Skip to main content
SpringerLink
Log in

Perioperative Blood Management of Preoperative Anemia Determines Long-Term Outcome in Patients with Pancreatic Surgery

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery Aims and scope

Abstract

Background/Purpose

Anemia affects the postoperative course of patients undergoing a major surgical procedure. However, it remains unclear whether anemia has a different impact on the long-term outcome of patients with malignant or benign pancreatic disease.

Methods

A retrospective analysis of patients undergoing pancreatic surgery for pancreatic malignancies or chronic pancreatitis was conducted between January 2012 and June 2018 at the University Hospital Dresden, Germany. The occurrence of preoperative anemia and the administration of pre-, intra-, and postoperative blood transfusions were correlated with postoperative complications and survival data by uni- and multivariate analysis.

Results

A total of 682 patients were included with 482 (70.7%) undergoing surgical procedures for pancreatic malignancies. Univariate regression analysis confirmed preoperative anemia as a risk factor for postoperative complications > grade 2 according to the Clavien-Dindo classification. Multivariate regression analyses indicated postoperative blood transfusion as an independent risk factor for postoperative complications in patients with a benign (OR 20.5; p value < 0.001) and a malignant pancreatic lesion (OR 4.7; p value < 0.01). Univariate and multivariate analysis revealed preoperative anemia and pre-, intra-, and postoperative blood transfusions as independent prognostic factors for shorter overall survival in benign and malignant patients (p value < 0.001–0.01).

Conclusion

Preoperative anemia is a prevalent, independent, and adjustable factor in pancreatic surgery, which poses a significant risk for postoperative complications irrespective of the entity of the underlying disease. It should therefore be understood as an adjustable factor rather than an indicator of underlying disease severity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. R. S. Swanson, C. M. Pezzi, K. Mallin, A. M. Loomis, D. P. Winchester (2014) The 90-day mortality after pancreatectomy for cancer is double the 30-day mortality: more than 20,000 resections from the national cancer data base. Annals of surgical oncology 21 (13):4059-4067. https://doi.org/10.1245/s10434-014-4036-4

    Article  PubMed  Google Scholar 

  2. F. C. Althoff, H. Neb, E. Herrmann, K. M. Trentino, L. Vernich, C. Fullenbach, J. Freedman, J. H. Waters, S. Farmer, M. F. Leahy, K. Zacharowski, P. Meybohm, S. Choorapoikayil (2019) Multimodal Patient Blood Management Program Based on a Three-pillar Strategy: A Systematic Review and Meta-analysis. Annals of surgery 269 (5):794-804. https://doi.org/10.1097/sla.0000000000003095

    Article  PubMed  Google Scholar 

  3. K. M. Musallam, H. M. Tamim, T. Richards, D. R. Spahn, F. R. Rosendaal, A. Habbal, M. Khreiss, F. S. Dahdaleh, K. Khavandi, P. M. Sfeir, A. Soweid, J. J. Hoballah, A. T. Taher, F. R. Jamali (2011) Preoperative anaemia and postoperative outcomes in non-cardiac surgery: a retrospective cohort study. Lancet (London, England) 378 (9800):1396-1407. https://doi.org/10.1016/s0140-6736(11)61381-0

    Article  Google Scholar 

  4. D. J. Lucas, K. I. Schexneider, M. Weiss, C. L. Wolfgang, S. M. Frank, K. Hirose, N. Ahuja, M. Makary, J. L. Cameron, T. M. Pawlik (2014) Trends and risk factors for transfusion in hepatopancreatobiliary surgery. Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract 18 (4):719-728. https://doi.org/10.1007/s11605-013-2417-9

    Article  Google Scholar 

  5. P. Meybohm, E. Herrmann, A. U. Steinbicker, M. Wittmann, M. Gruenewald, D. Fischer, G. Baumgarten, J. Renner, H. K. Van Aken, C. F. Weber, M. M. Mueller, C. Geisen, J. Rey, D. Bon, G. Hintereder, S. Choorapoikayil, J. Oldenburg, C. Brockmann, R. G. Geissler, E. Seifried, K. Zacharowski (2016) Patient Blood Management is Associated With a Substantial Reduction of Red Blood Cell Utilization and Safe for Patient's Outcome: A Prospective, Multicenter Cohort Study With a Noninferiority Design. Annals of surgery 264 (2):203-211. https://doi.org/10.1097/sla.0000000000001747

    Article  PubMed  Google Scholar 

  6. V. Keding, K. Zacharowski, W. O. Bechstein, P. Meybohm, A. A. Schnitzbauer (2018) Patient Blood Management improves outcome in oncologic surgery. World journal of surgical oncology 16 (1):159. https://doi.org/10.1186/s12957-018-1456-9

