Skip to main content

Advertisement

Log in

Impact of the preoperative bone mineral density on the outcomes after resection of pancreatic cancer

  • Original Article
  • Published:
Surgery Today Aims and scope Submit manuscript

Abstract

Purpose

The aim of this study is to evaluate the correlation between bone mineral density (BMD) and other body composition markers, as well as, the impact of preoperative BMD on the surgical outcomes after resection of pancreatic cancer.

Methods

This retrospective study included 275 patients who underwent surgical resection of pancreatic cancer in our institute between 2003 and 2016. Patients were divided according to BMD into low and normal groups and their postoperative outcomes were compared. Risk factors for mortality and tumor recurrence were also evaluated.

Results

Patients with low BMD were older (P < 0.001), had a higher intramuscular adipose tissue content (P = 0.011) and higher visceral fat area (P = 0.003). The incidence of postoperative pancreatic fistula (POPF) (grade ≥ B) was higher in the low BMD group. No significant difference was observed between the two groups regarding overall survival and recurrence-free survival and low BMD was not a risk factor for mortality or tumor recurrence after resection of pancreatic cancer.

Conclusion

A low preoperative BMD was not found to be a risk factor for mortality or tumor recurrence after resection of pancreatic cancer; however, it was associated with a higher incidence of clinically relevant POPF.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

BMD:

Bone mineral density

CA 19.9:

Carbohydrate antigen 19.9

CT:

Computed tomography

DP:

Distal pancreatectomy

DXA:

Dual-energy X-ray absorptiometry

HR:

Hazard ratio

HCC:

Hepatocellular carcinoma

HU:

Hounsfield unit

IMAC:

Intramuscular adipose tissue content

IQR:

Interquartile range

mGPS:

Modified Glasgow prognostic score

NAC:

Neoadjuvant chemotherapy

OS:

Overall survival

PD:

Pancreaticodudonectomy

PMI:

Psoas muscle index

PNI:

Prognostic nutritional index

POPF:

Postoperative pancreatic fistula

RFS:

Recurrence-free survival

SMI:

Skeletal mass index

UICC:

Union for International Cancer Control

VSR:

Visceral to subcutaneous adipose tissue area ratio

References

  1. Ilic M, Ilic I. Epidemiology of pancreatic cancer. World J Gastroenterol. 2016;22:9694–705.

    Article  Google Scholar 

  2. Okumura S, Kaido T, Hamaguchi Y, Kobayashi A, Shirai H, Yao S, et al. Visceral adiposity and sarcopenic visceral obesity are associated with poor prognosis after resection of pancreatic cancer. Ann Surg Oncol. 2017;24:3732–40.

    Article  Google Scholar 

  3. Reynolds RB, Folloder J. Clinical management of pancreatic cancer. J Adv Pract Oncol. 2014;5:356–64.

    PubMed  PubMed Central  Google Scholar 

  4. Kaido T, Ogawa K, Fujimoto Y, Ogura Y, Hata K, Ito T, et al. Impact of sarcopenia on survival in patients undergoing living donor liver transplantation. Am J Transplant. 2013;13:1549–56.

    Article  CAS  Google Scholar 

  5. Hamaguchi Y, Kaido T, Okumura S, Kobayashi A, Shirai H, Yagi S, et al. Impact of skeletal muscle mass index, intramuscular adipose tissue content, and visceral to subcutaneous adipose tissue area ratio on early mortality of living donor liver transplantation. Transplantation. 2017;101:565–74.

    Article  Google Scholar 

  6. Hamaguchi Y, Kaido T, Okumura S, Fujimoto Y, Ogawa K, Mori A, et al. Impact of quality as well as quantity of skeletal muscle on outcomes after liver transplantation. Liver Transplant. 2014;20:1413–9.

    Article  Google Scholar 

  7. Peng P, Hyder O, Firoozmand A, Kneuertz P, Schulick RD, Huang D, et al. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg. 2012;16:1478–86.

    Article  Google Scholar 

  8. Levolger S, Ijzermans JNM, Ayez N, Tran TCK, Verhoef C, van Vledder MG. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg. 2012;99:550–7.

    Article  Google Scholar 

  9. Okumura S, Kaido T, Hamaguchi Y, Fujimoto Y, Masui T, Mizumoto M, et al. Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery. 2015;157:1088–98.

    Article  Google Scholar 

  10. Verschueren S, Gielen E, O’Neill TW, Pye SR, Adams JE, Ward KA, et al. Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int. 2013;24:87–988.

    Article  CAS  Google Scholar 

  11. Pereira FB, Leite AF, de Paula AP. Relationship between pre-sarcopenia, sarcopenia and bone mineral density in elderly men. Arch Endocrinol Metab. 2015;59:59–655.

    Article  Google Scholar 

  12. Schreiber JJ, Anderson PA, Rosas HG, Buchholz AL, Au AG. Hounsfield units for assessing bone mineral density and strength: a tool for osteoporosis management. J Bone Jt Surg Ser A. 2011;93:1057–63.

    Article  Google Scholar 

  13. Yao S, Kaido T, Okumura S, Iwamura S, Miyachi Y, Shirai H, et al. Bone mineral density correlates with survival after resection of extrahepatic biliary malignancies. Clin Nutr. 2018;38:2770–7.

