Skip to main content
Download PDF

Physiological stress level and screening for malnutrition as preoperative predictors of postoperative complications in pancreatic surgery: a retrospective study

BMC Surgery volume 23, Article number: 156 (2023) Cite this article

Abstract

Background

Assessment of ‘physiological stress levels’ and ‘nutritional status’ before surgery is important for predicting complications and indirect interventions on the pancreas. The aim of this study was to determine neutrophil–lymphocyte ratio (NLR) and nutritional risk index (NRI) indicators before surgery to predict 90-day complications and mortality in a cohort of patients with complicated chronic pancreatitis and cancer of the head of the pancreas.

Methods

We evaluated preoperative levels of NLR and NRI among 225 subjects treated at different centres located in three countries. Short-term outcomes included length of hospital stay, postoperative complications, and mortality at 90 days and were appreciated based on NLR and NRI. The level of physiological stress was divided according by the formulas: neutrophil–lymphocyte ratio (NLR) = (neutrophil count, %)/(lymphocyte count, %). The nutritional state of the patients was divided according to the INR: NRI = (1.519 × serum albumin, g/L) + (41.7 × present weight, kg / usual weight, kg)].

Results

All patients were operated. An analysis of the operations performed in three institutions demonstrated mortality in chronic pancreatitis and pancreatic pseudocysts in 1.4%, in chronic pancreatitis and the presence of an inflammatory mass mainly in the pancreatic head in 1.2%, and in cancer of the pancreatic head in 5.9%. The mean preoperative NLR was normal in 33.8% of the patients, the mild physiologic stress level was 54.7%, and the moderate was 11.5% before surgery. 10.2% of patients had a normal nutritional status, 20% had mild, 19.6% had moderate, and 50.2% had severe malnutrition. In a univariate analysis, at the cutoff of NLR ≥ 9.5 (AUC = 0.803) and the cutoff of NRI ≤ 98.5 (AUC = 0.801), increasing the risk of complications was observed (hazard ratio, 2.01; 95% CI, 1.247–3.250, p = 0.006), but at the cutoff of NRI ≤ 83.55 (AUC = 0.81), we observed a survival difference in operated patients (hazard ratio, 2.15; 95% CI, 1.334–3.477, p = 0.0025).

Conclusions

Our study demonstrated that NLR and NRI were predictors of postoperative complications, but only NRI was a predictor of 90-day mortality in patients after surgery.

Peer Review reports

Introduction

According to statistics, the number of patients with chronic, and pancreatic cancer has increased dramatically in recent years, both in Ukraine and abroad, as has the number of operations performed on these patients. Surgical treatment of these diseases is the most difficult problem in abdominal surgery, which is confirmed by the presence of a high number of postoperative complications, low resectability in cancer, high operational risk, unsatisfactory long-term treatment results, poor patient quality of life, etc. Modern ideas about the mechanisms of development of pancreatitis and tumour growth, despite studying the mechanisms of intracellular and extracellular signalling, do not allow us to unequivocally state the cause-and-effect relationships between the structural, functional, and clinical manifestations of inflammation on the one hand and the development of diseases on the other hand. The lack of convincing data on the relationship between inflammation and proliferative processes in the epithelium and stroma of the pancreas explains the existing debate on the issues of differentiation, diagnosis, prognosis complications, and the choice of surgical tactics in different diseases of the pancreas.

The quantitative indicators of blood leucocytes and the formula of leucocytes are used in clinical practice and are essential for diagnosing acute inflammatory diseases of various locations and etiologies. Currently, several indicators have been suggested for assessing the severity of inflammatory changes in the body and the effectiveness of therapy. One such indicator is the relationship between neutrophils and lymphocytes (NLR) as a marker of systemic inflammation and physiological stress levels. An analysis of recent literature has shown the predictive value of NLR in patients with oncological, cardiovascular, autoimmune, and infectious diseases, including chronic obstructive pulmonary disease, Alzheimer's disease, multiple sclerosis, schizophrenia [1,2,3,4,5,6,7,8], and COVID-19 [9]. Interesting is the study of this indicator in gastroenterology, in particular, its prognostic and diagnostic value in different patients [9,10,11,12,13,14,15,16,17]. Several previous studies have assessed the predictive role of inflammatory indicators in different diseases [18,19,20,21].

It was well known that malnutrition is a significant risk factor for morbidity and mortality after gastrointestinal surgery. The nutritional risk index (NRI) and the NLR are two well-tested tools that are used for diagnosis and prognosis outcomes in surgery [22,23,24,25,26]. For many years, the nutritional status of the patient before surgery was considered one of the key factors influencing the occurrence of various complications after surgery, and there are several studies on the possibility of using the NRI as a screening tool for malnutrition to predict postoperative complications and the impact on patient survival [27]. Currently, there is no predictive nomogram system for predictive screening among patients with pancreatic disease who are scheduled for surgery, both in patients with complicated chronic pancreatitis and in patients with pancreatic cancer [28]. On the one hand, most prognostic models are based on factors obtained after surgery; on the other hand, in several studies, the authors tried to use various non-tumor and tumor biomarkers associated with hepatopancreatobiliary diseases to assess the development of postoperative complications [28,29,30,31]. It is known that such non-tumour-biomarkers as the NLR and NRI are associated with the patient's preoperative inflammatory response to a pathological process in the pancreas, and, therefore, can facilitate the assessment of prognosis before surgery [32, 33]. It is also known that the disease of the pancreas is associated with severe nutritional problems with the development of malnutrition and the implementation of systematic nutritional support for these patients [34, 35]. Preoperative assessment of the diagnostic and prognostic value of NLR and NRI for predicting surgical risk may facilitate the identification of strategies to prevent postoperative complications and improve overall survival in various patient categories [36, 37].