    Article  PubMed  PubMed Central  Google Scholar 

  7. D. Fischer, H. Neb, S. Choorapoikayil, K. Zacharowski, P. Meybohm (2019) Red blood cell transfusion and its alternatives in oncologic surgery-A critical evaluation. Critical reviews in oncology/hematology 134:1-9. https://doi.org/10.1016/j.critrevonc.2018.11.011

    Article  PubMed  Google Scholar 

  8. M. Munoz, S. Gomez-Ramirez, A. Campos, J. Ruiz, G. M. Liumbruno (2015) Pre-operative anaemia: prevalence, consequences and approaches to management. Blood transfusion = Trasfusione del sangue 13 (3):370-379. https://doi.org/10.2450/2015.0014-15

    Article  PubMed  PubMed Central  Google Scholar 

  9. A. J. Kansagra, M. S. Stefan (2016) Preoperative Anemia: Evaluation and Treatment. Anesthesiology clinics 34 (1):127-141. https://doi.org/10.1016/j.anclin.2015.10.011

    Article  PubMed  Google Scholar 

  10. W. C. Wu, T. L. Schifftner, W. G. Henderson, C. B. Eaton, R. M. Poses, G. Uttley, S. C. Sharma, M. Vezeridis, S. F. Khuri, P. D. Friedmann (2007) Preoperative hematocrit levels and postoperative outcomes in older patients undergoing noncardiac surgery. Jama 297 (22):2481-2488. https://doi.org/10.1001/jama.297.22.2481

    Article  CAS  PubMed  Google Scholar 

  11. J. J. Yeh, M. Gonen, J. S. Tomlinson, K. Idrees, M. F. Brennan, Y. Fong (2007) Effect of blood transfusion on outcome after pancreaticoduodenectomy for exocrine tumour of the pancreas. The British journal of surgery 94 (4):466-472. https://doi.org/10.1002/bjs.5488

    Article  CAS  PubMed  Google Scholar 

  12. H. S. Yao, Q. Wang, W. J. Wang, Z. Q. Hu (2008) Intraoperative allogeneic red blood cell transfusion in ampullary cancer outcome after curative pancreatoduodenectomy: a clinical study and meta-analysis. World journal of surgery 32 (9):2038-2046. https://doi.org/10.1007/s00268-008-9675-9

    Article  PubMed  Google Scholar 

  13. H. M. Park, S. J. Park, J. R. Shim, E. C. Lee, S. D. Lee, S. S. Han, S. H. Kim (2017) Perioperative transfusion in pancreatoduodenectomy: The double-edged sword of pancreatic surgeons. Medicine 96 (49):e9019. https://doi.org/10.1097/md.0000000000009019

    Article  PubMed  PubMed Central  Google Scholar 

  14. P. Marincola Smith, J. Baechle, C. C. Solorzano, M. Tan, A. G. Lopez-Aguiar, M. Dillhoff, E. Beal, G. Poultsides, J. G. D. Cannon, F. G. Rocha, A. Crown, C. Cho, M. Beems, E. R. Winslow, V. R. Rendell, B. A. Krasnick, R. C. Fields, S. K. Maithel, C. E. Bailey, K. Idrees (2019) Impact of perioperative blood transfusion on survival in pancreatic neuroendocrine tumor patients: analysis from the US Neuroendocrine Study Group. HPB : the official journal of the International Hepato Pancreato Biliary Association. https://doi.org/10.1016/j.hpb.2019.10.2441

  15. R. A. Snyder, L. R. Prakash, G. M. Nogueras-Gonzalez, M. P. Kim, T. A. Aloia, J. N. Vauthey, J. E. Lee, J. B. Fleming, M. H. G. Katz, C. D. Tzeng (2019) Perioperative blood transfusions for vein resection during pancreaticoduodenectomy for pancreatic adenocarcinoma: Identification of clinical targets for optimization. HPB : the official journal of the International Hepato Pancreato Biliary Association 21 (7):841-848. https://doi.org/10.1016/j.hpb.2018.10.018

    Article  Google Scholar 

  16. E. von Elm, D. G. Altman, M. Egger, S. J. Pocock, P. C. Gotzsche, J. P. Vandenbroucke (2008) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Journal of clinical epidemiology 61 (4):344-349. https://doi.org/10.1016/j.jclinepi.2007.11.008

    Article  Google Scholar 

  17. A. S. Keats (1978) The ASA classification of physical status--a recapitulation. Anesthesiology 49 (4):233-236. https://doi.org/10.1097/00000542-197810000-00001

