Neutrophil-to-lymphocyte ratio is a predictive marker for invasive malignancy in intraductal papillary mucinous neoplasms of the pancreas
Abstract
OBJECTIVE: To evaluate the correlation between neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte ratio (PLR) values, and the presence of invasive carcinoma in patients with intraductal papillary mucinous neoplasm (IPMN). BACKGROUND: NLR and (PLR) are inflammatory markers that have been associated with overall survival in patients with invasive malignancies, including pancreatic cancer. METHODS: We retrospectively reviewed 272 patients who underwent surgical resection for histologically confirmed IPMN from January 1997 to July 2015. NLR and PLR were calculated and coevaluated with additional demographic, clinical, and imaging data for possible correlation with IPMN-associated carcinoma in the form of a predictive nomogram. RESULTS: NLR and PLR were significantly elevated in patients with IPMN-associated invasive carcinoma (P < 0.001). In the multivariate analysis, NLR value higher than 4 (P < 0.001), IPMN cyst of size more than 3 cm (P < 0.001), presence of enhanced solid component (P = 0.014), main pancreatic duct dilatation of more than 5 mm (P < 0.001), and jaundice (P < 0.001) were statistically significant variables. The developed statistical model has a c-index of 0.895. Implementation of the statistically significant variables in a predictive nomogram provided a reliable point system for estimating the presence of IPMN-associated invasive carcinoma. CONCLUSIONS: NLR is an independent predictive marker for the presence of IPMN-associated invasive carcinoma. Further prospective studies are needed to assess the predictive ability of NLR and how it can be applied in the clinical setting.
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The Clavien-Dindo Classification of Surgical Complications: Five-Year Experience
Clavien, P. A., Barkun, J., de Oliveira, M. L., Vauthey, J. N., Dindo, D., Schulick, R. D., de Santibañes, E., Pekolj, J., Slankamenac, K., Bassi, C., et al. (2009) · Annals of Surgery · doi:10.1097/sla.0b013e3181b13ca2 · Cited by 11,482 · see citing works
Self-citationImmunity, Inflammation, and Cancer
Grivennikov, S. I., Greten, F. R., & Karin, M. (2010) · Cell · doi:10.1016/j.cell.2010.01.025 · Cited by 10,755 · see citing works
Templeton, A. J., McNamara, M. G., Šeruga, B., Vera-Badillo, F., Aneja, P., Ocaña, A., Leibowitz‐Amit, R., Sonpavde, G., Knox, J. J., Tran, B., et al. (2014) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dju124 · Cited by 3,304 · see citing works
International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas
Tanaka, M., Fernández-del Castillo, C., Adsay, V., Chari, S., Falconi, M., Jang, J.-Y., Kimura, W., Levy, P., Pitman, M. B., Schmidt, C. M., et al. (2012) · Pancreatology · doi:10.1016/j.pan.2012.04.004 · Cited by 2,354 · see citing works
Self-citationParadoxical roles of the immune system during cancer development
de Visser, K. E., Eichten, A., & Coussens, L. M. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1782 · Cited by 2,261 · see citing works
Tanaka, M., Chari, S. T., Adsay, V. N., Carlos, F.-D., Falconi, M., Shimizu, M., Yamaguchi, K., Yamao, K., & Matsuno, S. (2005) · Pancreatology · doi:10.1159/000090023 · Cited by 2,042 · see citing works
Ruopp, M. D., Perkins, N. J., Whitcomb, B. W., & Schisterman, E. F. (2008) · Biometrical Journal · doi:10.1002/bimj.200710415 · Cited by 1,320 · see citing works
Liang, W., Zhang, L., Jiang, G., Wang, Q., Liu, L.-X., Liu, D.-R., Wang, Z., Zhu, Z.-H., Deng, Q., Xiong, X., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2014.56.6661 · Cited by 539 · see citing works
Self-citationSpringer, S., Wang, Y., Dal Molin, M., Masica, D. L., Jiao, Y., Kinde, I., Blackford, A., Raman, S. P., Wolfgang, C. L., Tomita, T., et al. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.07.041 · Cited by 477 · see citing works
Self-citationSahora, K., Mino-Kenudson, M., Brugge, W., Thayer, S. P., Ferrone, C. R., Sahani, D., Pitman, M. B., Warshaw, A. L., Lillemoe, K. D., & Fernandez-del Castillo, C. F. (2013) · Annals of Surgery · doi:10.1097/sla.0b013e3182a18f48 · Cited by 285 · see citing works
Immune Suppression by Neutrophils in HIV-1 Infection: Role of PD-L1/PD-1 Pathway