This study aimed to determine how the preoperative NLR and NRI levels predict postoperative complications and mortality in direct pancreatic interventions for complicated chronic pancreatitis and pancreatic head cancer.

Materials and methods

Patient selection and data collection

A three-center retrospective study was conducted on 225 patients who were operated on with follow-up between January 1, 2014, and December 1, 2022, retrospectively evaluated in each of the 3 participating institutions in Ukraine (Kharkiv Regional Clinical Hospital and Institute Emergency and General Surgery named after V.T. Zaitcev) and Germany (Krankenhaus Sachsenhausen Hospital, Frankfurt am Main, Germany). The respective institutional review boards of each participating institution have approved this study. Demographic and clinical data were collected, including age, gender, BMI, diabetes mellitus, white blood cell count, total neutrophil and lymphocyte count, serum albumin, preoperative bilirubin level, preoperative biliary drainage, and preoperative nutritional support. Short-term outcomes included length of hospital stay, postoperative complications, and mortality at 90 days and were appreciated based on NLR and NRI.

This two-institution retrospective cohort study was handled in accordance with the Declaration of Helsinki. This manuscript adheres to the applicable STROBE guideline. The use of registered data follows the General Data Protection Regulation of the European Union.

The patient’s written Informed consent was signed for each bio-object from the residual materials.

The study and the use of data were consented to by the Ethics Committee of Kharkiv National Medical University, Ukraine (Protocol No. 6, November 11, 2022).

The level of physiological stress was divided according to the formulas: neutrophil–lymphocyte ratio (NLR) = (neutrophil count, percentages)/(lymphocyte count, percentages) [38, 39].

The nutritional state of the patients was divided according to the INR [40, 41]: NRI = (1.519 × serum albumin, g/L) + (41.7 × present weight, kg / usual weight*, kg)] *Usual weight is defined as stable body weight for last 6 months.

For both univariate analysis and the predictive model, cutoffs for NLR and NRI were calculated.

Statistical analysis

The analysis was completed via IBM SPSS Statistics (https://www.ibm.com/products/spss-statistics).

We compared the reference characteristics of the patients with all the data. Missing data for serum albumin, current body weight, and usual body weight were excluded from the study to ensure the validity of the data. Differences in baseline characteristics using χ2 test for categorical variables for normally distributed or not normally distributed variables, respectively. Summary statistics were presented as integers and percentages for categorical variables and medians with interquartile ranges (IQRs) for continuous variables. The primary endpoint of interest was the presence of postoperative complications; the secondary endpoint was mortality within 90 days postoperatively, defined as the time interval between the date of surgery and the date of death or last follow-up, as appropriate. A p-value ≤ 0.05 was considered statistically significant. To determine the appropriate cutoff values, we used receiver operating characteristic (ROC) curves and determined the area under the curve (AUC). The efficacy of the model was considered limited at AUC ≥ 0.70; good at AUC ≥ 0.80; excellent at AUC ≥ 0.90. The predictive value of NLR and NRI for patients is carried out through univariate logistic regression analysis as predictive variables which were presented as risk ratios (HR) at 95% confidence intervals (CI). Overall survival within 90 was compared for various categories of interest using the Kaplan–Meier method with the log-rank test.

Results

Study characteristics and patient demographics

A total of 225 patients were retrospectively assessed and their demographic characteristics are presented in Table 1.

Table 1 Demographic, clinical, and laboratory characteristics of 225 patients
Full size table

In the group of patients with pancreatic head cancer, the main morphological type was volume-forming (n = 61, 89.1%). Characteristics of the features of the operations performed on the analyzed patients are presented in Table 2. Postoperative complications occurred in 12 patients (16.9%) with pseudocysts of the pancreas, in 13 (15.1%) with chronic pancreatitis, and in 37 (54.4%) with cancer. 6 patients (2.7%) died within 90 days after the operation. The median length of hospital stay was 10, 12, and 24 days, respectively (χ2 = 8.218, p = 0.017).

