Mature MUC5AC Expression in Resected Pancreatic Ductal Adenocarcinoma Predicts Treatment Response and Outcomes
Abstract
:1. Introduction
2. Results
2.1. Baseline Characteristics
2.2. MUC5AC Detection and Distribution for Patients with Resected PDA
2.3. MUC5AC Expression Levels and Pathological Treatment Responses in PDA Post-NAT
2.4. Impact of MUC5AC on Pathological Features of Resected PDA
2.5. The Impact of MUC5AC on Progression-Free Survival and Overall Survival in R-PDA
2.6. MUC5AC Expression in Primary and Distant Metastatic Sites
3. Discussion
4. Materials and Methods
4.1. Study Design and Population
4.2. Immunohistochemistry
4.3. Clinical and Pathology Data Collection
4.4. Statistical Considerations
5. Conclusions
6. Patents
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Siegel, R.L.; Giaquinto, A.N.; Jemal, A. Cancer statistics, 2024. CA Cancer J. Clin. 2024, 74, 12–49. [Google Scholar] [CrossRef]
- Sheel, A.; Addison, S.; Nuguru, S.P.; Manne, A. Is Cell-Free DNA Testing in Pancreatic Ductal Adenocarcinoma Ready for Prime Time? Cancers 2022, 14, 3453. [Google Scholar] [CrossRef]
- Neoptolemos, J.P.; Palmer, D.H.; Ghaneh, P.; Psarelli, E.E.; Valle, J.W.; Halloran, C.M.; Faluyi, O.; O’Reilly, D.A.; Cunningham, D.; Wadsley, J.; et al. Comparison of adjuvant gemcitabine and capecitabine with gemcitabine monotherapy in patients with resected pancreatic cancer (ESPAC-4): A multicentre, open-label, randomised, phase 3 trial. Lancet 2017, 389, 1011–1024. [Google Scholar] [CrossRef]
- Conroy, T.; Hammel, P.; Hebbar, M.; Ben Abdelghani, M.; Wei, A.C.; Raoul, J.-L.; Choné, L.; Francois, E.; Artru, P.; Biagi, J.J.; et al. FOLFIRINOX or Gemcitabine as Adjuvant Therapy for Pancreatic Cancer. N. Engl. J. Med. 2018, 379, 2395–2406. [Google Scholar] [CrossRef]
- Valle, J.W.; Palmer, D.; Jackson, R.; Cox, T.; Neoptolemos, J.P.; Ghaneh, P.; Rawcliffe, C.L.; Bassi, C.; Stocken, D.D.; Cunningham, D.; et al. Optimal Duration and Timing of Adjuvant Chemotherapy after Definitive Surgery for Ductal Adenocarcinoma of the Pancreas: Ongoing Lessons from the ESPAC-3 Study. J. Clin. Oncol. 2014, 32, 504–512. [Google Scholar] [CrossRef] [PubMed]
- Unno, M.; Motoi, F.; Matsuyama, Y.; Satoi, S.; Matsumoto, I.; Aosasa, S.; Shirakawa, H.; Wada, K.; Fujii, T.; Yoshitomi, H.; et al. Randomized phase II/III trial of neoadjuvant chemotherapy with gemcitabine and S-1 versus upfront surgery for resectable pancreatic cancer (Prep-02/JSAP-05). J. Clin. Oncol. 2019, 37, 189. [Google Scholar] [CrossRef]
- Liu, S.; Li, H.; Xue, Y.; Yang, L. Prognostic value of neoadjuvant therapy for resectable and borderline resectable pancreatic cancer: A meta-analysis of randomized controlled trials. PLoS ONE 2023, 18, e0290888. [Google Scholar] [CrossRef]
- Kolbeinsson, H.M.; Chandana, S.; Wright, G.P.; Chung, M. Pancreatic Cancer: A Review of Current Treatment and Novel Therapies. J. Investig. Surg. 2023, 36, 2129884. [Google Scholar] [CrossRef] [PubMed]