    Article  Google Scholar 

  14. Miyachi Y, Kaido T, Yao S, Shirai H, Kobayashi A, Hamaguchi Y, et al. Bone mineral density as a risk factor for patients undergoing surgery for hepatocellular carcinoma. World J Surg. 2019;43:920–8.

    Article  Google Scholar 

  15. Sun K, Chen S, Xu J, Li G, He Y. The prognostic significance of the prognostic nutritional index in cancer: a systematic review and meta-analysis. J Cancer Res Clin Oncol. 2014;140:1537–49.

    Article  Google Scholar 

  16. Proctor MJ, Morrison DS, Talwar D, Balmer SM, O’Reilly DSJ, Foulis AK, et al. An inflammation-based prognostic score (mGPS) predicts cancer survival independent of tumour site: a Glasgow Inflammation Outcome Study. Br J Cancer. 2011;104:726–34.

    Article  CAS  Google Scholar 

  17. Dindo D, Demartines N, Clavien P-A. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.

    Article  Google Scholar 

  18. Dervenis C, Izbicki J, Neoptolemos J, Bassi C, Butturini G, Yeo C, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138:8–13.

    Article  Google Scholar 

  19. Sharma P, Parikh ND, Yu J, Barman P, Derstine BA, Sonnenday CJ, et al. Bone mineral density predicts posttransplant survival among hepatocellular carcinoma liver transplant recipients. Liver Transplant. 2016;22:1092–8.

    Article  Google Scholar 

  20. Richards JB, Rivadeneira F, Inouye M, Pastinen TM, Soranzo N, Wilson SG, et al. Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet (London, England). 2008;371:1505–12.

    Article  CAS  Google Scholar 

  21. Marinova M, Edon B, Wolter K, Katsimbari B, Schild HH, Strunk HM. Use of routine thoracic and abdominal computed tomography scans for assessing bone mineral density and detecting osteoporosis. Curr Med Res Opin. 2015;31:1871–81.

    Article  Google Scholar 

  22. Brett AD, Brown JK. Quantitative computed tomography and opportunistic bone density screening by dual use of computed tomography scans. J Orthop Transl. 2015;3:178–84.

    Google Scholar 

  23. Gausden EB, Nwachukwu BU, Schreiber JJ, Lorich DG, Lane JM. Opportunistic use of CT imaging for osteoporosis screening and bone density assessment. J Bone Jt Surg. 2017;99:1580–90.

    Article  Google Scholar 

  24. Ziemlewicz TJ, Binkley N, Pickhardt PJ. Opportunistic osteoporosis screening: addition of quantitative CT bone mineral density evaluation to CT colonography. J Am Coll Radiol. 2015;12:1036–41.

    Article  Google Scholar 

  25. Reuss-Borst M, Hartmann U, Scheede C, Weiß J. Prevalence of osteoporosis among cancer patients in Germany: prospective data from an oncological rehabilitation clinic. Osteoporos Int. 2012;23:1437–44.

    Article  CAS  Google Scholar 

  26. Axelsen CT, Jensen AB, Jakobsen EH, Bechmann T. Bone loss during neoadjuvant/adjuvant chemotherapy for early stage breast cancer: a retrospective cohort study. Mol Clin Oncol. 2018;8:767.

    CAS  PubMed  Google Scholar 

  27. Chen Y, Xu G, Yang F. Effect of neoadjuvant chemotherapy on the serum levels of bone turnover markers in women with early-stage breast cancer. PLoS ONE. 2015;10:e0126053.

    Article  Google Scholar 

  28. Lee H-F, Wu C-E, Lin Y-S, Hwang J-S, Wu C-H, Chu P-H. Low bone mineral density may be associated with long-term risk of cancer in the middle-aged population: a retrospective observational study from a single center. J Formos Med Assoc. 2018;117:339–45.

    Article  Google Scholar 

  29. Tanishima S, Morio Y. A review of minodronic acid hydrate for the treatment of osteoporosis. Clin Interv Aging. 2013;8:185.

    Article  CAS  Google Scholar 

  30. Bolam KA, van Uffelen JGZ, Taaffe DR. The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporos Int. 2013;24:2749–62.

    Article  CAS  Google Scholar 

  31. Szulc P, Beck TJ, Marchand F, Delmas PD. Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men—the MINOS study. J Bone Miner Res. 2004;20:721–9.

    Article  Google Scholar 

  32. Nahm CB, Connor SJ, Samra JS, Mittal A. Postoperative pancreatic fistula: a review of traditional and emerging concepts. Clin Exp Gastroenterol. 2018;11:105–18.

    Article  CAS  Google Scholar 

  33. Nishida Y, Kato Y, Kudo M, Aizawa H, Okubo S, Takahashi D, et al. Preoperative sarcopenia strongly influences the risk of postoperative pancreatic fistula formation after pancreaticoduodenectomy. J Gastrointest Surg. 2016;20:1586–94.

    Article  Google Scholar 

  34. Sato N, Tamura T, Minagawa N, Hirata K. Preoperative body mass index-to-prognostic nutritional index ratio predicts pancreatic fistula after pancreaticoduodenectomy. Hepatobiliary Surg Nutr. 2016;5:256–62.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Toshimi Kaido.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest in association with the present study.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharshar, M., Kaido, T., Shirai, H. et al. Impact of the preoperative bone mineral density on the outcomes after resection of pancreatic cancer. Surg Today 50, 757–766 (2020). https://doi.org/10.1007/s00595-019-01954-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-019-01954-y

Keywords

Navigation