Bowers, N. L., Helton, E. S., Huijbregts, R. P. H., Goepfert, P., Heath, S. L., & Hel, Z. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1003993 · Cited by 256 · see citing works
Prognostic significance of neutrophil to lymphocyte ratio in pancreatic cancer: A meta-analysis
Yang, J. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i9.2807 · Cited by 210 · see citing works
Tan, M. C. B., Baştürk, O., Brannon, R., Bhanot, U. K., Scott, S. N., Bouvier, N., LaFemina, J., Jarnagin, W. R., Berger, M. F., Klimstra, D. S., et al. (2015) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2014.11.029 · Cited by 202 · see citing works
Anand, N., Sampath, K., & Wu, B. U. (2013) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2013.02.010 · Cited by 195 · see citing works
Lorente, D., Mateo, J., Templeton, A. J., Zafeiriou, Z., Bianchini, D., Ferraldeschi, R., Bahl, A. K., Shen, L., Su, Z. Z., Sartor, O. A., et al. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu587 · Cited by 193 · see citing works
Sideras, K., Braat, H., Kwekkeboom, J., van Eijck, C. H. J., Peppelenbosch, M. P., Sleijfer, S., & Bruno, M. J. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.11.005 · Cited by 174 · see citing works
Asano, Y., Kashiwagi, S., Onoda, N., et al. (2015) · Annals of Surgical Oncology · doi:10.1245/s10434-015-4934-0 · Cited by 151 · see citing works
Wang, S. C., Chou, J. F., Strong, V. E. M., Brennan, M. F., Capanu, M., & Coit, D. G. (2015) · Annals of Surgery · doi:10.1097/sla.0000000000001189 · Cited by 150 · see citing works
Luo, G., Guo, M., Liu, Z., et al. (2014) · Annals of Surgical Oncology · doi:10.1245/s10434-014-4021-y · Cited by 150 · see citing works
Complex role for the immune system in initiation and progression of pancreatic cancer
Inman, K. S. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i32.11160 · Cited by 137 · see citing works
Main-duct Intraductal Papillary Mucinous Neoplasm
Hackert, T., Fritz, S., Klauß, M., Bergmann, F., Hinz, U., Strobel, O., Schneider, L., & Büchler, M. W. (2015) · Annals of Surgery · doi:10.1097/sla.0000000000001462 · Cited by 134 · see citing works
Jang, J.-Y., Park, T., Lee, S., Kang, M. J., Lee, S. Y., Lee, K. B., Chang, Y. R., & Kim, S.-W. (2014) · British journal of surgery · doi:10.1002/bjs.9491 · Cited by 132 · see citing works
Seretis, C., Gourgiotis, S., Gemenetzis, G., et al. (2013) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2012.08.006 · Cited by 131 · see citing works
Self-citationPrognostic Role of NLR in Urinary Cancers: A Meta-Analysis
Wei, Y., Jiang, Y.-Z., & Qian, W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092079 · Cited by 129 · see citing works
Prognostic value of systemic inflammation‐based markers in advanced pancreatic cancer
Martin, H. L., Ohara, K., Kiberu, A. D., van Hagen, T., Davidson, A., & Khattak, M. A. (2014) · Internal Medicine Journal · doi:10.1111/imj.12453 · Cited by 108 · see citing works
Goh, B. K. P., Thng, C. H., Tan, D. M. Y., Low, A. S.-C., Wong, J.-S., Cheow, P. C., Chow, P. K. H., Chung, A. Y. F., Wong, W., & Ooi, L. L. (2014) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2013.09.031 · Cited by 101 · see citing works
Neutrophil‐to‐lymphocyte ratio predicts mortality in patients listed for liver transplantation
Leithead, J., Rajoriya, N., Gunson, B. K., & Ferguson, J. (2014) · Liver International · doi:10.1111/liv.12688 · Cited by 95 · see citing works
Correa‐Gallego, C., Do, R., LaFemina, J., Gönen, M., D'Angelica, M. I., DeMatteo, R. P., Fong, Y., Kingham, T. P., Brennan, M. F., Jarnagin, W. R., et al. (2013) · Annals of Surgical Oncology · doi:10.1245/s10434-013-3207-z · Cited by 93 · see citing works
Seo, N., Byun, J. H., Kim, J. H., Kim, H. J., Lee, S. S., Song, K. B., Kim, S. C., Han, D. J., Hong, S., & Lee, M.-G. (2015) · Annals of Surgery · doi:10.1097/sla.0000000000001217 · Cited by 86 · see citing works
Prognostic role of the neutrophil-to-lymphocyte ratio in pancreatic cancer: a meta-analysis
Cheng, H., Long, F., Jaiswar, M., Yang, L., Wang, C., & Zhou, Z. (2015) · Scientific Reports · doi:10.1038/srep11026 · Cited by 85 · see citing works
Zhang, H., Xia, H., Zhang, L., et al. (2015) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2015.03.022 · Cited by 85 · see citing works
Pancreatic adenocarcinoma pathology: changing "landscape".