- van Dam, J.L.; Janssen, Q.P.; Besselink, M.G.; Homs, M.Y.V.; van Santvoort, H.C.; van Tienhoven, G.; de Wilde, R.F.; Wilmink, J.W.; van Eijck, C.H.; Koerkamp, B.G.; et al. Neoadjuvant therapy or upfront surgery for resectable and borderline resectable pancreatic cancer: A meta-analysis of randomised controlled trials. Eur. J. Cancer 2022, 160, 140–149. [Google Scholar] [CrossRef]
- Versteijne, E.; van Dam, J.L.; Suker, M.; Janssen, Q.P.; Groothuis, K.; Akkermans-Vogelaar, J.M.; Besselink, M.G.; Bonsing, B.A.; Buijsen, J.; Busch, O.R.; et al. Neoadjuvant Chemoradiotherapy versus Upfront Surgery for Resectable and Borderline Resectable Pancreatic Cancer: Long-Term Results of the Dutch Randomized PREOPANC Trial. J. Clin. Oncol. 2022, 40, 1220–1230. [Google Scholar] [CrossRef]
- Springfeld, C.; Ferrone, C.R.; Katz, M.H.G.; Philip, P.A.; Hong, T.S.; Hackert, T.; Büchler, M.W.; Neoptolemos, J. Neoadjuvant therapy for pancreatic cancer. Nat. Rev. Clin. Oncol. 2023, 20, 318–337. [Google Scholar] [CrossRef]
- Jiang, Y.; Sohal, D.P.S. Pancreatic Adenocarcinoma Management. JCO Oncol. Pract. 2023, 19, 19–32. [Google Scholar] [CrossRef]
- Labori, K.J.; Bratlie, S.O.; Andersson, B.; Angelsen, J.-H.; Biörserud, C.; Björnsson, B.; Bringeland, E.A.; Elander, N.; Garresori, H.; Grønbech, J.E.; et al. Neoadjuvant FOLFIRINOX versus upfront surgery for resectable pancreatic head cancer (NORPACT-1): A multicentre, randomised, phase 2 trial. Lancet Gastroenterol. Hepatol. 2024, 9, 205–217. [Google Scholar] [CrossRef] [PubMed]
- Chatzizacharias, N.A.; Tsai, S.; Griffin, M.; Tolat, P.; Ritch, P.; George, B.; Barnes, C.; Aldakkak, M.; Khan, A.H.; Hall, W.; et al. Locally advanced pancreas cancer: Staging and goals of therapy. Surgery 2018, 163, 1053–1062. [Google Scholar] [CrossRef]
- Khorana, A.A.; Mangu, P.B.; Berlin, J.; Engebretson, A.; Hong, T.S.; Maitra, A.; Mohile, S.G.; Mumber, M.; Schulick, R.; Shapiro, M.; et al. Potentially Curable Pancreatic Cancer: American Society of Clinical Oncology Clinical Practice Guideline. J. Clin. Oncol. 2016, 34, 2541–2556. [Google Scholar] [CrossRef]
- Elbanna, K.Y.; Jang, H.-J.; Kim, T.K. Imaging diagnosis and staging of pancreatic ductal adenocarcinoma: A comprehensive review. Insights Imaging 2020, 11, 58. [Google Scholar] [CrossRef]
- Poruk, K.E.; Gay, D.Z.; Brown, K.; Mulvihill, J.D.; Boucher, K.M.; Scaife, C.L.; Firpo, M.A.; Mulvihill, S.J. The clinical utility of CA 19-9 in pancreatic adenocarcinoma: Diagnostic and prognostic updates. Curr. Mol. Med. 2013, 13, 340–351. [Google Scholar] [CrossRef] [PubMed]
- Manne, A.; Esnakula, A.; Abushahin, L.; Tsung, A. Understanding the Clinical Impact of MUC5AC Expression on Pancreatic Ductal Adenocarcinoma. Cancers 2021, 13, 3059. [Google Scholar] [CrossRef] [PubMed]
- Manne, A.; Kasi, A.; Esnakula, A.K.; Paluri, R.K. Predictive Value of MUC5AC Signature in Pancreatic Ductal Adenocarcinoma: A Hypothesis Based on Preclinical Evidence. Int. J. Mol. Sci. 2023, 24, 8087. [Google Scholar] [CrossRef]
- Manne, A.; Mneimneh, W.; Elkadi, O.; Escobar, D.E.; Coley, J.; Guzman, G.B.; Fnu, S.M.D.; Alkharabsheh, O.; Khushman, M.D.M. The pattern of mucin 5AC (MUC5AC) expression using immunohistochemistry and its prognostic significance in patients with pancreatic ductal adenocarcinoma. J. Clin. Oncol. 2020, 38, e16756. [Google Scholar] [CrossRef]
