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Published in: Cancer and Metastasis Reviews 2/2022

02-04-2022 | Pancreatic Cancer

Connecting the Human Microbiome and Pancreatic Cancer

Authors: Rachel E. Sexton, Md Hafiz Uddin, Sahar Bannoura, Husain Yar Khan, Yousef Mzannar, Yiwei Li, Amro Aboukameel, Mohammad Najeeb Al-Hallak, Bayan Al-Share, Amr Mohamed, Misako Nagasaka, Bassel El-Rayes, Asfar S. Azmi

Published in: Cancer and Metastasis Reviews | Issue 2/2022

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Abstract

Pancreatic cancer is a deadly disease that is increasing in incidence throughout the world. There are no clear causal factors associated with the incidence of pancreatic cancer; however, some correlation to smoking, diabetes and alcohol has been described. Recently, a few studies have linked the human microbiome (oral and gastrointestinal tract) to pancreatic cancer development. A perturbed microbiome has been shown to alter normal cells while promoting cancer-related processes such as increased cell signaling, immune system evasion and invasion. In this article, we will review in detail the alterations within the gut and oral microbiome that have been linked to pancreatic cancer and explore the ability of other microbiomes, such as the lung and skin microbiome, to contribute to disease development. Understanding ways to identify a perturbed microbiome can result in advancements in pancreatic cancer research and allow for prevention, earlier detection and alternative treatment strategies for patients.
Literature
1.
go back to reference Seer.cancer.gov. Cancer Stat Facts: Pancreatic Cancer. Surveillance, Epidemiology and End Results Program. Accessed 11/12/2021. Seer.cancer.gov. Cancer Stat Facts: Pancreatic Cancer. Surveillance, Epidemiology and End Results Program. Accessed 11/12/2021.
22.
go back to reference Grice, E. A., Kong, H. H., Conlan, S., Deming, C. B., Davis, J., Young, A. C., NISC Comparative Sequencing Program, Bouffard, G. G., Blakesley, R. W., Murray, P. R., Green, E. D., Turner, M. L., & Segre, J. A. (2009). Topographical and temporal diversity of the human skin microbiome. Science (New York, N.Y.), 324(5931), 1190–1192. https://doi.org/10.1126/science.1171700 Grice, E. A., Kong, H. H., Conlan, S., Deming, C. B., Davis, J., Young, A. C., NISC Comparative Sequencing Program, Bouffard, G. G., Blakesley, R. W., Murray, P. R., Green, E. D., Turner, M. L., & Segre, J. A. (2009). Topographical and temporal diversity of the human skin microbiome. Science (New York, N.Y.)324(5931), 1190–1192. https://​doi.​org/​10.​1126/​science.​1171700
25.
go back to reference Grice, E. A., Kong, H. H., Conlan, S., Deming, C. B., Davis, J., Young, A. C., et al. (2009). Topographical and temporal diversity of the human skin microbiome. Science, 324, 1190–1192.CrossRef Grice, E. A., Kong, H. H., Conlan, S., Deming, C. B., Davis, J., Young, A. C., et al. (2009). Topographical and temporal diversity of the human skin microbiome. Science, 324, 1190–1192.CrossRef
27.
go back to reference Busse, K., & Liao, W. (2010). Which Psoriasis Patients Develop Psoriatic Arthritis? Psoriasis forum, 16(4), 17–25.CrossRef Busse, K., & Liao, W. (2010). Which Psoriasis Patients Develop Psoriatic Arthritis? Psoriasis forum, 16(4), 17–25.CrossRef
30.
go back to reference Tong, T. R., Chan, A., Lai, T. W., Chan, O. W., Lee, K. C., Lo, S. T., Lung, R., Li, J. Y., & Chow, T. C. (2007). Identification of HPV-16 in Borderline Mucinous Cystic Neoplasm of Pancreas. International journal of biomedical science : IJBS, 3(1), 72–75.PubMedPubMedCentral Tong, T. R., Chan, A., Lai, T. W., Chan, O. W., Lee, K. C., Lo, S. T., Lung, R., Li, J. Y., & Chow, T. C. (2007). Identification of HPV-16 in Borderline Mucinous Cystic Neoplasm of Pancreas. International journal of biomedical science : IJBS, 3(1), 72–75.PubMedPubMedCentral
36.
