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Impact of hypoalbuminemia on outcomes following pancreaticoduodenectomy: a NSQIP retrospective cohort analysis of 25,848 patients

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Abstract

Background

Efforts to preoperatively risk stratify and optimize patients before pancreaticoduodenectomy continue to improve outcomes. This study aims to determine the impact of hypoalbuminemia on outcomes following pancreaticoduodenectomy and outline optimal hypoalbuminemia cut-off values in this population.

Methods

The ACS-NSQIP (2016–2021) database was used to extract patients who underwent pancreaticoduodenectomy, comparing those with hypoalbuminemia (< 3.0 g/L) to those with normal albumin. Demographics and 30-day outcomes were compared. Multivariable modeling evaluated factors including hypoalbuminemia to characterize their independent effect on serious complications, and mortality. Optimal albumin cut-offs for serious complications and mortality were evaluated using receiver-operating characteristic curves.

Results

We evaluated 25,848 pancreaticoduodenectomy patients with 2712 (10.5%) having preoperative hypoalbuminemia. Patients with hypoalbuminemia were older (68.2 vs. 65.1; p < 0.0001), and were significantly more likely to be ASA class 4 or higher (13.9% vs. 6.7%; p < 0.0001). Patients with hypoalbuminemia had significantly more 30-day complications and after controlling for comorbidities hypoalbuminemia remained a significant independent factor associated with 30-day serious complications (OR 1.80, p < 0.0001) but not mortality (OR 1.37, p = 0.152).

Conclusions

Hypoalbuminemia plays a significant role in 30-day morbidity following pancreaticoduodenectomy. Preoperative albumin may serve as a useful marker for risk stratification and optimization.

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References

  1. Heeger K, Fendrich V, Waldmann J, Langer P, Kanngießer V, Bartsch DK (2013) Reduced complication rate after modified binding purse-string-mattress sutures pancreatogastrostomy versus duct-to-mucosa pancreaticojejunostomy. The Surgeon 11(5):246–252

    Article  PubMed  Google Scholar 

  2. Schmidt CM, Powell ES, Yiannoutsos CT, Howard TJ, Wiebke EA, Wiesenauer CA et al (2004) Pancreaticoduodenectomy: a 20-year experience in 516 patients. Arch Surg 139(7):718–727

    Article  PubMed  Google Scholar 

  3. Parikh P, Shiloach M, Cohen ME, Bilimoria KY, Ko CY, Hall BL et al (2010) Pancreatectomy risk calculator: an ACS-NSQIP resource. HPB 12(7):488–497

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cusworth BM, Krasnick BA, Nywening TM, Woolsey CA, Fields RC, Doyle MM et al (2017) Whipple-specific complications result in prolonged length of stay not accounted for in ACS-NSQIP Surgical Risk Calculator. HPB 19(2):147–153

    Article  PubMed  Google Scholar 

  5. Dewulf M, Verrips M, Coolsen MM, Damink SWO, Den Dulk M, Bongers BC et al (2021) The effect of prehabilitation on postoperative complications and postoperative hospital stay in hepatopancreatobiliary surgery a systematic review. HPB 23(9):1299–1310

    Article  PubMed  Google Scholar 

  6. Deprato A, Verhoeff K, Purich K, Kung JY, Bigam DL, Dajani KZ (2022) Surgical Outcomes and quality of life following exercise-based prehabilitation for hepato-pancreatico-biliary surgery: a systematic review and meta-analysis. Hepatobiliary Pancreat Dis Int 21(3):207–217

    Article  PubMed  Google Scholar 

  7. ACS NSQIP Surgical Risk Calculator [Internet]. 2021 [cited 2023 Jun 16]. Available from: https://riskcalculator.facs.org/RiskCalculator/

  8. Martín Santos S, Sorribas Grifell M, Busquets Barenys J, Secanella Medayo L, Peláez Serra N, Carnaval T et al (2023) Hypoalbuminemia and advanced age are risk factors for delayed gastric emptying after pancreaticoduodenectomy. Nutr Hosp 40(3):517–520

    PubMed  Google Scholar 

  9. Tfaily MA, Ghanem P, Farran SH, Dabdoub F, Kanafani ZA (2022) The role of preoperative albumin and white blood cell count in surgical site infections following whipple surgery. Sci Rep 12(1):19184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Moman RN, Gupta N, Varacallo M (2022) Physiology, albumin. StatPearls [Internet]. StatPearls Publishing, Treasure Island, FL