Brosens, L. A. A., Hackeng, W. M., Offerhaus, G. J. A., Hruban, R. H., & Wood, L. D. (2015) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.2078-6891.2015.032 · Cited by 73 · see citing works
Self-citationGraziosi, L., Marino, E., Angelis, V. D., Rebonato, A., Cavazzoni, E., & Donini, A. (2014) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2014.06.014 · Cited by 73 · see citing works
Kim, J. R., Jang, J., Kang, M. J., Park, T., Lee, S., Jung, W., Chang, J., Shin, Y., Han, Y., & Kim, S. (2015) · Journal of Hepato-Biliary-Pancreatic Sciences · doi:10.1002/jhbp.275 · Cited by 72 · see citing works
Kaimakliotis, P. Z., Riff, B. P., Pourmand, K., Chandrasekhara, V., Furth, E. E., Siegelman, E. S., Drebin, J. A., Vollmer, C. M., Kochman, M. L., Ginsberg, G. G., et al. (2015) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2015.03.017 · Cited by 67 · see citing works
Nguyen, A. H., Toste, P. A., Farrell, J. J., Clerkin, B. M., Williams, J. L., Muthusamy, V. R., Watson, R. R., Tomlinson, J. S., Hines, O. J., Reber, H. A., et al. (2014) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-014-2693-z · Cited by 64 · see citing works
The immunoregulatory mechanisms of carcinoma for its survival and development
Du, C., & Wang, Y. Z. (2011) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-30-12 · Cited by 61 · see citing works
Yamada, S., Fujii, T., Murotani, K., Kanda, M., Sugimoto, H., Nakayama, G., Koike, M., Fujiwara, M., Nakao, A., & Kodera, Y. (2015) · Surgery · doi:10.1016/j.surg.2015.08.042 · Cited by 58 · see citing works
Gian, R. K., Katz, S. S., Gollub, M. J., Li, J., LaFemina, J., Zabor, E. C., Moskowitz, C. S., Klimstra, D. S., & Allen, P. J. (2014) · American Journal of Roentgenology · doi:10.2214/ajr.13.11490 · Cited by 52 · see citing works
Arima, K., Okabe, H., Hashimoto, D., Chikamoto, A., Kuroki, H., Taki, K., Kaida, T., Higashi, T., Nitta, H., Komohara, Y., et al. (2015) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-015-2973-2 · Cited by 51 · see citing works
Inflammation and pancreatic cancer: disease promoter and new therapeutic target
Hamada, S., Masamune, A., & Shimosegawa, T. (2013) · Journal of Gastroenterology · doi:10.1007/s00535-013-0915-x · Cited by 49 · see citing works
Goh, B. K. P., Tan, D. M. Y., Chan, C. Y., Lee, S. Y., Lee, V. T. W., Thng, C. H., Low, A. S.-C., Tai, D. W.-M., Cheow, P. C., Chow, P. K. H., et al. (2015) · Journal of Surgical Oncology · doi:10.1002/jso.23997 · Cited by 44 · see citing works
Tumor-associated Neutrophils and Malignant Progression in Intraductal Papillary Mucinous Neoplasms
Sadot, E., Baştürk, O., Klimstra, D. S., Gönen, M., Lokshin, A. E., Gian, R. K., D'Angelica, M. I., DeMatteo, R. P., Kingham, T. P., Jarnagin, W. R., et al. (2015) · Annals of Surgery · doi:10.1097/sla.0000000000001044 · Cited by 44 · see citing works
Kawai, K., Ishihara, S., Yamaguchi, H., et al. (2015) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2015.01.026 · Cited by 39 · see citing works
