Review ArticleReview
Open Access

Clinical Impact of Nutrition and Inflammation Assessment Tools in Pancreatic Cancer Treatment

TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, YASUSHI RINO and TAKASHI OSHIMA
Anticancer Research September 2023, 43 (9) 3849-3860; DOI: https://doi.org/10.21873/anticanres.16572

Abstract

Perioperative adjuvant treatment and complete resection is the standard treatment for resectable pancreatic cancer and systemic chemotherapy is standard treatment for unresectable pancreatic cancer. To improve the survival of patients with pancreatic cancer, it is necessary to identify promising biomarkers to optimize the treatment. The availability of biomarkers may allow patients to receive a more aggressive or less toxic treatment. Recent studies showed that the inflammatory and nutritional status perioperatively and/or during chemotherapy affect short and long-term oncological outcomes in pancreatic cancer. Introduction of inflammatory and nutritional status evaluation in pancreatic cancer treatment might improve the postoperative surgical complications or chemotherapy-induced adverse events. However, to introduce these various nutritional and inflammation assessment tools in daily clinical practice, it is necessary to understand the characteristics of each nutrition and inflammation assessment tool. This review summarizes the background, current status, and future perspectives of nutrition and inflammation assessment tools in pancreatic cancer treatment.

Key Words:

Pancreatic cancer is one of the leading cancers in the world. Every year 496,000 patients suffer, and 466,000 patients die due to pancreatic cancer (1, 2). Perioperative adjuvant treatment and complete resection is the standard treatment for resectable pancreatic cancer and systemic chemotherapy is standard treatment for unresectable pancreatic cancer (3, 4). Although the survival rate after treatment is gradually improving, 5-years survival rates of both resectable and unresectable pancreatic cancer is poor. To improve the survival of patients with pancreatic cancer, it is necessary to identify a valid biomarker to optimize treatment. Such biomarker can guide treatment and the patients can receive the more aggressive or less toxic treatment.

Recent studies showed that inflammatory and nutritional status perioperatively and/or during chemotherapy affect for short and long-term oncological outcomes in various malignancies (5, 6). In pancreatic cancer, the usefulness of several inflammation and nutritional status indices, such as Glasgow Prognostic Score, Prognostic Nutritional Index, and Controlling Nutritional Status, have been reported (7-10). Introduction of inflammatory and nutritional status evaluation in pancreatic cancer treatment might improve the postoperative surgical complications or chemotherapy-related adverse events. However, to introduce these nutritional and inflammation assessment tools in daily clinical practice, it is necessary to understand the characteristics of each nutrition and inflammation assessment tool.

This review summarizes the background, current status, and future perspectives of nutrition and inflammation assessment tools in pancreatic cancer treatment.

Clinical Impact of Glasgow Prognostic Score (GPS) and Modified Glasgow Prognostic Score (mGPS) in Pancreatic Cancer Treatment

Glasgow Prognostic Score (GPS) and modified Glasgow Prognostic Score (mGPS) are calculated by the serum C-reactive protein level and serum albumin level. The GPS is categorized as follows: score 2 cases have both elevated CRP (>10 mg/l) and low albumin (<35 g/l); score 1 cases have elevated CRP (>10 mg/l) or low albumin (<35 g/l); and score 0 cases have both normal CRP (≤10 mg/l) and normal albumin (≥35 g/l). There were 19 studies evaluating the clinical impacts of GPS/mGPS in pancreatic cancer (11-29). The first study was reported in 2011. Jamieson evaluated the prognostic value of mGPS in 135 pancreatic cancer patients who received pancreaticoduodenectomy. They found that elevated GPS showed a clear difference in median overall survival. Median overall survival was 26.7 months in the mGPS 0 group, 16.5 months in mGPS 1 group, and 13.1 months in mGPS 2 group. They also found that elevated mGPS was one of the significant independent risk factors for poor overall survival (HR=2.26, 95%CI=1.43-3.57, p<0.001). So far, 9 studies used GPS and 10 studies used mGPS. Hazard ratio of GPS/mGPS was 0.4 to 4.93 in patients who received chemotherapy or chemoradiation therapy and 1.723 to 3.642 in patients who received curative resection. Previous studies evaluated the clinical impact of GPS/mGPS on long-term oncological outcomes (Table I). Among these studies, high score of GPS/mGPS was associated with poor prognosis. Further studies are needed to evaluate ad clarify the clinical impact of GPS/mGPS on short-term oncological outcomes, such as occurrence of postoperative surgical complications and continuation of perioperative adjuvant treatment.