    Google Scholar 

  11. Silva-Fhon JR, Rojas-Huayta VM, Aparco-Balboa JP, Cespedes-Panduro B, Partezani-Rodrigues RA (2021) Sarcopenia and blood albumin: a systematic review with meta-analysis. Biomedica 41(3):590–603

    Article  PubMed  PubMed Central  Google Scholar 

  12. Baumgartner RN, Koehler KM, Romero L, Garry PJ (1996) Serum albumin is associated with skeletal muscle in elderly men and women. Am J Clin Nutr 64(4):552–558

    Article  CAS  PubMed  Google Scholar 

  13. Liu X, Wu X, Zhou C, Hu T, Ke J, Chen Y et al (2017) Preoperative hypoalbuminemia is associated with an increased risk for intra-abdominal septic complications after primary anastomosis for Crohn’s disease. Gastroenterol Rep 5(4):298–304

    Article  Google Scholar 

  14. Gibbs J, Cull W, Henderson W, Daley J, Hur K, Khuri SF (1999) Preoperative serum albumin level as a predictor of operative mortality and morbidity: results from the National VA Surgical Risk Study. Arch Surg 134(1):36–42

    Article  CAS  PubMed  Google Scholar 

  15. Eckart A, Struja T, Kutz A, Baumgartner A, Baumgartner T, Zurfluh S et al (2020) Relationship of nutritional status, inflammation, and serum albumin levels during acute illness: a prospective study. Am J Med 133(6):713–722

    Article  CAS  PubMed  Google Scholar 

  16. Farag E, Ebrahim ZY (2020) The perioperative use of albumin. Perioper Fluid Manag 2020:235–254

    Article  Google Scholar 

  17. Lee E-H, Baek S-H, Chin J-H, Choi D-K, Son H-J, Kim W-J et al (2012) Preoperative hypoalbuminemia is a major risk factor for acute kidney injury following off-pump coronary artery bypass surgery. Intensive Care Med 38:1478–1486

    Article  PubMed  Google Scholar 

  18. Nazha B, Moussaly E, Zaarour M, Weerasinghe C, Azab B (2015) Hypoalbuminemia in colorectal cancer prognosis: nutritional marker or inflammatory surrogate? World J Gastrointest Surg 7(12):370

    Article  PubMed  PubMed Central  Google Scholar 

  19. Greenblatt DY, Kelly KJ, Rajamanickam V, Wan Y, Hanson T, Rettammel R et al (2011) Preoperative factors predict perioperative morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol 18:2126–2135

    Article  PubMed  Google Scholar 

  20. Bretschera C, Boesiger F, Kaegi-Braun N, Hersberger L, Lobo DN, Evans DC et al (2022) Admission serum albumin concentrations and response to nutritional therapy in hospitalised patients at malnutrition risk: Secondary analysis of a randomised clinical trial. EClinicalMedicine 45:101301

    Article  PubMed  PubMed Central  Google Scholar 

  21. Rungsakulkij N, Tangtawee P, Suragul W, Muangkaew P, Mingphruedhi S, Aeesoa S (2019) Correlation of serum albumin and prognostic nutritional index with outcomes following pancreaticoduodenectomy. World J Clin Cases 7(1):28

    Article  PubMed  PubMed Central  Google Scholar 

  22. Bharadwaj S, Ginoya S, Tandon P, Gohel TD, Guirguis J, Vallabh H et al (2016) Malnutrition: laboratory markers vs nutritional assessment. Gastroenterol Rep 4(4):272–280

    Google Scholar 

  23. User Guide for the 2021 ACS NSQIP Participant Use Data File (PUF) https://www.facs.org/quality-programs/data-and-registries/acs-nsqip/participant-use-data-file/2022 [

  24. Xu W, Peng X, Jiang B (2020) Hypoalbuminemia after pancreaticoduodenectomy does not predict or affect short-term postoperative prognosis. BMC Surg 20:1–11

    Article  Google Scholar 

  25. Pulvirenti A, Ramera M, Bassi C (2017) Modifications in the International Study Group for Pancreatic Surgery (ISGPS) definition of postoperative pancreatic fistula. Translat Gastroenterol Hepatol 2:107