Table 2 Intra- and postoperative outcomes
Full size table

The cutoff value for blood albumin was 32 g/l, and the preoperative area under the curve was better than that for C-reactive protein (area under the curve: 0.802 vs. 0.617, Fig. 1). However, there was no significant difference according to the χ2 criterion both in the average values of blood serum albumin (χ2 = 0.576∕p = 0.750) and in the level of C-reactive protein (χ2 = 4.913∕p = 0.086) in all types of pancreatic pathology before surgery. In addition, patients with albumin levels ≥ 32 g/l and C-reactive protein (CRP) ≤ 68 mg/l were more likely to have short-term complications (Clavien-Dindo I and II) after surgery (48% versus 52% and 42% versus 58%, χ2 = 0.162∕ p = 0.688) than patients with albumin < 32 g/l and CRP > 68 mg/l (46% versus 54% and 36% versus 64%, respectively, χ2 = 1.674∕p = 0.619). The mean preoperative NLR was normal in 33.8% of the patients, with mild physiological stress in 54.7% and moderate in 11.5% before surgery (Table 3). According to the NRI, 10.2% of patients had a normal nutritional status, 20% had mild, 19.6% had moderate, and 50.2% had severe malnutrition. Figure 2 depicts the ability of selected indicators NLR and NRI to predict complications and mortality in patients using ROC curve analysis. It should be noted that NLR had the optimal cutoff value of 9.5 points before surgery by criterion complications/non-complications (AUC 0.803, 95% CI 0.742–0.844, p = 0.0011), and by criterion survivors/non-survivors it had the optimal cutoff value of 8.5 points (AUC 0.649, 95% CI 0.509–0.745, p = 0.045); NRI had the optimal cutoff value of 98.5 points (AUC 0.801, 95% CI 0.738–0.841, p = 0.0013) by criterion complications/non-complications, and by criterion survivors/non-survivors its had the optimal cutoff value of 83.55 points (AUC 0.810, 95% CI 0.732–0.873, p = 0.0008) (Fig. 2). Using the predetermined cutoffs for survivors and non-survivors, 24.8% and 9.3% it was noted that overall survival was significantly shorter among patients with an NLR ≥ 8.5 than patients with an NLR < 8.5 in univariate (HR, 1.63 [95% CI, 1.01–2.647]; p = 0.056) and in NRI ≤ 83.55 than in patients with an NRI > 83.55 (HR, 2.31 [95% CI, 1.431–3.736]; p = 0.0009) analyses (Table 4). However, 11.6% and 60.8% of patients with complications after surgery with an NLR ≥ 9.5 than patients and in NRI ≤ 98.8 (HR, 2.01 [95% CI, 1.247–3.250]; p = 0.006) unlike the patients without complications (HR, 1.8 [95% CI, 1.112–2.905]; p = 0.022).

Fig. 1
figure 1

The area under the receiver operating characteristics curve for albumin level and C-reactive protein level in patients with complications after surgery

Full size image
Table 3 Summary statistics of ratios
Full size table
Fig. 2
figure 2

The area under the receiver operating characteristics curve for Neutrophil-Lymphocyte Ratio in patients with complications (1) and those who died (2), as well as the Nutritional Risk Index in patients with complications (3) and those who died (4 ) after surgery

Full size image
Table 4 Univariate proportional hazard models for overall survival (n = 225)
Full size table

Following the retro selection of survival predictors (Table 4), only the NRI remained an independent risk factor for the operational system in the model (HR: 2.31, 95% CI: 1.431–3.736; p = 0.0009). Other analyses have shown no “dose effect” of NLR on prognosis (HR: 1.63, 95% CI: 1.01–2.647; p = 0.056). Patients with a moderate and severe violation by data NRI died more often within 90 days compared with patients with a normal and mild violation (4.1% vs. 0.98%, p = 0.022). During the first fifteen days post-operatively the survival of patients with and without elevated NRI was equal (Fig. 3).

Fig. 3
figure 3

Cumulative Kaplan-Meier survival estimate over 90 days after surgery in Neutrophil-Lymphocyte Ratio (NLR, 1), and in Nutritional Risk Index (NRI, 2) in patients who died

Full size image

Discussion

An analysis of the operations performed in three institutions demonstrated mortality in chronic pancreatitis and pancreatic pseudocysts in 1.4%, in chronic pancreatitis and the presence of an inflammatory mass mainly in the pancreatic head in 1.2%, and in cancer of the pancreatic head in 5.9%. That is, we have demonstrated that the use of various surgical interventions in this category of patients is not accompanied by high postoperative mortality, depending on the geographical location and volume of hospitals, but the number of development of postoperative complications is comparable to the figures given by other authors [44,45,46,47].

Our study examined the effect of preoperative NRI on 90-day mortality in a selected cohort of 225 patients, and this indicator, along with a high NLR, is also associated with the occurrence of postoperative complications in patients undergoing elective pancreatic surgery, as evidenced by studies conducted by other authors that different parameters in these patients were significantly associated with a higher rate of surgical complications and mortality [48,49,50,51].

When assessing the 90-day survival curve of NLR and NRI levels before surgery, it was determined that their values are statistically significant for predicting 90-day mortality after pancreatic surgery (p = 0.022). The optimal cutoff for NLR in the development of postoperative complications was determined before surgery and was 9.5 with a specificity of 85.3%, a sensitivity of 64.3% and an AUC of 0.803, which indicated a good sign of this selected indicator for the prognosis, but not satisfactory for the prognosis of mortality: the optimal cutoff was 8.5 with a specificity of 89.5%, a sensitivity of 35.7% and an AUC of 0.649. On the contrary, NRI had a good predictive value in the development of postoperative complications (optimum cutoff of 98.5 points with a specificity of 65.3%, a sensitivity of 95.2%, and an AUC of 0.801) and 90-day mortality with an optimal cutoff of 83.55 points, with a specificity of 60%, a sensitivity of 91.4%, and an AUC of 0.810. The combined use of the two indicators that were studied is possible as a screening tool to identify a group of patients with an increased risk of developing postoperative complications as well as 90-day mortality after surgery using NRI only.