View this table:
Table I.

Clinical impacts of Glasgow Prognostic Score (GPS) and modified Glasgow Prognostic Score (mGPS) in pancreatic cancer treatment.

Clinical Impact of Neutrophil to Lymphocyte Ratio (NLR) in Pancreatic Cancer Treatment

Neutrophil to lymphocyte ratio (NLR) is calculated using the serum neutrophil and lymphocyte numbers. The first study of NLR in pancreatic cancer was reported in 2010. In resectable setting, Bhati evaluated the prognostic value of NLR in 84 patients with pancreatic cancer who received pancreaticoduodenectomy (30). They found that elevated NLR showed a clear difference in median overall survival. Median overall survival was 5.9 months in the group with NLR of more than 4.0, 17.0 months in the group with NLR of 3.0 to 4.0, and 13.7 months in the group with NLR of less than 3.0. They also found that elevated NLR was one of the significant independent risk factors for poor overall survival (HR=1.784, 95%CI=1.085-2.934, p=0.023). In metastatic setting, one study evaluated the prognostic value of NLR in 95 pancreatic cancer patients who received chemotherapy (31). They found that elevated NLR (cutoff value 5) clearly showed a clear difference in median overall survival. Median overall survival was 2.4 months in the high NLR group and 7.7 months in the low NLR group. They also demonstrated that elevated NLR was one of the significant independent risk factors for poor overall survival (HR=4.489, 95%CI=1.372-14.692, p=0.013). So far, 44 studies showed the significant prognostic value of NLR in pancreatic cancer (32-73) (Table II). Hazard ratio of NLR was 0.31 to 9.13 in patients who received chemotherapy or chemoradiation therapy and 1.581 to 5.35 in patients who received curative resection. Previous studies set the cutoff value of NLR at 1.7 to 14.1. Change of NLR during the perioperative or chemotherapy treatment period affects long-term oncological outcomes. Further studies are needed to clarify this issue.

View this table:
Table II.

Clinical impacts of neutrophil to lymphocyte ratio (NLR) in pancreatic cancer treatment.

Clinical Impact of Prognostic Nutritional Index (PNI) in Pancreatic Cancer Treatment

The prognostic nutritional index (PNI) is calculated using the serum albumin level and the number of serum lymphocytes. The first study of PNI in pancreatic cancer was reported in 2010. Kanda evaluated the prognostic value of preoperative PNI in 268 patients with pancreatic cancer who received pancreaticoduodenectomy (74). They found that decreased PNI (cutoff value 45) clearly showed a clear difference in median overall survival. Median overall survival was 9.0 months in the low PNI group and 15.7 months in high PNI group. They found that decreased PNI was one of the significant independent risk factors for poor overall survival (HR=2.06, 95%CI=1.46-2.91, p<0.001). In addition, they demonstrated that preoperative PNI status affects the occurrence of postoperative surgical complications (POC). Incidence of the POC was 45% in the low PNI group and 27.3% in high PNI group (p=0.007). PNI was one of the significant predictors of POC. So far, 15 studies examined the significant prognostic value of PNI in pancreatic cancer (75-90) (Table III). Hazard ratio of PNI was 0.627 to 3.53 in patients who received chemotherapy and 0.359 to 6.803 in patients who received curative resection. Previous studies set the cutoff value of PNI at 36 to 53. Interestingly, there were 2 studies evaluating the clinical effects of PNI on continuation of adjuvant chemotherapy and postoperative deep venous thrombosis (DVT). Yamada et al. clarified the risk factors of continuation of postoperative adjuvant chemotherapy in 121 pancreatic cancer patients. They found that PNI (at first visit) was significantly different between the adjuvant chemotherapy complete group and adjuvant chemotherapy incomplete group (46.8 vs. 44.3, p=0.017). Moreover, PNI (at first visit) was one of the significant risk factors for completion of adjuvant chemotherapy (OR=0.92, 95%CI=0.84-0.99, p=0.041). In addition, Iguchi et al. evaluated preoperative PNI as a predictor of development of DVT in 100 patients with pancreatic cancer. When comparing preoperative PNI between non-DVT and DVT-groups, there was a marginally significant difference. Mean PNI was 46.4 in the DVT group and 43.7 in non-DVT group (0.079). They found that decreased PNI (cutoff value at 44.3) was one of the significant independent risk factors for DVT (OR=31.3, 95%CI=2.0-486.4, p=0.014). These results need to be confirmed by other studies.