    Article  CAS  PubMed  Google Scholar 

  18. M. M. Oken, R. H. Creech, D. C. Tormey, J. Horton, T. E. Davis, E. T. McFadden, P. P. Carbone (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. American journal of clinical oncology 5 (6):649-655

  19. World Health Organization (1994) Indicators and strategies for iron deficiency and anemia programmes. Report of the WHO/UNICEF/UNU Consultation. Geneva, Switzerland, 6–10 December, 1993

  20. D. Dindo, N. Demartines, P. A. Clavien (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Annals of surgery 240 (2):205-213. https://doi.org/10.1097/01.sla.0000133083.54934.ae

    Article  PubMed  PubMed Central  Google Scholar 

  21. W. S. Beattie, K. Karkouti, D. N. Wijeysundera, G. Tait (2009) Risk associated with preoperative anemia in noncardiac surgery: a single-center cohort study. Anesthesiology 110 (3):574-581. https://doi.org/10.1097/ALN.0b013e31819878d3

    Article  PubMed  Google Scholar 

  22. M. Hogan, A. A. Klein, T. Richards (2015) The impact of anaemia and intravenous iron replacement therapy on outcomes in cardiac surgery. European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery 47 (2):218-226. https://doi.org/10.1093/ejcts/ezu200

    Article  Google Scholar 

  23. S. Lasocki, R. Krauspe, C. von Heymann, A. Mezzacasa, S. Chainey, D. R. Spahn (2015) PREPARE: the prevalence of perioperative anaemia and need for patient blood management in elective orthopaedic surgery: a multicentre, observational study. European journal of anaesthesiology 32 (3):160-167. https://doi.org/10.1097/eja.0000000000000202

    Article  PubMed  Google Scholar 

  24. S. Westphal, S. Isik, S. Choorapoikayil, C. Fullenbach, K. Zacharowski, P. Meybohm (2019) [Patient Blood Management: Preoperative Anemia and Case Reports from the Anemia Walk-In Clinic]. Anasthesiologie, Intensivmedizin, Notfallmedizin, Schmerztherapie : AINS 54 (3):182-193. https://doi.org/10.1055/a-0593-4354

    Article  PubMed  Google Scholar 

  25. B. Froessler, P. Palm, I. Weber, N. A. Hodyl, R. Singh, E. M. Murphy (2016) The Important Role for Intravenous Iron in Perioperative Patient Blood Management in Major Abdominal Surgery: A Randomized Controlled Trial. Annals of surgery 264 (1):41-46. https://doi.org/10.1097/sla.0000000000001646

    Article  PubMed  Google Scholar 

  26. C. Triphaus, L. Judd, P. Glaser, M. H. Goehring, E. Schmitt, S. Westphal, C. Fullenbach, S. Lindau, K. Zacharowski, P. Meybohm, S. Choorapoikayil (2019) Effectiveness of Preoperative Iron Supplementation in Major Surgical Patients with Iron Deficiency: A Prospective Observational Study. Annals of surgery. https://doi.org/10.1097/sla.0000000000003643

  27. P. J. Kneuertz, H. A. Pitt, K. Y. Bilimoria, J. P. Smiley, M. E. Cohen, C. Y. Ko, T. M. Pawlik (2012) Risk of morbidity and mortality following hepato-pancreato-biliary surgery. Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract 16 (9):1727-1735. https://doi.org/10.1007/s11605-012-1938-y

    Article  Google Scholar 

  28. J. M. Sutton, D. A. Kooby, G. C. Wilson, M. H. Squires, 3rd, D. J. Hanseman, S. K. Maithel, D. J. Bentrem, S. M. Weber, C. S. Cho, E. R. Winslow, C. R. Scoggins, R. C. Martin, 2nd, H. J. Kim, J. J. Baker, N. B. Merchant, A. A. Parikh, D. E. Abbott, M. J. Edwards, S. A. Ahmad (2014) Perioperative blood transfusion is associated with decreased survival in patients undergoing pancreaticoduodenectomy for pancreatic adenocarcinoma: a multi-institutional study. Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract 18 (9):1575-1587. https://doi.org/10.1007/s11605-014-2567-4

    Article  Google Scholar 

  29. E. L. Whitlock, H. Kim, A. D. Auerbach (2015) Harms associated with single unit perioperative transfusion: retrospective population based analysis. BMJ (Clinical research ed) 350:h3037. https://doi.org/10.1136/bmj.h3037

    Article  Google Scholar 

  30. A. J. Nanavati (2015) Letter in response to "Perioperative blood transfusion is associated with decreased survival in patients undergoing pancreaticoduodenectomy for pancreatic adenocarcinoma: a multi-institutional study". Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract 19 (2):407-408. https://doi.org/10.1007/s11605-014-2704-0

