary tumors: which ones should be resected? Am J Surg 149(1):46–52

    Article  CAS  PubMed  Google Scholar 

  53. Ouriel K, Adams JT (1984) Adenocarcinoma of the small intestine. Am J Surg 147(1):66–71

    Article  CAS  PubMed  Google Scholar 

  54. Cortese AF, Cornell GN (1972) Carcinoma of the duodenum. Cancer 29(4):1010–1015

    Article  CAS  PubMed  Google Scholar 

  55. Lowell JA, Rossi RL, Munson JL et al (1992) Primary adenocarcinoma of third and fourth portions of duodenum. Favorable prognosis after resection. Arch Surg 127(5):557–560

    Article  CAS  PubMed  Google Scholar 

  56. Lai EC, Doty JE, Irving C et al (1988) Primary adenocarcinoma of the duodenum: analysis of survival. World J Surg 12(5):695–699

    Article  CAS  PubMed  Google Scholar 

  57. Malleo G, Tonsi A, Marchegiani G et al (2013) Postoperative morbidity is an additional prognostic factor after potentially curative pancreaticoduodenectomy for primary duodenal adenocarcinoma. Langenb Arch Surg 398(2):287–294

    Article  Google Scholar 

  58. Sakamoto T, Saiura A, Ono Y et al (2017) Optimal lymphadenectomy for duodenal adenocarcinoma: does the number alone matter? Ann Surg Oncol 24(11):3368–3377

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the Japan Duodenal Cancer Guideline Committee and many doctors related to this research opportunity. Japan Duodenal Cancer Guideline Committee: S. N. Souya Nunobe, S. K. Shingo Kanaji, H. E. Hidetoshi Eguchi, K. O. Ken-ichi Okada, T. F. Tsutomu Fujii, Y. N. Yuichi Nagakawa, K. K. Kengo Kanetaka, H. Y. Hiroharu Yamashita, S. Y. Suguru Yamada, S. K.Shinji Kuroda, T. A. Toru Aoyama, T. A. Takahiro Akahori, K. N. Kenji Nakagawa, R. H. Ryota Higuchi, H. Y. Hiroki Yamaue, M. S. Masayuki Sho, Y. K. Yasuhiro Kodera.

Funding

This work was supported by the Health and Labor Sciences Research Grant (Grant number H29-GANTAISAKU-IPPAN-013) and JSPS KAKENHI (Grant number 18K08632). The funders had no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

Author information

Authors and Affiliations

Authors

Consortia

Contributions

Study conception and design of study: RH. Duodenal Guidelines Committee, Surgery Group: SN, SK, HE, KO, TF, YN, KK, HY, SY, SK, TA, TA, KN, RH, HY, MS and YK. Organizing committee meetings and providing opportunities for making article: KO, MS and YK. Acquisition of data: SN, SK, HE, PB and RH. Analysis and interpretation of data: PB. and RH. Drafting of manuscript: PB. and RH. Critical revision of manuscript: SN, SK, HE, MY, KO, MS and YK.

Corresponding author

Correspondence to Ryota Higuchi.

Ethics declarations

Conflict of interest statement

The authors have no conflicts of interest to declare.

Ethical approval

The authors have no ethical conflicts to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The members of the Japan Duodenal Cancer Guideline Committee are mentioned in “Acknowledgements” section

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 245 KB)

Supplementary file1 (DOCX 37 KB)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Burasakarn, P., Higuchi, R., Nunobe, S. et al. Limited resection vs. pancreaticoduodenectomy for primary duodenal adenocarcinoma: a systematic review and meta-analysis. Int J Clin Oncol 26, 450–460 (2021). https://doi.org/10.1007/s10147-020-01840-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10147-020-01840-5

Keywords

Navigation