View this table:
Table III.

Clinical impacts of prognostic nutritional index (PNI) in pancreatic cancer treatment.

Clinical Impact of C-reactive Protein to Albumin Ratio (CAR) in Pancreatic Cancer Treatment

C-reactive protein to albumin ratio (CAR) is calculated using the levels of serum C-reactive protein and albumin. The first study of CAR in pancreatic cancer was reported in 2016. Wu evaluated the prognostic value of CAR in 386 patients with pancreatic cancer (91). According to receiver operating characteristics curves, they set the cutoff value of CAR at 0.180. They found that CAR high group (CAR ≥0.18) had significantly worse prognosis than the CAR low group (CAR <0.18). They found that high CAR was one of the significant independent risk factors for poor overall survival (HR=2.07, 95%CI=1.59-2.70, p<0.001). So far, 9 studies examined the prognostic value of PNI in pancreatic cancer (92-101) (Table IV). The HR of PNI was 1.45 to 4.00. Previous studies set the cutoff value of CAR at 0.03 to 3.85. There were 2 studies evaluating the impacts of CAR on the occurrence postoperative pancreatic fistula and pathological response. Funamizu et al. evaluated the clinical impact of CAR on postoperative pancreatic fistula (POPF) in 72 patients with pancreatic cancer who received distal pancreatomy. When comparing CAR between the POPF and non-POPF groups, there was a statistically significant difference in mean preoperative CAR (0.35 vs. 0.03, p=0.001). They demonstrated that high CAR (≥0.05) was one of the risk factors of POPE (OR=12.419, 95%CI=2.687-57.393, p=0.013). Moreover, Mori et al. evaluated the clinical impact of CAR on pathological response in 81 patients with pancreatic cancer who received neoadjuvant gemcitabine plus S-1 chemotherapy. They found that CAR >0.062 was independent predictor for Evans I disease (OR=5.310, 95%CI=1.354-20.829, p=0.017). They concluded that preoperative CAR was associated with poor pathological response.

View this table:
Table IV.

Clinical impacts of C-reactive protein to albumin ratio (CAR) in pancreatic cancer treatment.

Clinical Impact of Controlling Nutritional Status (CONUT) in Pancreatic Cancer Treatment

Controlling nutritional status (CONUT) is calculated using serum albumin and serum cholesterol levels, and total lymphocyte count. The nutritional status of patients with CONUT scores of 0-1, 2-4, 5-8, and 9-12 is normal, light, moderate, and severe, respectively. The higher the CONUT score, the worse the nutritional status. The first study of CONUT in pancreatic cancer was reported in 2018 (102). Kato et al. evaluated the prognostic value of CONUT in 344 patients with pancreatic cancer who received pancreatomy. They set the cutoff value of CONUT at 4. Median OS was 26.8 months in the CONUT low group (CONUT <4) and 18.0 months in the CONUT high group (CONUT ≥4); The difference was statistically significant. They clarified that high CONUT was one of the significant independent risk factors for poor overall survival (HR=1.64, 95%CI=1.19-2.26, p=0.003). So far, 6 studies examined the prognostic value of CONUT in pancreatic cancer (103-107) (Table V). Among them, 5 studies evaluated the clinical impact of CONUT on resectable cancer and one study on unresectable cancer. In the resectable setting, the HR of CONUT was 1.145 to 4 and the cutoff value 2 to 4. One study examined the association between CONUT and postoperative surgical complications (POC). Shiihara et al. evaluated the predictive value of CONUT for POC in 206 patients with pancreatic cancer who received pancreaticoduodenectomy. They reported that incidence of postoperative complications (Clavien–Dindo grade ≥IIIb) was significantly higher in the CONUT high group (CONUT ≥5) than in the CONUT low group (CONUT 0-4) (20.0% vs. 3.1%, p=0.020). They demonstrated that high CONUT was one of the risk factors of POC (OR=5.89, 95%CI=1.01-34.5, p=0.038).