In summary, the assessment of INR in patients undergoing pancreatic surgery for various pancreatic diseases was positive evaluated in this study to predict postoperative complications and mortality. It is helpful to determine NLI before surgery, although this indicator is not acceptable for predicting mortality up to 90-days after surgery based on our data.

Limitations of the research. This study has had several limitations. Firstly, it was a retrospective study, and our data was based on patient medical records that were processed. Secondly, not all patients were accounted for in this study, but only those with a full set of biomarkers in their study profile. Certainly, in the ignoring group have been patients who had died after surgery. As a result, bias in data selection could not be completely avoided and all results obtained require further verification in many more patients.

Conclusions

Differences in local resources, opportunities for diagnostic and treatment procedures, institutional preferences, different experiences, and the severity of the disease all contribute to the variability in the effectiveness of a particular approach to the treatment of patients with complicated chronic pancreatitis and cancer of the pancreas. As shown in this study, the development of local and systemic complications of this disease, due to the individual characteristics of the patient's body, is of paramount importance for achieving clinically significant success after surgery. Preoperatively, low NRI as well as high NLR were significantly associated with higher rates of postoperative complications, and low NRI was a predictor of mortality in patients undergoing direct pancreatic interventions. Thus, the preoperative NRI and NLR values can be used to detect patients with possible postoperative complications, as demonstrated in the three centres where these patients were operated on.

Availability of data and materials

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

AUC:

Area under curve

BMI:

Body Mass Index

CI:

95% Confidence interval

DPPHR:

Duodenum-preserving pancreatic head resection

HR:

Hazard Ratio

IQR:

Interquartile ranges

ISGLS:

International Study Group of Liver Surgery

ISGPF:

International Study Group of Pancreatic Fistula

NA:

Not applicable

NLR:

Neutrophil–lymphocyte ratio

NRI:

Nutritional risk index

ROC:

Receiver operating characteristic

References

  1. Cupp M, Cariolou M, Tzoulaki I, Aune D, Evangelou E, Berlanga-Taylor AJ. Neutrophil to lymphocyte ratio and cancer prognosis: an umbrella review of systematic reviews and meta-analyses of observational studies. BMC Med. 2020;18(1):360. https://doi.org/10.1186/s12916-020-01817-1.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Kim S, Eliot M, Koestler DC, Wu W, Kelsey KT. Association of Neutrophil-to-Lymphocyte Ratio With Mortality and Cardiovascular Disease in the Jackson Heart Study and Modification by the Duffy Antigen Variant. JAMA Cardiol. 2018;3(6):455–62. https://doi.org/10.1001/jamacardio.2018.1042.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Yu H, Jiang L, Yao L, Gan C, Han X, Liu R, Su N. Predictive value of the neutrophil-to-lymphocyte ratio and hemoglobin in systemic lupus erythematosus. Exp Ther Med. 2018;16(2):1547–53. https://doi.org/10.3892/etm.2018.6309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Russell CD, Parajuli A, Gale HJ, Bulteel NS, Schuetz P, de Jager CPC, Loonen AJM, Merekoulias GI, Baillie JK. The utility of peripheral blood leucocyte ratios as biomarkers in infectious diseases: A systematic review and meta-analysis. J Infect. 2019;78(5):339–48. https://doi.org/10.1016/j.jinf.2019.02.006.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Pascual-González Y, López-Sánchez M, Dorca J, Santos S. Defining the role of neutrophil-to-lymphocyte ratio in COPD: a systematic literature review. Int J Chron Obstruct Pulmon Dis. 2018;13:3651–62. https://doi.org/10.2147/COPD.S178068.

    Article  PubMed  PubMed Central  Google Scholar 

  6. An Peilin, Zhou Xuan, Du Yue, Zhao Jiangang, Song Aili, Liu Huan, Ma Fei and Huang Guowei. Association of Neutrophil-Lymphocyte Ratio with Mild Cognitive Impairment in Elderly Chinese Adults: A Case-control Study, Current Alzheimer Research 2019; 16(14). https://doi.org/10.2174/1567205017666200103110521

  7. D’Amico E, Zanghì A, Romano A, Sciandra M, Palumbo GAM, Patti F. The Neutrophil-to-Lymphocyte Ratio is Related to Disease Activity in Relapsing Remitting Multiple Sclerosis. Cells. 2019;8(10):1114. https://doi.org/10.3390/cells8101114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Steiner J, Frodl T, Schiltz K, Dobrowolny H, Jacobs R, Fernandes BS, Guest PC, Meyer-Lotz G, Borucki K, Bahn S, Bogerts B, Falkai P, Bernstein HG. Innate Immune Cells and C-Reactive Protein in Acute First-Episode Psychosis and Schizophrenia: Relationship to Psychopathology and Treatment. Schizophr Bull. 2020;46(2):363–73. https://doi.org/10.1093/schbul/sbz068.

    Article  PubMed  Google Scholar 

  9. Moutchia J, Pokharel P, Kerri A, McGaw K, Uchai S, Nji M, Goodman M. PLoS ONE. 2020;15(10):e0239802. https://doi.org/10.1371/journal.pone.0239802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Güell E, Martín-Fernandez M, De la Torre MC, Palomera E, Serra M, Martinez R, ManelSolsona M, Miró G, Vallès J, Fernández S, Cortés E, Ferrer V, Morales M, Yébenes JC, Almirall J. and Bermejo-Martin JFJ. Clin Med. 2019;8(5):754. https://doi.org/10.3390/jcm8050754.