    Article  Google Scholar 

  31. J. W. Valle, D. Palmer, R. Jackson, T. Cox, J. P. Neoptolemos, P. Ghaneh, C. L. Rawcliffe, C. Bassi, D. D. Stocken, D. Cunningham, D. O'Reilly, D. Goldstein, B. A. Robinson, C. Karapetis, A. Scarfe, F. Lacaine, J. Sand, J. R. Izbicki, J. Mayerle, C. Dervenis, A. Olah, G. Butturini, P. A. Lind, M. R. Middleton, A. Anthoney, K. Sumpter, R. Carter, M. W. Buchler (2014) Optimal duration and timing of adjuvant chemotherapy after definitive surgery for ductal adenocarcinoma of the pancreas: ongoing lessons from the ESPAC-3 study. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 32 (6):504-512. https://doi.org/10.1200/jco.2013.50.7657

    Article  Google Scholar 

Download references

Author information

Author notes

  1. T. Welsch and C. Kahlert share senior authorship.

Authors and Affiliations

  1. Department for Visceral, Thoracic and Vascular Surgery, University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307, Dresden, Germany

    F. Oehme, S. Hempel, R. Knote, D. Addai, M. Distler, B. Muessle, U. Bork, J. Weitz, T. Welsch & C. Kahlert

Authors
  1. F. Oehme
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Hempel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Knote
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. Addai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Distler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. B. Muessle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. U. Bork
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. Weitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. T. Welsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. C. Kahlert
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study conception and design: FO, RK, DA, SH, and BM

Acquisition of data: FO, RK, DA, SH, MD, CK, and TW

Analysis and interpretation of data: FO, RK, DA, SH, MD, BM, UB, JW, CK, and TW

Writing of manuscript: FO, RK, DA, SH, MD, BM, UB, CK, TW, and JW with input and final approval of all authors

Corresponding author

Correspondence to C. Kahlert.

Ethics declarations

Previous Publication

None of the information contained in this manuscript, either in part or in whole, has been published elsewhere. Furthermore, this manuscript is not under consideration for publication in any other journal either in part or in whole.

Study Location

The study was carried out at the Department for Visceral, Thoracic and Vascular Surgery at the University Hospital Carl Gustav Carus, Fetscherstrasse 74, 01307 Dresden, Germany.

Conflict of Interest

The authors declare no competing interest.

Additional information

Publisher’s Note

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

Supplementary Information

Supplementary Fig. 1:

Kaplan–Meier analysis for patients with a benign disease. (a) Kaplan–Meier analysis for patients with and without a preoperative anemia. Patients with preoperative anemia had a significantly (p-value < 0.01) shorter OS of 18 months. (b) Kaplan–Meier analysis adjusted for patients with and without a preoperative blood transfusion. Patients with a preoperative blood transfusion had a significantly (p-value < 0.001) shorter OS of 64 months. (c) Kaplan–Meier analysis adjusted for patients with and without a preoperative blood transfusion. Patients with a intraoperative blood transfusion had a significantly (p-value = 0.01) shorter OS of 25 months. (d) Kaplan–Meier analysis adjusted for patients with and without a preoperative blood transfusion. Patients with a postoperative blood transfusion had a significantly (p-value < 0.001) shorter OS of 31 months. (PNG 503 kb)

High Resolution Image (TIFF 3075 kb)

Supplementary Fig. 2:

Kaplan–Meier analysis for patients with a malignant disease. (a) Kaplan–Meier analysis for patients with and without a preoperative anemia. Patients with preoperative anemia had a significantly (p-value < 0.001) shorter OS of 13 months. (b) Kaplan–Meier analysis adjusted for patients with and without a preoperative blood transfusion. Patients with a preoperative blood transfusion had a significantly (p-value < 0.01) shorter OS of 23 months. (c) Kaplan–Meier analysis adjusted for patients with and without a preoperative blood transfusion. Patients with a intraoperative blood transfusion had a significantly (p-value < 0.001) shorter OS of 16 months. (d) Kaplan–Meier analysis adjusted for patients with and without a preoperative blood transfusion. Patients with a postoperative blood transfusion had a significantly (p-value < 0.001) shorter OS of 19 months. (PNG 571 kb)

High Resolution Image (TIFF 3075 kb)

ESM 3

(DOCX 10 kb)

ESM 4

(DOCX 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oehme, F., Hempel, S., Knote, R. et al. Perioperative Blood Management of Preoperative Anemia Determines Long-Term Outcome in Patients with Pancreatic Surgery. J Gastrointest Surg 25, 2572–2581 (2021). https://doi.org/10.1007/s11605-021-04917-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-021-04917-2

Keywords

Search

Navigation