View this table:
Table V.

Clinical impacts of Controlling Nutritional Status (CONUT) in pancreatic cancer treatment.

Clinical Impact of Platelet to Lymphocyte Ratio (PLR) in Pancreatic Cancer Treatment

Platelet to lymphocyte ratio (PLR) is calculated using the platelet and total lymphocyte count. The first study of PLR in pancreatic cancer was reported in 2015. Shirai evaluated the prognostic value of PLR in 131 patients with pancreatic cancer who received pancreatomy (108). They set the cutoff value of PLR at 150. PLR status was a significant risk factor for both OS (HR=1.688, 95%CI=1.045-2.726, p=0.032) and RFS (HR=1.528, 95%CI=1.005-2.322, p=0.047). So far, 5 studies examined the significant prognostic value of PLR in pancreatic cancer (109-112) (Table VI); three for resectable and two for unresectable cancer. The HR of PLR was 1.345 to 3.137 and the cutoff value of PLR was 117 to 250. However, all studies examined the clinical impact on long-term oncological outcomes. Therefore, further studies are needed to evaluate the impact of PLR on short-term oncological outcomes, such as incidence of postoperative surgical complications, continuation of chemotherapy, and incidence of adverse events due to chemotherapy.

View this table:
Table VI.

Clinical impacts of platelet to lymphocyte ratio (PLR) in pancreatic cancer treatment.

The Future Application of Tools for the Assessment of Nutrition and Inflammation in Pancreatic Cancer Treatment

Various studies have evaluated different nutrition and inflammation assessment tools in pancreatic cancer treatment. Before they can be applied in the clinical setting, further studies are needed to determine the optimal cutoff value of each tool as various cutoff values have been reported. These differences arise from heterogeneity in patient background factors as well as the methods of treatment and evaluation. In addition, the optimal timing for the application of each tool remains to be determined. In previous reports, assessments using each tool were applied at different time points, including the diagnosis, first visit, preoperatively, postoperatively, and before the initiation of chemotherapy. Thus, the optimal timing for the application of these tools should be determined. Finally, the underlying mechanisms through which nutrition and inflammation affect gastric cancer prognosis remain to be elucidated. The nutrition and inflammation status was recently reported to impact postoperative surgical complications, the introduction of chemotherapy, and adverse events of chemotherapy. Postoperative surgical complications and chemotherapy management have previously been reported to affect the survival of patients with pancreatic cancer. However, the precise mechanisms through which the nutritional and inflammatory status, as assessed by these tools, influence the prognosis of patients with pancreatic cancer remains unclear.

Conclusion

The nutritional and inflammatory status may have some clinical influence on both the short- and long-term oncological outcomes in patients with pancreatic cancer. However, the optimal cutoff values of each nutrition and inflammation assessment tool are unclear and the mechanism through which these parameters influence the prognosis is unclear. To optimize the nutrition and inflammation assessment tools for pancreatic cancer patients, it is necessary to clarify these points in further studies.

Acknowledgements

This study was supported, in part, by the non-profit organization Yokoyama surgical research group (YSRG).

Footnotes

  • Authors’ Contributions

    TA, IH, and YM made substantial contributions to the concept and design. TA, TO and YR made substantial contributions to the acquisition, analysis, and interpretation of the data. TA, IH, YM, and YR were involved in drafting the article or revising it critically for important intellectual content. TA and IH give their final approval of the version to be published.

  • Conflicts of Interest

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

  • Received June 12, 2023.
  • Revision received July 13, 2023.
  • Accepted July 14, 2023.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Clinical Impact of Nutrition and Inflammation Assessment Tools in Pancreatic Cancer Treatment
TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, YASUSHI RINO, TAKASHI OSHIMA
Anticancer Research Sep 2023, 43 (9) 3849-3860; DOI: 10.21873/anticanres.16572
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