- Manne, A.; Yu, L.; Hart, P.A.; Tsung, A.; Esnakula, A. Differential Expression and Diagnostic Value of MUC5AC Glycoforms in Pancreatic Ductal Adenocarcinoma. Cancers 2023, 15, 4832. [Google Scholar] [CrossRef]
- Benson, K.K.; Sheel, A.; Rahman, S.; Esnakula, A.; Manne, A. Understanding the Clinical Significance of MUC5AC in Biliary Tract Cancers. Cancers 2023, 15, 433. [Google Scholar] [CrossRef]
- Bansil, R.; Turner, B.S. Mucin structure, aggregation, physiological functions and biomedical applications. Curr. Opin. Colloid Interface Sci. 2006, 11, 164–170. [Google Scholar] [CrossRef]
- Kebouchi, M.; Hafeez, Z.; Le Roux, Y.; Dary-Mourot, A.; Genay, M. Importance of digestive mucus and mucins for designing new functional food ingredients. Food Res. Int. 2020, 131, 108906. [Google Scholar] [CrossRef]
- Yamazoe, S.; Tanaka, H.; Iwauchi, T.; Yoshii, M.; Ito, G.; Amano, R.; Yamada, N.; Sawada, T.; Ohira, M.; Hirakawa, K. Identification of HLA-A*0201- and A*2402-restricted epitopes of mucin 5AC expressed in advanced pancreatic cancer. Pancreas 2011, 40, 896–904. [Google Scholar] [CrossRef]
- Matsuyama, M.; Kondo, F.; Ishihara, T.; Yamaguchi, T.; Ito, R.; Tsuyuguchi, T.; Tawada, K.; Yokosuka, O. Evaluation of pancreatic intraepithelial neoplasia and mucin expression in normal pancreata. J. Hepato-Biliary-Pancreat. Sci. 2012, 19, 242–248. [Google Scholar] [CrossRef]
- Nagata, K.; Horinouchi, M.; Saitou, M.; Higashi, M.; Nomoto, M.; Goto, M.; Yonezawa, S. Mucin expression profile in pancreatic cancer and the precursor lesions. J. Hepato-Biliary-Pancreat. Surg. 2007, 14, 243–254. [Google Scholar] [CrossRef]
- Krishn, S.R.; Ganguly, K.; Kaur, S.; Batra, S.K. Ramifications of secreted mucin MUC5AC in malignant journey: A holistic view. Carcinogenesis 2018, 39, 633–651. [Google Scholar] [CrossRef]
- Kim, G.E.; Bae, H.I.; Park, H.U.; Kuan, S.F.; Crawley, S.C.; Ho, J.J.; Kim, Y.S. Aberrant expression of MUC5AC and MUC6 gastric mucins and sialyl Tn antigen in intraepithelial neoplasms of the pancreas. Gastroenterology 2002, 123, 1052–1060. [Google Scholar] [CrossRef] [PubMed]
- Yamasaki, H.; Ikeda, S.; Okajima, M.; Miura, Y.; Asahara, T.; Kohno, N.; Shimamoto, F. Expression and localization of MUC1, MUC2, MUC5AC and small intestinal mucin antigen in pancreatic tumors. Int. J. Oncol. 2004, 24, 107–113. [Google Scholar] [CrossRef]
- Nollet, S.; Forgue-Lafitte, M.E.; Kirkham, P.; Bara, J. Mapping of two new epitopes on the apomucin encoded by MUC5AC gene: Expression in normal GI tract and colon tumors. Int. J. Cancer 2002, 99, 336–343. [Google Scholar] [CrossRef] [PubMed]
- Nollet, S.; Escande, F.; Buisine, M.P.; Forgue-Lafitte, M.E.; Kirkham, P.; Okada, Y.; Bara, J. Mapping of SOMU1 and M1 epitopes on the apomucin encoded by the 5′ end of the MUC5AC gene. Hybrid. Hybridomics 2004, 23, 93–99. [Google Scholar] [CrossRef] [PubMed]
- Bara, J.; Chastre, E.; Mahiou, J.; Singh, R.L.; Forgue-Lafitte, M.E.; Hollande, E.; Godeau, F. Gastric M1 mucin, an early oncofetal marker of colon carcinogenesis, is encoded by the MUC5AC gene. Int. J. Cancer 1998, 75, 767–773. [Google Scholar] [CrossRef]