go back to reference Ohlund, D., Handly-Santana, A., Biffi, G., Elyada, E., Almeida, A. S., Ponz-Sarvise, M., Corbo, V., Oni, T. E., Hearn, S. A., Lee, E. J., et al. (2017). Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. Journal of Experimental Medicine., 214(3), 579–596.CrossRef Ohlund, D., Handly-Santana, A., Biffi, G., Elyada, E., Almeida, A. S., Ponz-Sarvise, M., Corbo, V., Oni, T. E., Hearn, S. A., Lee, E. J., et al. (2017). Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. Journal of Experimental Medicine., 214(3), 579–596.CrossRef
37.
go back to reference Domen, A., Quatannens, D., Zanivan, S., Deben, C., Van Audenaerde, J., Smits, E., Wouters, A., Lardon, F., Roeyen, G., Verhoeven, Y., Janssens, A., Vandamme, T., van Dam, P., Peeters, M., & Prenen, H. (2021). Cancer-Associated Fibroblasts as a Common Orchestrator of Therapy Resistance in Lung and Pancreatic Cancer. Cancers, 13(5), 987. https://doi.org/10.3390/cancers13050987CrossRefPubMedPubMedCentral Domen, A., Quatannens, D., Zanivan, S., Deben, C., Van Audenaerde, J., Smits, E., Wouters, A., Lardon, F., Roeyen, G., Verhoeven, Y., Janssens, A., Vandamme, T., van Dam, P., Peeters, M., & Prenen, H. (2021). Cancer-Associated Fibroblasts as a Common Orchestrator of Therapy Resistance in Lung and Pancreatic Cancer. Cancers, 13(5), 987. https://​doi.​org/​10.​3390/​cancers13050987CrossRefPubMedPubMedCentral
40.
go back to reference Steele, N. G., Biffi, G., Kemp, S. B., Zhang, Y., Drouillard, D., Syu, L., Hao, Y., Oni, T. E., Brosnan, E., Elyada, E., Doshi, A., Hansma, C., Espinoza, C., Abbas, A., The, S., Irizarry-Negron, V., Halbrook, C. J., Franks, N. E., Hoffman, M. T., … Pasca di Magliano, M. (2021). Inhibition of Hedgehog Signaling Alters Fibroblast Composition in Pancreatic Cancer. Clinical Cancer Research, 27(7), 2023–2037. https://doi.org/10.1158/1078-0432.CCR-20-3715CrossRefPubMedPubMedCentral Steele, N. G., Biffi, G., Kemp, S. B., Zhang, Y., Drouillard, D., Syu, L., Hao, Y., Oni, T. E., Brosnan, E., Elyada, E., Doshi, A., Hansma, C., Espinoza, C., Abbas, A., The, S., Irizarry-Negron, V., Halbrook, C. J., Franks, N. E., Hoffman, M. T., … Pasca di Magliano, M. (2021). Inhibition of Hedgehog Signaling Alters Fibroblast Composition in Pancreatic Cancer. Clinical Cancer Research, 27(7), 2023–2037. https://​doi.​org/​10.​1158/​1078-0432.​CCR-20-3715CrossRefPubMedPubMedCentral
41.