    Article  Google Scholar 

  26. Dindo D, Demartines N, Clavien P-A (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 

  27. Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien P-A (2013) The comprehensive complication index (CCI). A novel continuous scale to measure surgical morbidity. Ann Surg 258(1):21–38

    Article  Google Scholar 

  28. Cai Z, Yang Y, Han Y, Fu X, Mao L, Qiu Y (2023) Clinical validation of the comprehensive complication index in a pancreaticoduodenectomy cohort. Eur Surg Res 64(3):334–341

    Article  CAS  PubMed  Google Scholar 

  29. Ray S, Mehta NN, Mangla V, Lalwani S, Mehrotra S, Chugh P et al (2019) A comparison between the comprehensive complication index and the Clavien-Dindo grading as a measure of postoperative outcome in patients undergoing gastrointestinal surgery—a prospective study. J Surg Res 244:417–424

    Article  PubMed  Google Scholar 

  30. Ricci C, Ingaldi C, Grego DG, Alberici L, De Raffele E, Pagano N et al (2021) The use of comprehensive complication Index® in pancreatic surgery: a comparison with the Clavien-Dindo system in a high volume center. HPB 23(4):618–624

    Article  PubMed  Google Scholar 

  31. Lovasik BP, Kron P, Clavien P-A, Petrowsky H, Kooby DA (2019) Pancreatectomy and body mass index: an international evaluation of cumulative postoperative complications using the comprehensive complications index. HPB 21(12):1761–1772

    Article  PubMed  Google Scholar 

  32. Kim SH, Hwang HK, Lee WJ, Kang CM (2021) Comprehensive complication index or Clavien-Dindo classification: which is better for evaluating the severity of postoperative complications following pancreatectomy? World J Surg 45:849–856

    Article  PubMed  Google Scholar 

  33. Kim S, Hwang H, Kim K, Lee W, Kang C (2018) A validation of comprehensive complication index for postoperative complication severity compared to the clavien-dindo classification. HPB 20:S247–S248

    Article  Google Scholar 

  34. Liu X (2012) Classification accuracy and cut point selection. Stat Med 31(23):2676–2686

    Article  PubMed  Google Scholar 

  35. Ge L-N, Wang F (2018) Prognostic significance of preoperative serum albumin in epithelial ovarian cancer patients: a systematic review and dose–response meta-analysis of observational studies. Cancer Manag Res 10:815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gu A, Malahias M-A, Strigelli V, Nocon AA, Sculco TP, Sculco PK (2019) Preoperative malnutrition negatively correlates with postoperative wound complications and infection after total joint arthroplasty: a systematic review and meta-analysis. J Arthroplasty 34(5):1013–1024

    Article  PubMed  Google Scholar 

  37. Gupta A, Gupta E, Hilsden R, Hawel JD, Elnahas AI, Schlachta CM et al (2021) Preoperative malnutrition in patients with colorectal cancer. Can J Surg 64(6):E621

    Article  PubMed  PubMed Central  Google Scholar 

  38. Hennessey DB, Burke JP, Ni-Dhonochu T, Shields C, Winter DC, Mealy K (2010) Preoperative hypoalbuminemia is an independent risk factor for the development of surgical site infection following gastrointestinal surgery: a multi-institutional study. Ann Surg 252(2):325–329

    Article  PubMed  Google Scholar 

  39. Xu R, Hao M, Zhou W, Liu M, Wei Y, Xu J et al (2022) Preoperative hypoalbuminemia in patients undergoing cardiac surgery: a meta-analysis. Surg Today 2022:1–12

    Google Scholar 

  40. Christina NM, Tjahyanto T, Lie JG, Santoso TA, Albertus H, Octavianus D et al (2023) Hypoalbuminemia and colorectal cancer patients: Any correlation?: a systematic review and meta-analysis. Medicine 102:8

    Article  Google Scholar 

  41. Gaspar-Figueiredo S, Labgaa I, Demartines N, Schäfer M, Joliat G-R (2023) Assessment of the predictive value of preoperative serum albumin and postoperative albumin drop (ΔAlb) for complications after pancreas surgery: a single-center cross-sectional study. J Clin Med 12(3):972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Vincent J-L, Dubois M-J, Navickis RJ, Wilkes MM (2003) Hypoalbuminemia in acute illness: is there a rationale for intervention?: a meta-analysis of cohort studies and controlled trials. Ann Surg 237(3):319