- Takano, Y.; Ohike, N.; Tajiri, T.; Asonuma, K.; Harada, K.; Takahashi, H.; Morohoshi, T. Gastric- and intestinal-type marker expression in invasive ductal adenocarcinoma of the pancreas. Hepatobiliary Pancreat. Dis. Int. 2012, 11, 424–428. [Google Scholar] [CrossRef]
- Jinfeng, M.; Kimura, W.; Hirai, I.; Sakurai, F.; Moriya, T.; Mizutani, M. Expression of MUC5AC and MUC6 in invasive ductal carcinoma of the pancreas and relationship with prognosis. Int. J. Gastrointest. Cancer 2003, 34, 9–18. [Google Scholar] [CrossRef]
- Aloysius, M.M.; Zaitoun, A.M.; Awad, S.; Ilyas, M.; Rowlands, B.J.; Lobo, D.N. Mucins and CD56 as markers of tumour invasion and prognosis in periampullary cancer. J. Br. Surg. 2010, 97, 1269–1278. [Google Scholar] [CrossRef]
- Takikita, M.; Altekruse, S.; Lynch, C.F.; Goodman, M.T.; Hernandez, B.Y.; Green, M.; Cozen, W.; Cockburn, M.; Saber, M.S.; Topor, M.; et al. Associations between selected biomarkers and prognosis in a population-based pancreatic cancer tissue microarray. Cancer Res. 2009, 69, 2950–2955. [Google Scholar] [CrossRef] [PubMed]
- Higashi, M.; Yokoyama, S.; Yamamoto, T.; Goto, Y.; Kitazono, I.; Hiraki, T.; Taguchi, H.; Hashimoto, S.; Fukukura, Y.; Koriyama, C.; et al. Mucin expression in endoscopic ultrasound-guided fine-needle aspiration specimens is a useful prognostic factor in pancreatic ductal adenocarcinoma. Pancreas 2015, 44, 728–734. [Google Scholar] [CrossRef]
- Krishn, S.R. Secretory Mucin MUC5AC in Gastrointestinal Malignancies. Ph.D. Thesis, University of Nebraska Medical Center, Omaha, NE, USA, 2016; p. 110. [Google Scholar]
- Ganguly, K.; Cox, J.L.; Ghersi, D.; Grandgenett, P.M.; Hollingsworth, M.A.; Jain, M.; Kumar, S.; Batra, S.K. Mucin 5AC—Mediated CD44/ITGB1 Clustering Mobilizes Adipose-Derived Mesenchymal Stem Cells to Modulate Pancreatic Cancer Stromal Heterogeneity. Gastroenterology 2022, 162, 2032–2046. [Google Scholar] [CrossRef]
- Ganguly, K.; Bhatia, R.; Rauth, S.; Kisling, A.; Atri, P.; Thompson, C.; Vengoji, R.; Krishn, S.R.; Shinde, D.; Thomas, V.; et al. Mucin 5AC Serves as the Nexus for β-Catenin/c-Myc Interplay to Promote Glutamine Dependency during Pancreatic Cancer Chemoresistance. Gastroenterology 2022, 162, 253–268. [Google Scholar] [CrossRef]
- Ganguly, K.; Krishn, S.R.; Jahan, R.; Atri, P.; Rachagani, S.; Rauth, S.; Xi, H.; Lu, Y.; Batra, S.; Kaur, S. Abstract 65: Gel-forming mucin MUC5AC as the nexus for cell-adhesion molecules governing pancreatic cancer aggressiveness and chemoresistance. Cancer Res. 2019, 79, 65. [Google Scholar] [CrossRef]
- Ghaneh, P.; Palmer, D.; Cicconi, S.; Jackson, R.; Halloran, C.M.; Rawcliffe, C.; Sripadam, R.; Mukherjee, S.; Soonawalla, Z.; Wadsley, J.; et al. Immediate surgery compared with short-course neoadjuvant gemcitabine plus capecitabine, FOLFIRINOX, or chemoradiotherapy in patients with borderline resectable pancreatic cancer (ESPAC5): A four-arm, multicentre, randomised, phase 2 trial. Lancet Gastroenterol. Hepatol. 2022, 8, 157–168. [Google Scholar] [CrossRef] [PubMed]