    Article  Google Scholar 

  11. Hajibandeh S, Hajibandeh S, Hobbs N, Mansour M. Neutrophil-to-lymphocyte ratio predicts acute appendicitis and distinguishes between complicated and uncomplicated appendicitis: A systematic review and meta-analysis. Am J Surg. 2020;219(1):154–63. https://doi.org/10.1016/j.amjsurg.2019.04.018.

    Article  PubMed  Google Scholar 

  12. Begic-Kapetanovic S, Avdagic N, Zaciragic A, Hasic S, Babic N, Hadzimuratovic A. Could the neutrophil-to-lymphocyte ratio serve as a marker in the diagnosis and prediction of acute appendicitis complications in children? Arch Med Sci. 2021;17(6):1672–8. https://doi.org/10.5114/aoms.2019.87697.

    Article  PubMed  Google Scholar 

  13. Murakami Y, Saito H, Shimizu S, Kono Y, Shishido Y, Miyatani K, Matsunaga T, Fukumoto Y, Fujiwara Y. Neutrophil–to–Lymphocyte Ratio as a Prognostic Indicator in Patients With Unresectable Gastric Cancer. Anticancer Res. 2019;39:2583–9. https://doi.org/10.21873/anticanres.13381.

    Article  CAS  PubMed  Google Scholar 

  14. Nora I, Shridhar R, Huston J, Meredith K. The accuracy of neutrophil to lymphocyte ratio and platelet to lymphocyte ratio as a marker for gastrointestinal malignancies. J Gastrointest Oncol. 2018;9(5):972–8. https://doi.org/10.21037/jgo.2018.08.05.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pointer DT, Roife D, Powers BD, Murimwa G, Elessawy S, Thompson ZJ, Schell MJ, Hodul PJ, Pimiento JM, Fleming JB, Malafa MP. Neutrophil to lymphocyte ratio, not platelet to lymphocyte or lymphocyte to monocyte ratio, is predictive of patient survival after resection of early-stage pancreatic ductal adenocarcinoma. BMC Cancer. 2020;20:750. https://doi.org/10.1186/s12885-020-07182-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Nicolás-Ávila JÁ, Adrover JM, Hidalgo A. Neutrophils in homeostasis, immunity, and cancer. Immunity. 2017;46(1):15–28. https://doi.org/10.1016/j.immuni.2016.12.012.

    Article  CAS  PubMed  Google Scholar 

  17. Shaul ME, Fridlender ZG. Cancer related circulating and tumorassociated neutrophils – subtypes, sources and function. FEBS J. 2018;285(23):4316–42. https://doi.org/10.1111/febs.14524.

    Article  CAS  PubMed  Google Scholar 

  18. Bagante F, Tran TB, Postlewait LM, Maithel SK, Wang TS, Evans DB, Hatzaras I, Shenoy R, Phay JE, Keplinger K, Fields RC, Jin LX, Weber SM, Salem A, Sicklick JK, Gad S, Yopp AC, Mansour JC, Duh QY, Seiser N, Solorzano CC, Kiernan CM, Votanopoulos KI, Levine EA, Poultsides GA, Pawlik TM. Neutrophil-lymphocyte and platelet-lymphocyte ratio as predictors of disease specific survival after resection of adrenocortical carcinoma. J Surg Oncol. 2015;112(2):164–72. https://doi.org/10.1002/jso.23982.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Liao LJ, Hsu WL, Wang CT, Lo WC, Cheng PW, Shueng PW, Hsieh CH, Chiu YL, Lin YC. Prognostic impact of pre-treatment neutrophil-to-lymphocyte ratio (NLR) in nasopharyngeal carcinoma: A retrospective study of 180 Taiwanese patients. Clin Otolaryngol. 2018;43(2):463–9. https://doi.org/10.1111/coa.12992.

    Article  PubMed  Google Scholar 

  20. Borazan E, Balik AA, Bozdag Z, Arık MK, Aytekin A, Yılmaz L, Elçi M, Başkonuş İ. Assessment of the relationship between neutrophil lymphocyte ratio and prognostic factors in non-metastatic colorectal cancer. Turk J Surg. 2017;33(3):185–9. https://doi.org/10.5152/turkjsurg.2017.3528.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Wang YQ, Zhi QJ, Wang XY, Yue DS, Li K, Jiang RC. Prognostic value of combined platelet, fibrinogen, neutrophil to lymphocyte ratio and platelet to lymphocyte ratio in patients with lung adenosquamous cancer. Oncol Lett. 2017;14(4):4331–8. https://doi.org/10.3892/ol.2017.6660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bennett S, Murphy CF, Fanning M, Reynolds JV, Doyle SL, Donohoe CL. The impact of Nutrition and Gastrointestinal Symptoms on Health-related Quality of Life in Survivorship after Oesophageal Cancer Surgery. Clin Nutr Open Sci. 2022;41:44–61. https://doi.org/10.1016/j.nutos.2021.11.005.