42.
go back to reference Cigrovski Bervkovic, M., Cacev, T., Catela Ivkovic, T., Zjacic-Rotkvic, V., & Kapitanovic, S. (2014). New Insights into the Role of Chronic Inflammation and Cytokines in the Etiopathogenesis of Gastroenteropancreatic Neuroendocrine Tumors. Neuroendocrinology, 99, 75–84. https://doi.org/10.1159/0003624339CrossRef Cigrovski Bervkovic, M., Cacev, T., Catela Ivkovic, T., Zjacic-Rotkvic, V., & Kapitanovic, S. (2014). New Insights into the Role of Chronic Inflammation and Cytokines in the Etiopathogenesis of Gastroenteropancreatic Neuroendocrine Tumors. Neuroendocrinology, 99, 75–84. https://​doi.​org/​10.​1159/​0003624339CrossRef
46.
go back to reference Ikebe, M., Kitaura, Y., Nakamura, M., Tanaka, H., Yamasaki, A., Nagai, S., Wada, J., Yanai, K., Koga, K., Sato, N., Kubo, M., Tanaka, M., Onishi, H., & Katano, M. (2009). Lipopolysaccharide (LPS) increases the invasive ability of pancreatic cancer cells through the TLR4/MyD88 signaling pathway. Journal of Surgical Oncology, 100(8), 725–731. https://doi.org/10.1002/jso.21392CrossRefPubMed Ikebe, M., Kitaura, Y., Nakamura, M., Tanaka, H., Yamasaki, A., Nagai, S., Wada, J., Yanai, K., Koga, K., Sato, N., Kubo, M., Tanaka, M., Onishi, H., & Katano, M. (2009). Lipopolysaccharide (LPS) increases the invasive ability of pancreatic cancer cells through the TLR4/MyD88 signaling pathway. Journal of Surgical Oncology, 100(8), 725–731. https://​doi.​org/​10.​1002/​jso.​21392CrossRefPubMed
48.
go back to reference Hoefs, J. C., Renner, I. G., Askhcavai, M., & Redeker, A. G. (1980). Hepatitis B surface antigen in pancreatic and biliary secretions. Gastroenterology, 79(2), 191–194.CrossRef Hoefs, J. C., Renner, I. G., Askhcavai, M., & Redeker, A. G. (1980). Hepatitis B surface antigen in pancreatic and biliary secretions. Gastroenterology, 79(2), 191–194.CrossRef
49.
go back to reference Hassan, M. M., Li, D., El-Deeb, A. S., Wolff, R. A., Bondy, M. L., Davila, M., & Abbruzzese, J. L. (2008). Association between hepatitis B virus and pancreatic cancer. Journal of clinical oncology : Official journal of the American Society of Clinical Oncology, 26(28), 4557–4562. https://doi.org/10.1200/JCO.2008.17.3526CrossRef Hassan, M. M., Li, D., El-Deeb, A. S., Wolff, R. A., Bondy, M. L., Davila, M., & Abbruzzese, J. L. (2008). Association between hepatitis B virus and pancreatic cancer. Journal of clinical oncology : Official journal of the American Society of Clinical Oncology, 26(28), 4557–4562. https://​doi.​org/​10.​1200/​JCO.​2008.​17.​3526CrossRef
50.
go back to reference Xia JY, Zhou YY, Zhao YY. (2005) [Relationship between hepatitis B virus in gastric mucosa and syndrome of disharmony between liver and stomach in patients with chronic hepatitis B]. Zhong Xi Yi Jie He Xue Bao. 3(1):19–22. Chinese. https://doi.org/10.3736/jcim20050107. Xia JY, Zhou YY, Zhao YY. (2005) [Relationship between hepatitis B virus in gastric mucosa and syndrome of disharmony between liver and stomach in patients with chronic hepatitis B]. Zhong Xi Yi Jie He Xue Bao. 3(1):19–22. Chinese. https://​doi.​org/​10.​3736/​jcim20050107.