- Sohal, D.; Duong, M.T.; Ahmad, S.A.; Gandhi, N.; Beg, M.S.; Wang-Gillam, A.; Wade, J.L.; Chiorean, E.G.; Guthrie, K.A.; Lowy, A.M.; et al. SWOG S1505: Results of perioperative chemotherapy (peri-op CTx) with mfolfirinox versus gemcitabine/nab-paclitaxel (Gem/nabP) for resectable pancreatic ductal adenocarcinoma (PDA). J. Clin. Oncol. 2020, 38, 4504. [Google Scholar] [CrossRef]
- Meyerholz, D.K.; Beck, A.P. Principles and approaches for reproducible scoring of tissue stains in research. Lab. Investig. 2018, 98, 844–855. [Google Scholar] [CrossRef]
- Ryan, R.; Gibbons, D.; Hyland, J.M.; Treanor, D.; White, A.; Mulcahy, H.E.; O’Donoghue, D.P.; Moriarty, M.; Fennelly, D.; Sheahan, K. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology 2005, 47, 141–146. [Google Scholar] [CrossRef] [PubMed]
- Huffman, B.M.; Mallick, A.B.; Horick, N.K.; Wang-Gillam, A.; Hosein, P.J.; Morse, M.A.; Beg, M.S.; Murphy, J.E.; Mavroukakis, S.; Zaki, A.; et al. Effect of a MUC5AC Antibody (NPC-1C) Administered with Second-Line Gemcitabine and Nab-Paclitaxel on the Survival of Patients with Advanced Pancreatic Ductal Adenocarcinoma. JAMA Netw. Open 2023, 6, e2249720. [Google Scholar] [CrossRef]
Pathological Feature | Distribution in Percentages (%) |
---|---|
Differentiation (G1 vs. G2 vs. G3) | 11 vs. 62 vs. 27 |
Peripancreatic extension | 50 |
Treatment effect noted in NAT group (n = 43). Objective response (OR) vs. no response (NR). | 27 (OR) vs. 16 (NR) (OR: nCR—4; PR—23) |
T-stage, T1 vs. T2 vs. T3 vs. T4 | 23 vs. 54 vs. 21 vs. 2 |
Tumor size, ≤2 cms vs. 2–4 cms vs. >4 cms | 23 vs. 55 vs. 22 |
Lymph vascular invasion identified | 64 |
Perineural invasion identified | 80 |
Margins positive | 29 |
Residual disease: R0 vs. R1 vs. R2 | 72 vs. 26 vs. 2 |
Node positivity: N0 vs. N1–2 | 29 vs. 71 |
Association with premalignant lesion: PanIN vs. IPMN vs. no lesion identified | 54 vs. 9 vs. 37 |
Mean H-Scores OR vs. NR vs. UpS | Head-to-Head Comparisons | |
---|---|---|
45M1 * | 113.3 vs. 154.38 vs. 163.6 (p = 0.0612) | OR vs. UpS (p = 0.0498) |
NR vs. UpS (p = 0.9308) | ||
OR vs. NR (p = 0.3245) | ||
CLH2 * | 104.07 vs. 151.88 vs. 162.93 (p = 0.0184) | OR vs. UpS (p = 0.0140) |
NR vs. UpS (p = 0.8969) | ||
OR vs. NR (p = 0.2015) | ||
EC-45M1 # | 56% vs. 63% vs. 82% (p = 0.002) | OR vs. UpS (p = 0.0155) |
NR vs. UpS (p = 0.1008) | ||
OR vs. NR (p = 0.7548) |
MUC5AC Glycoform | Expression in H-Score | Impact on Response | Impact on EC-45M1 | |||
---|---|---|---|---|---|---|
OR (%) | NR (%) | p-Value | Detection (%) * | p-Value | ||
CLH2 | ≤100 | 77 | 23 | 0.04 | 37 | <0.01 |
>100 | 48 | 52 | 90 | |||
45M1 | ≤100 | 76 | 24 | 0.07 | 24 | <0.01 |
>100 | 50 | 50 | 91 |
Pathological Feature | 45M1 | CLH2 | EC-45M1 |
---|---|---|---|
Pathological differentiation, G1–2 vs. G3 | 0.6866 | 0.8559 | 0.4358 |
Peripancreatic extension | 0.6200 | 0.8741 | 0.1841 |
Treatment effect, OR vs. NR vs. UpS | 0.0317 | 0.0112 | 0.0081 |
Lymphovascular invasion | 0.8954 | 0.9811 | 0.3744 |
Perineural invasion | 0.4129 | 0.4802 | 0.8238 |
Margins | 0.5935 | 0.8658 | 0.5832 |
R0 vs. R1-R2 | 0.2971 | 0.6141 | 0.3642 |
Tumor size (≤2 cms vs. >2 cm) | 0.0523 | 0.0478 | 0.1796 |
N0 vs. N1–N1 | 0.9004 | 0.8697 | 0.5832 |
Premalignant lesion, yes vs. no | 0.0585 | 0.0643 | 0.0007 |