    Article  Google Scholar 

  23. Gianotti L, Besselink MG, Sandini M, Hackert T, Conlon K, Gerritsen A, Griffin O, Fingerhut A, Probst P, Hilal MA, Marchegiani G, Nappo G, Zerbi A, Amodio A, Perinel J, Adham M, Raimondo M, Asbun HJ, Sato A, Takaori K, Shrikhande SV, Del Chiaro M, Bockhorn M, Izbicki JR, Dervenis C, Charnley RM, Martignoni ME, Friess H, de Pretis N, Radenkovic D, Montorsi M, Sarr MG, Vollmer CM, Frulloni L, Büchler MW, Bassi C. Nutritional support and therapy in pancreatic surgery: A position paper of the International Study Group on Pancreatic Surgery (ISGPS). Surgery. 2018;164(5):1035–48. https://doi.org/10.1016/j.surg.2018.05.040.

    Article  PubMed  Google Scholar 

  24. El Asmar A, Elie Ghabi E, Akl B, Malhab CA, Saber T, Eid S, Mahfouz E, Rahban H, El Rassi Z. Preoperative NLR and PLR are predictive of clinically relevant postoperative pancreatic fistula. Surgery in Practice and Science. 2022;10:100122. https://doi.org/10.1016/j.sipas.2022.100122.

    Article  Google Scholar 

  25. Kim H, Jung W, Shin YC, Han IW, Byun Y, Lee HW, Heo JS, Choi DW, Lim C-S. The diagnostic and prognostic values of inflammatory markers in intraductal papillary mucinous neoplasm. HPB. 2021;23(10):1623–8.https://doi.org/10.1016/j.hpb.2021.04.001.

    Article  PubMed  Google Scholar 

  26. Shi N, Zhang X, Zhu Y, Deng L, Li L, Zhu P, Xia L, Jin T, Ward T, Sztamary P, Cai W, Yao L, Yang X, Lin Z, Jiang K, Guo J, Yang X, Singh VK, Sutton R, Lu N, Windsor JA, He W, Huang W, Xia Q. Predicting persistent organ failure on admission in patients with acute pancreatitis: development and validation of a mobile nomogram. HPB. 2022;24(1):1907–20. https://doi.org/10.1016/j.hpb.2022.05.1347.

    Article  PubMed  Google Scholar 

  27. PaProbst P, Fuchs J, Schoen MR, Polychronidis G, Forster T, Mehrabi A, Ulrich A, Knebel P, Hoffmann K. Nutritional risk in major abdominal surgery: NURIMAS Liver (DRKS00010923) – protocol of a prospective observational trial to evaluate the prognostic value of different nutritional scores in hepatic surgery. Int J Surg Protoc. 2017;6:5–10. https://doi.org/10.1016/j.isjp.2017.09.001.

    Article  Google Scholar 

  28. Buettner S, Galjart B, van Vugt JLA, Bagante F, Alexandrescu S, Marques HP, Lamelas J, Aldrighetti L, Gamblin TC, Maithel SK, Pulitano C, Margonis GA, Weiss M, Bauer TW, Shen F, Poultsides GA, Marsh JW. IJzermans JNM, Groot Koerkamp B, Pawlik TM. Performance of prognostic scores and staging systems in predicting long-term survival outcomes after surgery for intrahepatic cholangiocarcinoma J Surg Oncol. 2017;116:1085–95. https://doi.org/10.1002/jso.24759.

    Article  CAS  PubMed  Google Scholar 

  29. Hyder O, Marques H, Pulitano C, Marsh JW, Alexandrescu S, Bauer TW, Gamblin TC, Sotiropoulos GC, Paul A, Barroso E, Clary BM, Aldrighetti L, Ferrone CR, Zhu AX, Popescu I, Gigot JF, Mentha G, Feng S, Pawlik TM. A nomogram to predict long-term survival after resection for intrahepatic cholangiocarcinoma: an Eastern and Western experience. JAMA Surg. 2014;149(5):432–8. https://doi.org/10.1001/jamasurg.2013.5168.

    Article  PubMed  Google Scholar 

  30. Templeton AJ, McNamara MG, Vera-Badillo FE, Aneja P, Ocaña A, Leibowitz-Amit R, Sonpavde G, Knox JJ, Tran B, Tannock IF, Amir E. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst. 2014;106(6):dju124. https://doi.org/10.1093/jnci/dju124. PMID: 24875653.

    Article  CAS  PubMed  Google Scholar 

  31. Ergenç H, Ertürk Z, Eminler AT, Cinemre H. Diagnostic and Prognostic Value of Neutrophil/Lymphocyte Ratio and Platelet/Lymphocyte Ratios on Acute Pancreatitis Patients. OTJHS. 2022;7(1):80–5. https://doi.org/10.26453/otjhs.1022717.

    Article  Google Scholar 

  32. Wang Y, Zhi Q, Wang X, Yue D, Li K, Jiang R. Prognostic value of combined platelet, fibrinogen, neutrophil to lymphocyte ratio and platelet to lymphocyte ratio in patients with lung adenosquamous cancer. Oncol Lett. 2017;14:4331–8. https://doi.org/10.3892/ol.2017.6660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Romano L, Giuliani A, Tomarelli C, Nervini A, Lazzarin G, Pessia B, Vicentini V, Carlei F, Schietroma M. Impact of Preoperative Neutrophil-Lymphocyte and Platelet-Lymphocyte Ratios on Long-Term Survival in Patients with Operable Pancreatic Ductal Adenocarcinoma. Med Princ Pract. 2022;31:586–94. https://doi.org/10.1159/000527360.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Rivelsrud M, Paur I, Sygnestveit K, Nilsen RM, Tangvik RJ. Nutritional treatment is associated with longer survival in patients with pancreatic disease and concomitant risk of malnutrition. Clin Nutr. 2021;40(4):2128–37. https://doi.org/10.1016/j.clnu.2020.09.037.