Kang, M. J., Jang, J., Lee, S., Park, T., Lee, S., & Kim, S. (2015) · World Journal of Surgery · doi:10.1007/s00268-015-3062-0 · Cited by 27 · see citing works
Lawson, R. D., Hunt, G. C., Giap, A. Q., Krinsky, M. L., Slezak, J. M., Tang, R. S. Y., Gonzalez, I., Kwong, W. T.-Y., Fehmi, S. M. A., & Savides, T. J. (2015) · PubMed Central · Cited by 24 · see citing works
Rosenblatt, R. E., Gausman, V., Epelboym, I., Poneros, J. M., Sethi, A., Lightdale, C. J., Woo, Y., Gress, F. G., Allendorf, J., Schrope, B., et al. (2014) · Pancreas · doi:10.1097/mpa.0000000000000264 · Cited by 24 · see citing works
Roch, A. M., Barron, M. R., Tann, M. A., Sandrasegar, K., Hannaford, K. N., Ceppa, E. P., House, M. G., Zyromski, N. J., Nakeeb, A., & Schmidt, M. (2015) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2015.04.020 · Cited by 18 · see citing works
Lang, B. H., & Wong, C. K. H. (2015) · World Journal of Surgery · doi:10.1007/s00268-015-3044-2 · Cited by 17 · see citing works
The Changing Spectrum of Surgically Treated Cystic Neoplasms of the Pancreas
Plichta, J. K., Brosius, J. A., Pappas, S. G., Abood, G. J., & Aranha, G. V. (2015) · HPB Surgery · doi:10.1155/2015/791704 · Cited by 15 · see citing works
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- Authors
- Gemenetzis, G., Bagante, F., Griffin, J. F., Rezaee, N., Javed, A. A., Manos, L. L., Lennon, A. M., Wood, L. D., Hruban, R. H., Zheng, L., Zaheer, A., Fishman, E. K., Ahuja, N., Cameron, J. L., Weiss, M. J., He, J., & Wolfgang, C. L.
- Affiliations
- Johns Hopkins University (US)
- Johns Hopkins Medicine (US)
- Corresponding author
- Gemenetzis, Georgios
- Bagante, Fabio
- Griffin, James F.
- Rezaee, Neda
- Javed, Ammar A.
- Manos, Lindsey L.
- Ahuja, Nita
- Cameron, John L.
- Weiss, Matthew J.
- He, Jin
- Wolfgang, Christopher L.
- ORCID
- Venue
- Annals of Surgery
- Published
- 2017-08
- Volume
- 266
- Issue
- 2
- Pages
- 339-345
- ISSN
- 0003-4932 (ISSN-L)
- OpenAlex
- W2491724132
- Cited by
- 127
- References
- 50
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 4 · 2023: 8 · 2022: 17 · 2021: 24 · 2020: 21 · 2019: 15 · 2018: 14 · 2017: 9
- FWCI
- 6.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of Surgery (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Oncology › Inflammatory Biomarkers in Disease Prognosis
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, intraductal papillary mucinous neoplasm, pancreatic cancer, inflammatory markers, predictive nomogram, pancreatic cysts, main pancreatic duct dilatation, jaundice
- MeSH terms
- Aged, Carcinoma, Papillary, Female, Humans, Lymphocytes, Male, Middle Aged, Neoplasm Invasiveness, Neutrophils, Pancreatic Neoplasms, Platelet Count, Retrospective Studies, Biomarkers, Tumor, Multivariate Analysis, Lymphocyte Count, Carcinoma, Pancreatic Ductal, Nomograms
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