Neoadjuvant CRT | 0.3952 | 0.2876 | 0.3592 |
Neoadjuvant therapy | 0.0612 | 0.0264 | 0.0088 |
Site of recurrence (none vs. local vs. distant) | 0.1381 | 0.1405 | 0.6321 |
Parameter | Pr > ChiSq | Hazard Ratio | 95% Wald Confidence Limits | |
---|---|---|---|---|
45M1—H-score | 0.0398 | 0.968 | 0.938–0.998 | |
CLH2—H-score | 0.0741 | 1.029 | 0.007–1.063 | |
EC detection | Negative | 0.0178 | 0.213 | 0.05–0.766 |
Pathological differentiation, G1–2 vs. G3 | G1-2 | 0.0385 | 0.350 | 0.130–0.946 |
Peripancreatic extension | NO | 0.5607 | 0.734 | |
Treatment effect, OR vs. NR | OR 1 | 0.7106 | 0.789 | 0.226–2.755 |
Lymphovascular invasion | NO | 0.0551 | 0.313 | 0.095–1.026 |
Perineural invasion | NO | 0.6831 | 0.718 | |
Margins | Negative | 0.0014 | 0.127 | 0.03–0.452 |
R0 vs. R1–R2 | R0 | 0.7909 | 0.816 | |
Tumor size (≤2 cms vs. >2 cm) | ≤2 cms | 0.6069 | 1.562 | |
N0 vs. N1-N1 | N0 | 0.7950 | 0.853 | |
Premalignant | None | 0.9336 | 0.952 | |
NAT CRT | Had NAT CRT | 0.0459 | 0.369 | 0.138–0.982 |
Site of recurrence | Distant metastasis 1 | 0.0379 | 4.838 | 1.092–21.433 |
Site of recurrence | Local recurrence 1 | 0.0176 | 8.798 | 1.462–52.965 |
Parameter | Pr > ChiSq | Hazard Ratio | 95% Wald Confidence Limits | |
---|---|---|---|---|
45M1—H-score | 0.0170 | 0.959 | 0.926–0.993 | |
CLH2—H-score | 0.0205 | 1.043 | 1.006–1.080 | |
EC detection | Negative | 0.1406 | 0.343 | |
Pathological differentiation, G1–2 vs. G3 | G1-2 | 0.0038 | 0.193 | 0.06–0.588 |
Peripancreatic extension | NO | 0.5877 | 1.294 | |
Treatment effect, OR vs. NR | OR | 0.7734 | 1.219 | |
Lymphovascular invasion | NO | 0.1567 | 0.405 | |
Perineural invasion | NO | 0.5547 | 0.609 | |
Margins | Negative | <0001 | 0.040 | 0.009–0.180 |
R0 vs. R1-R2 | R0 | 0.0878 | 3.986 | 0.815–19.493 |
Tumor size (≤2 cms vs. >2 cm) | ≤2 cms | 0.1407 | 3.845 | |
N0 vs. N1-N1 | N0 | 0.2046 | 0.429 | |
Premalignant | None | 0.3680 | 1.670 | |
NAT CRT | Had NAT CRT | 0.1987 | 0.542 | |
Site of recurrence | Distant metastasis 1 | 0.8868 | 0.894 | |
Site of recurrence | Local recurrence 1 | 0.5050 | 1.961 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Manne, A.; Esnakula, A.; Sheel, A.; Sara, A.; Manne, U.; Paluri, R.K.; He, K.; Yang, W.; Sohal, D.; Kasi, A.; et al. Mature MUC5AC Expression in Resected Pancreatic Ductal Adenocarcinoma Predicts Treatment Response and Outcomes. Int. J. Mol. Sci. 2024, 25, 9041. https://doi.org/10.3390/ijms25169041
Manne A, Esnakula A, Sheel A, Sara A, Manne U, Paluri RK, He K, Yang W, Sohal D, Kasi A, et al. Mature MUC5AC Expression in Resected Pancreatic Ductal Adenocarcinoma Predicts Treatment Response and Outcomes. International Journal of Molecular Sciences. 2024; 25(16):9041. https://doi.org/10.3390/ijms25169041
Chicago/Turabian StyleManne, Ashish, Ashwini Esnakula, Ankur Sheel, Amir Sara, Upender Manne, Ravi Kumar Paluri, Kai He, Wancai Yang, Davendra Sohal, Anup Kasi, and et al. 2024. "Mature MUC5AC Expression in Resected Pancreatic Ductal Adenocarcinoma Predicts Treatment Response and Outcomes" International Journal of Molecular Sciences 25, no. 16: 9041. https://doi.org/10.3390/ijms25169041