    Article  CAS  PubMed  Google Scholar 

  35. Cañamares-Orbis P, García-Rayado G, Alfaro-Almajano E. Nutritional Support in Pancreatic Diseases. Nutrients. 2022;14:4570. https://doi.org/10.3390/nu14214570.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Cong K, Chunwei G. Exploration of three different nutritional scores in predicting postoperative complications after pancreaticoduodenectomy. Nutr Hosp. 2022;39(1):101–10. https://doi.org/10.20960/nh.03740.

    Article  PubMed  Google Scholar 

  37. Yamamoto M, Kawaguchi Y, Ichida A, Matsumura M, Sakamoto Y, Arita J, Akamatsu N, Kaneko J, Kokudo N, Hasegawa K. Evaluation of preoperative nutritional variables to predict postoperative complications after pancreaticoduodenectomy. Nutrition. 2019;67–68:100006.

    Article  CAS  Google Scholar 

  38. Zahorec R. Ratio of Neutrophil to Lymphocyte Counts-Rapid and Simple Parameter of Systemic Inflammation and Stress in Critically Ill. Bratisl Lek Listy. 2001;102(1):5–14.

    CAS  PubMed  Google Scholar 

  39. Yang AP, Liu JP, Tao WQ, Li HM. The diagnostic and predictive role of NLR, d-NLR and PLR in COVID-19 patients. Int Immunopharmacol. 2020;84:106504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Buzby GP, Williford WO, Peterson OL, Crosby LO, Page CP, Reinhardt GF, Mullen JL. A randomized clinical trial of total parenteral nutrition in malnourished surgical patients: the rationale and impact of previous clinical trials and pilot study on protocol design. Am J Clin Nutr. 1988;47(2 Suppl):357–65. https://doi.org/10.1093/ajcn/47.2.357.

    Article  CAS  PubMed  Google Scholar 

  41. Prasad N, Sinha A, Gupta A, Bhadauria D, Manjunath R, Kaul A, Sharma RK. Validity of nutrition risk index as a malnutrition screening tool compared with subjective global assessment in end-stage renal disease patients on peritoneal dialysis. Indian J Nephrol. 2016;26(1):27–32. https://doi.org/10.4103/0971-4065.158449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Brooke-Smith M, Figueras J, Ullah S, Rees M, Vauthey JN, Hugh TJ, Garden OJ, Fan ST, Crawford M, Makuuchi M, Yokoyama Y, Büchler M, Weitz J, Padbury R. Prospective evaluation of the International Study Group for Liver Surgery definition of bile leak after a liver resection and the role of routine operative drainage: an international multicentre study. HPB (Oxford). 2015;17(1):46–51. https://doi.org/10.1111/hpb.12322.

    Article  PubMed  Google Scholar 

  43. Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hila l M, Adham M, Allen P, Andersson R, Asbun HJ, Besselink MG, Conlon K, Del Chiaro M, Falconi M, Fernandez-Cruz L, Fernandez-Del Castillo C, Fingerhut A, Friess H, Gouma DJ, Hackert T, Izbicki J, Lillemoe KD, Neoptolemos JP, Olah A, Schulick R, Shrikhande SV, Takada T, Takaori K, Traverso W, Vollmer CR, Wolfgang CL, Yeo CJ, Salvia R, Buchler M. International Study Group on Pancreatic Surgery (ISGPS). The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery. 2017;161(3):584-591. https://doi.org/10.1016/j.surg.2016.11.014.

  44. Karim SAM, Abdulla KS, Abdulkarim QH, Rahim FH. The outcomes and complications of pancreaticoduodenectomy (Whipple procedure): Cross sectional study. Int J Surg. 2018;52:383–7. https://doi.org/10.1016/j.ijsu.2018.01.041.

    Article  PubMed  Google Scholar 

  45. Lubrano J, Bachelier P, Paye F, Le Treut YP, Chiche L, Sa-Cunha A, Turrini O, Menahem B, Launoy G, Delpero JR. Severe postoperative complications decrease overall and disease free survival in pancreatic ductal adenocarcinoma after pancreaticoduodenectomy. Eur J Surg Oncol. 2018;44(7):1078–82. https://doi.org/10.1016/j.ejso.2018.03.024.

    Article  PubMed  Google Scholar 

  46. Petrova E, Lapshyn H, Bausch D, D'Haese J, Werner J, Klier T, Nüssler NC, Gaedcke J, Ghadimi M, Uhl W, Belyaev O, Kantor O, Baker M, Keck T, Wellner UF. StuDoQ|Pancreas study group and members of StuDoQ|Pancreas registry of the German Society for General and Visceral Surgery (DGAV). Risk stratification for postoperative pancreatic fistula using the pancreatic surgery registry StuDoQ|Pancreas of the German Society for General and Visceral Surgery. Pancreatology. 2019 19(1):17-25 https://doi.org/10.1016/j.pan.2018.11.008.

