Metastatik Pankreas Kanseri Olan Hastalarda GRIm Skoru ile Prognoz Arasındaki İlişki

Öz

Amaç: Laktat dehidrogenaz (LDH), albümin ve nötrofil/lenfosit oranını (NLR) birleştiren Gustave Roussy Immün (GRIm) skoru, pratik bir immün–nutrisyonel indeks olarak öne çıkmıştır; ancak metastatik pankreas adenokarsinomunda kanıtlar sınırlıdır. Bu çalışma, sistemik tedavi alan hastalarda GRIm skorunun progresyonsuz sağkalım (PFS) ve genel sağkalım (OS) üzerindeki prognostik değerini değerlendirmeyi amaçladı. Yöntemler: Bu retrospektif çalışma, 2020–2024 yılları arasında sistemik tedavi alan metastatik pankreas kanseri tanılı 94 hastayı içerdi. GRIm skorunu hesaplamak için başlangıç LDH, albümin ve nötrofil-lenfosit oranı (NLR) kullanıldı. Her olumsuz faktör (yüksek LDH, hipoalbüminemi ve artmış NLR) için bir puan verildi ve 0 ile 3 arasında değişen toplam bir skor elde edildi; hastalar daha sonra düşük (0-1) veya yüksek (2-3) GRIm olarak kategorize edildi. Sonuçlar: Ortalama yaş 59.9 ± 10.1 yıl olup 59 hasta erkekti (%62.8). GRIm skoru dağılımı %33.0’da 0, %42.6’da 1 ve %24.5’te 2–3 idi. Medyan takip süresi 9 ay (aralık, 1–36) olup progresyon %74.5’te, mortalite %84’te görüldü. Medyan PFS 5.0 ay (IQR, 1.0–10.0) idi. GRIm arttıkça sonlanım noktaları basamaklı olarak kötüleşti: GRIm 0, 1 ve 2–3 için medyan PFS sırasıyla 9, 6 ve 2 ay idi (p<0.001) ve medyan OS 14, 10 ve 4 ay idi (p<0.001). Çok değişkenli analizlerde, GRIm 2–3, GRIm 0’a kıyasla hem progresyonu (PFS: HR 3.64, %95 GA 1.95–6.82, p<0.001) hem de ölümü (OS: HR 2.15, %95 GA 1.09–4.22, p=0.027) bağımsız olarak öngördü; buna karşın GRIm 1 anlamlı değildi. Sonuç: Yüksek GRIm skoru; hastalık evresi, metastatik yük ve tedavi rejiminden bağımsız olarak daha kötü PFS ve OS ile ilişkiliydi. GRIm skoru, metastatik pankreas kanserinde basit ve pratik bir prognostik biyobelirteçtir.

Anahtar Kelimeler

• pankreas kanseri
• metastatic
• GRIm skoru
• progresyonsuz sağkalım
• genel sağkalım

The Relationship Between GRIm Score and Prognosis in Patients with Metastatic Pancreatic Cancer

Öz

Aims: The Gustave Roussy Immune (GRIm) score, integrating lactate dehydrogenase (LDH), albumin, and neutrophil-to-lymphocyte ratio (NLR), has emerged as a practical immune–nutritional index; however, evidence in metastatic pancreatic adenocarcinoma remains limited. This study aimed to evaluate the prognostic value of the GRIm score for progression-free survival (PFS) and overall survival (OS) in patients receiving systemic therapy. Methods: This retrospective study included 94 patients diagnosed with metastatic pancreatic cancer who received systemic therapy between 2020 and 2024. Baseline LDH, albumin, and neutrophil-to-lymphocyte ratio (NLR) were used to compute the GRIm score. One point was assigned for each adverse factor (elevated LDH, hypoalbuminemia, and increased NLR), yielding a total score ranging from 0 to 3; patients were then categorized as low (0–1) or high (2–3) GRIm. Results: The mean age was 59.9 ± 10.1 years and 59 patients were men (62.8%). GRIm score distribution was 0 in 33.0%, 1 in 42.6%, and 2–3 in 24.5%. Median follow-up was 9 months (range, 1–36); progression occurred in 74.5% and mortality in 84%. Median PFS was 5.0 months (IQR, 1.0–10.0). Outcomes deteriorated stepwise with increasing GRIm: median PFS was 9, 6, and 2 months for GRIm 0, 1, and 2–3, respectively (p<0.001), and median OS was 14, 10, and 4 months (p<0.001). In multivariable analyses, GRIm 2–3 independently predicted both progression (PFS: HR 3.64, 95% CI 1.95–6.82, p<0.001) and death (OS: HR 2.15, 95% CI 1.09–4.22, p=0.027) compared with GRIm 0, whereas GRIm 1 was not significant. Conclusion: A high GRIm score was associated with worse PFS and OS, independent of disease stage, metastatic burden, and treatment regimen. The GRIm score is a simple, practical prognostic biomarker in metastatic pancreatic cancer.