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kim S, McClave SA, Martindale RG, Miller KR, Hurt RT (2017) Hypoalbuminemia and clinical outcomes: what is the mechanism behind the relationship? Am Surg 83(11):1220–1227

    Article  PubMed  Google Scholar 

  44. Kim K, Seo H, Chin J-H, Son H-J, Hwang J-H, Kim Y-K (2015) Preoperative hypoalbuminemia and anemia as predictors of transfusion in radical nephrectomy for renal cell carcinoma: a retrospective study. BMC Anesthesiol 15:1–7

    Article  Google Scholar 

  45. McCluskey SA, Karkouti K, Wijeysundera DN, Kakizawa K, Ghannam M, Hamdy A et al (2006) Derivation of a risk index for the prediction of massive blood transfusion in liver transplantation. Liver Transpl 12(11):1584–1593

    Article  PubMed  Google Scholar 

  46. Jeong H, Kim JA, Yang M, Ahn HJ, Heo J, Han IW et al (2022) Preemptive administration of albumin during pancreatectomy does not reduce postoperative complications: a prospective randomized controlled trial. J Clin Med 11(3):620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Schaller SJ, Fuest K, Ulm B, Schmid S, Bubb C, Eckstein H-H et al (2023) Goal-directed perioperative albumin substitution versus standard of care to reduce postoperative complications-a randomized clinical trial (SuperAdd Trial). Ann Surg 10:1097

    Google Scholar 

  48. McClave SA, Taylor BE, Martindale RG, Warren MM, Johnson DR, Braunschweig C et al (2016) Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: Society of Critical Care Medicine (SCCM) and American Society for Parenteral and Enteral Nutrition (ASPEN). JPEN J Parenter Enteral Nutr 40(2):159–211

    Article  CAS  PubMed  Google Scholar 

  49. Jie B, Jiang Z-M, Nolan MT, Zhu S-N, Yu K, Kondrup J (2012) Impact of preoperative nutritional support on clinical outcome in abdominal surgical patients at nutritional risk. Nutrition 28(10):1022–1027

    Article  PubMed  Google Scholar 

  50. Group* VATPNCS (1991) Perioperative total parenteral nutrition in surgical patients. N Engl J Med 325(8):525–532

    Article  Google Scholar 

  51. Kim L, Mabry C, Klimberg VS (2007) Quality of benchmarks for assessment of care will influence outcome. Ann Surg 245(5):672–673

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

AMJS serves as a consultant to ViaCyte Inc., Vertex Inc., Betalin Ltd., Hemostemix Inc. and Aspect Biosystems Ltd. Taylor Sawchuk, Kevin Verhoeff, Uzair Jogiat, Valentin Mocanu, Blaire Anderson, Khaled Dajani, and David Bigam have no conflicts of interest to disclose. Taylor Sawchuk, Kevin Verhoeff, Uzair Jogiat, Valentin Mocanu, James Shapiro, Blaire Anderson, Khaled Dajani, and David Bigam did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

Authors

Contributions

Taylor Sawchuk assisted with methodology, investigation, editing, and original draft writing. Kevin Verhoeff assisted with conceptualization, methodology, data curation and analysis, investigation, editing, and supervision. Uzair Jogiat and Valentin Mocanu assisted with methodology, data analysis, and manuscript editing. A.M. James Shapiro, Blaire Anderson, Khaled Dajani, and David Bigam assisted with conceptualization, methodology, manuscript editing, and supervision.

Corresponding author

Correspondence to Kevin Verhoeff.

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American College of Surgeons National Surgical Quality Improvement Program and the hospitals participating in the ACS NSQIP are the source of the data used herein; they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the authors.

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This study was exempt from ethics review.

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Sawchuk, T., Verhoeff, K., Jogiat, U. et al. Impact of hypoalbuminemia on outcomes following pancreaticoduodenectomy: a NSQIP retrospective cohort analysis of 25,848 patients. Surg Endosc (2024). https://doi.org/10.1007/s00464-024-11018-z

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