  47. Keung EZ, Asare EA, Chiang YJ, Prakash LR, Rajkot N, Torres KE, Hunt KK, Feig BW, Cormier JN, Roland CL, Katz MHG, Lee JE, Tzeng CD. Postoperative pancreatic fistula after distal pancreatectomy for non-pancreas retroperitoneal tumor resection. Am J Surg. 2020;220(1):140–6. https://doi.org/10.1016/j.amjsurg.2019.11.026.

    Article  PubMed  Google Scholar 

  48. Andreou A, Aeschbacher P, Candinas D, Gloor B. The Impact of Patient Age ≥80 Years on Postoperative Outcomes and Treatment Costs Following Pancreatic Surgery. J Clin Med. 2021;10(4):696. https://doi.org/10.3390/jcm10040696.

    Article  PubMed  PubMed Central  Google Scholar 

  49. De Schryver N, Wittebole X, Hubert C, Gigot J-F, Laterre P-F, Castanares-Zapatero D. Early hyperlactatemia predicts pancreatic fistula after surgery. BMC Anesthesiol. 2015;15:109. https://doi.org/10.1186/s12871-015-0093-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lermite E, Sommacale D, Piardi T, Arnaud JP, Sauvanet A, Dejong CH, Pessaux P. Complications after pancreatic resection: diagnosis, prevention and management. Clin Res Hepatol Gastroenterol. 2013;37(3):230–9. https://doi.org/10.1016/j.clinre.2013.01.003.

    Article  PubMed  Google Scholar 

  51. van Genderen ME, Paauwe J, de Jonge J, van der Valk RJ, Lima A, Bakker J, van Bommel J. Clinical assessment of peripheral perfusion to predict postoperative complications after major abdominal surgery early: a prospective observational study in adults. Crit Care. 2014;18(3):R114. https://doi.org/10.1186/cc13905.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the patients and clinical staff who gave up their time to take part in this clinical study.

Funding

This research was part of the research work of the Kharkiv National Medical University “Improvement and development of methods for diagnosis and surgical treatment of diseases and injuries of the abdominal cavity and chest, vessels of the upper and lower extremities using mini-invasive techniques in patients at high risk of postoperative complications” The number of state registration is 0116u00499. This research received no external funding.

Author information

Authors and Affiliations

  1. Department of Surgery No.2, Kharkiv National Medical University, Nezalezhnosti Avenue, Kharkiv, 61022, Ukraine

    Igor A. Kryvoruchko, Plamen Staikov & Andrij Honcharov

  2. Krankenhaus Sachsenhausen, 60594, SchulstraßeFrankfurt Am Main, Germany

    Plamen Staikov

  3. Institute General and Emergency Surgery Named After V.T. Zaitcev of the National Academy of Medical Sciences of Ukraine, Balakireva Entry, Kharkiv, 61103, Ukraine

    Valeriy V. Boyko

  4. Department of Surgery No.1, Kharkiv National Medical University, Balakireva Entry, Kharkiv, 61103, Ukraine

    Valeriy V. Boyko & Yulia V. Ivanova

  5. Department of Surgery Macerata Hospital, Santa Lucia Street, 62100, Macerata, Italy

    Massimo Sartelli

  6. Institute of Bio-Stem Cell Rehabilitation, Ukraine Association of Biobank, Puskinska Str, Kharkiv, 61022, Ukraine

    Massimo Sartelli & Svetlana Gramatiuk

  7. International Biobanking and Education, Medical University of Graz, Elisabethstraße, 8010, Graz, Austria

    Svetlana Gramatiuk & Karine Sargsyan

Authors
  1. Igor A. Kryvoruchko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Plamen Staikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valeriy V. Boyko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Massimo Sartelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yulia V. Ivanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrij Honcharov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Svetlana Gramatiuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Karine Sargsyan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

IK, PS, and VB constructed the study design. IK, VB, and MS contributed to data interpretation and manuscript drafting. YI, SG, and AH contributed to the statistical analysis. IK and SG prepared figures. IK, PS, YI, SG, and AH participated in the clinical investigation and contributed to the epidemiological data collection. IK and KS revised the manuscript.

Corresponding author

Correspondence to Igor A. Kryvoruchko.

Ethics declarations

Ethics approval and consent to participate

This two-institution retrospective cohort study was handled in accordance with the Declaration of Helsinki. The use of registered data follows the General Data Protection Regulation of the European Union. The study and the use of data were consented to by the Ethics Committee of Kharkiv National Medical University, Ukraine ((Protocol No. 6, November 11, 2022). The number of state registration is 0116u00499. All patients or their authorizers gave written informed consent before the operation.

Consent for publication

The manuscript is approved for publication by all the authors. Written informed consent was obtained from the patients and/or their legal guardians for publication, and any accompanying images, sex, age of these patients.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

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

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kryvoruchko, I.A., Staikov, P., Boyko, V.V. et al. Physiological stress level and screening for malnutrition as preoperative predictors of postoperative complications in pancreatic surgery: a retrospective study. BMC Surg 23, 156 (2023). https://doi.org/10.1186/s12893-023-02062-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12893-023-02062-y

Keywords

BMC Surgery

ISSN: 1471-2482

Contact us