Anahtar Kelimeler

• pancreatic cancer
• metastatic
• GRIm score
• progression-free survival
• overall survival

Kaynakça

1. McGuigan A, Kelly P, Turkington RC, Jones C, Coleman HG, McCain RS. Pancreatic cancer: A review of clinical diagnosis, epidemiology, treatment and outcomes. World J Gastroenterol 2018; 24: 4846-61.
2. Lai ECH, Ung AKY. Update on management of pancreatic cancer: a literature review. Chin Clin Oncol 2024; 13: 41.
3. Shinde RS, Bhandare M, Chaudhari V, Shrikhande SV. Cutting-edge strategies for borderline resectable pancreatic cancer. Ann Gastroenterol Surg 2019; 3: 368-72.
4. Uesato Y, Sasahira N, Ozaka M, Sasaki T, Takatsuki M, Zembutsu H. Evaluation of circulating tumor DNA as a biomarker in pancreatic cancer with liver metastasis. PLoS One 2020; 15: e0235623.
5. Bigot F, Castanon E, Baldini C, Hollebecque A, Carmona A, Postel-Vinay S et al. Prospective validation of a prognostic score for patients in immunotherapy phase I trials: The Gustave Roussy Immune Score (GRIm-Score). Eur J Cancer 2017; 84: 212-18.
6. Feng JF, Wang L, Yang X, Chen S. Gustave Roussy Immune Score (GRIm-Score) is a prognostic marker in patients with resectable esophageal squamous cell carcinoma. J Cancer 2020; 11: 1334-40.
7. Tian S, Cao Y, Duan Y, Liu Q, Peng P. Gustave Roussy Immune Score as a Novel Prognostic Scoring System for Colorectal Cancer Patients: A Propensity Score Matching Analysis. Front Oncol 2021; 11: 737283.
8. Shi Y, Shen G, Zeng Y, Jin X, Zhang S, Hou X et al. Predictive values of the hemoglobin, albumin, lymphocyte and platelet score (HALP) and the modified-Gustave Roussy immune score for esophageal squamous cell carcinoma patients undergoing concurrent chemoradiotherapy. Int Immunopharmacol 2023; 123: 110773.

9. Tolunay PK, İnci BK, Hacan BA, Yaşar S, Karaçin C, Ateş Ö. Gustave Roussy Immune Score in Nivolumab Treated Metastatic Renal Cell Carcinoma. Med Records 2024; 7: 679-82.
10. Gökşen HB, Arslan A. The Predictivity Evaluation of Prognostic Nutritional Index, Neutrophil to Lymphocyte Ratio and Platalet to Lymphocyte Ratio with Gustave-Roussy Immune Score in Patients Diagnosed with Pancreatic Carcinoma: Single Center Trial. Turk J Oncol 2025; 40: 76-82.
11. Basoglu T, Babacan NA, Ozturk FE, Aksoy A, Kilic H, Karacin C et al. Prognostic value of Gustave Roussy immune score in operable pancreatic adenocarcinoma. Indian J Cancer 2023; 60: 179-84.
12. Ma LX, Wang Y, Espin-Garcia O, Berry S, McNamara MG, Shaya S et al. Systemic inflammatory prognostic scores in advanced pancreatic adenocarcinoma. Br J Cancer 2023; 128: 1916-21.
13. Sun KX, Xu RQ, Rong H, Pang HY, Xiang TX. Prognostic significance of the Gustave Roussy immune (GRIm) score in cancer patients: a meta-analysis. Ann Med 2023; 55: 2236640.
14. Wang M, Di X, Zhang S, Li J, Zhao X, Yuan Y et al. Prognostic value of integrated inflammatory-nutritional evaluation in neoadjuvant-treated rectal cancer: a retrospective cohort analysis. BMC Cancer 2025; 25: 1453.
15. Onder AH, İlhan Y, Balçık OY, Karakaya G. Gustave roussy immün skor operabl kolorektal kanserli hastalarda prognozu ve sağkalımı öngörebilir mi? Turk J Clin Lab 2023; 14: 496-507.
16. Cotan H, Iaciu C, Radu E, Niculae T, Rosu OA, Nitipir C. Gustave Roussy immune score (GRIm-score) as a prognostic and predictive score in metastatic colorectal cancer. Cureus 2024; 16: e58362.
17. Jiang H, Li B, Wu M, Wang Q, Li Y. Association of the Advanced Lung Cancer Inflammation Index (ALI) and Gustave Roussy Immune (GRIm) score with immune checkpoint inhibitor efficacy in patients with gastrointestinal and lung cancer. BMC Cancer 2024; 24: 428.
18. Ji Y, Wang W. Prognostic Value of the Gustave Roussy Immune Score in Lung Cancer: A Meta-Analysis. Nutr Cancer 2024; 76: 707-16.
19. Lenci E, Cantini L, Pecci F, Cognigni V, Agostinelli V, Fanelli M et al. The Gustave Roussy Immune (GRIm)-Score Variation Is an Early-on-Treatment Biomarker of Outcome in Advanced Non-Small Cell Lung Cancer (NSCLC) Patients Treated with First-Line Pembrolizumab. J Clin Med 2021; 10: 1276.
20. Ding J, Karp JE, Emadi A. Elevated lactate dehydrogenase (LDH) can be a marker of immune suppression in cancer: Interplay between hematologic and solid neoplastic clones and their microenvironments. Cancer Biomark 2017; 19: 353-63.
21. Liu W, Wang X, Wu W. Role and functional mechanisms of IL 17/IL 17R signaling in pancreatic cancer (Review). Oncol Rep 2024; 52: 124.
22. Yang JJ, Hu ZG, Shi WX, Deng T, He SQ, Yuan SG. Prognostic significance of neutrophil to lymphocyte ratio in pancreatic cancer: a meta-analysis. World J Gastroenterol 2015; 21: 2807-15.
23. Iwai N, Okuda T, Sakagami J, Harada T, Ohara T, Tanabe M et al. Neutrophil to lymphocyte ratio predicts prognosis in unresectable pancreatic cancer. Sci Rep 2020; 10: 18758.
24. Yang MJ, Kim S, Hwang JC, Kim JH, Kim JW, Park JS et al. High Neutrophil-to-Lymphocyte Ratio Predicts a Suppressive Immune Microenvironment and Basal-Like Subtype in Pancreatic Cancer. J Gastroenterol Hepatol 2025; 40: 2623-31.
25. Jiang W, Li X, Xiang C, Zhou W. Neutrophils in pancreatic cancer: Potential therapeutic targets. Front Oncol 2022; 12: 1025805.
26. Sturgeon R, Goel P, Molczyk C, Smith L, Coulter DW, Singh S et al. Neutrophil Dynamics Contribute to Disease Progression and Poor Survival in Pancreatic Cancer. Cancers (Basel) 2025; 17: 5214.
27. Brautigam K, Skok K, Szymonski K, Rift CV, Karamitopoulou E. Tumor immune microenvironment in pancreatic ductal adenocarcinoma revisited - Exploring the "Space". Cancer Lett 2025; 622: 217699.
28. Saito Y, Takekuma Y, Komatsu Y, Sugawara M. Impact of baseline hypoalbuminemia on peripheral edema induced by gemcitabine and nab-paclitaxel for pancreatic cancer treatment. Support Care Cancer 2025; 33: 938.
29. Kim YJ, Seo DW, Pack KM, Pack SK, Lee SS, Pack MH et al. The prognostic factors of pancreatic cancer can be different according to clinical stages. Korean J Gastroenterol 2008; 51: 181-9.
30. Soeters PB, Wolfe RR, Shenkin A. Hypoalbuminemia: Pathogenesis and Clinical Significance. JPEN J Parenter Enteral Nutr 2019; 43: 181-93.