55.
go back to reference Fan, X., Alekseyenko, A. V., Wu, J., Peters, B. A., Jacobs, E. J., Gapstur, S. M., Purdue, M. P., Abnet, C. C., Stolzenberg-Solomon, R., Miller, G., Ravel, J., Hayes, R. B., & Ahn, J. (2018). Human oral microbiome and prospective risk for pancreatic cancer: A population-based nested case-control study. Gut, 67(1), 120–127. https://doi.org/10.1136/gutjnl-2016-312580CrossRefPubMed Fan, X., Alekseyenko, A. V., Wu, J., Peters, B. A., Jacobs, E. J., Gapstur, S. M., Purdue, M. P., Abnet, C. C., Stolzenberg-Solomon, R., Miller, G., Ravel, J., Hayes, R. B., & Ahn, J. (2018). Human oral microbiome and prospective risk for pancreatic cancer: A population-based nested case-control study. Gut, 67(1), 120–127. https://​doi.​org/​10.​1136/​gutjnl-2016-312580CrossRefPubMed
58.
go back to reference Lovegrove, J. M. (2004). Dental plaque revisited: Bacteria associated with periodontal disease. Journal of the New Zealand Society of Periodontology, 87, 7–21. Lovegrove, J. M. (2004). Dental plaque revisited: Bacteria associated with periodontal disease. Journal of the New Zealand Society of Periodontology, 87, 7–21.
62.
go back to reference Aykut, B., Pushalkar, S., Chen, R., Li, Q., Abengozar, R., Kim, J. I., Shadaloey, S. A., Wu, D., Preiss, P., Verma, N., Guo, Y., Saxena, A., Vardhan, M., Diskin, B., Wang, W., Leinwand, J., Kurz, E., Kochen Rossi, J. A., Hundeyin, M., … Miller, G. (2019). The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature, 574(7777), 264–267. https://doi.org/10.1038/s41586-019-1608-2CrossRefPubMedPubMedCentral Aykut, B., Pushalkar, S., Chen, R., Li, Q., Abengozar, R., Kim, J. I., Shadaloey, S. A., Wu, D., Preiss, P., Verma, N., Guo, Y., Saxena, A., Vardhan, M., Diskin, B., Wang, W., Leinwand, J., Kurz, E., Kochen Rossi, J. A., Hundeyin, M., … Miller, G. (2019). The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature, 574(7777), 264–267. https://​doi.​org/​10.​1038/​s41586-019-1608-2CrossRefPubMedPubMedCentral
63.
go back to reference Rudramurthy, S. M., Honnavar, P., Dogra, S., Yegneswaran, P. P., Handa, S., & Chakrabarti, A. (2014). Association of Malassezia species with dandruff. The Indian journal of medical research, 139(3), 431–437.PubMedPubMedCentral Rudramurthy, S. M., Honnavar, P., Dogra, S., Yegneswaran, P. P., Handa, S., & Chakrabarti, A. (2014). Association of Malassezia species with dandruff. The Indian journal of medical research, 139(3), 431–437.PubMedPubMedCentral
65.
go back to reference Löwik CAM, Zijlstra WP, Knobben BAS, Ploegmakers JJW, Dijkstra B, de Vries AJ, Kampinga GA, Mithoe G, Al Moujahid A, Jutte PC, Wouthuyzen-Bakker M; Northern Infection Network Joint Arthroplasty (NINJA). (2019) Obese patients have higher rates of polymicrobial and Gram-negative early periprosthetic joint infections of the hip than non-obese patients. PLoS One. 14(4):e0215035. https://doi.org/10.1371/journal.pone.0215035. Löwik CAM, Zijlstra WP, Knobben BAS, Ploegmakers JJW, Dijkstra B, de Vries AJ, Kampinga GA, Mithoe G, Al Moujahid A, Jutte PC, Wouthuyzen-Bakker M; Northern Infection Network Joint Arthroplasty (NINJA). (2019) Obese patients have higher rates of polymicrobial and Gram-negative early periprosthetic joint infections of the hip than non-obese patients. PLoS One. 14(4):e0215035. https://​doi.​org/​10.​1371/​journal.​pone.​0215035.
66.
go back to reference Hu, F., Guo, F., Zhu, Y., Zhou, Q., Li, T., Xiang, H., & Shang, D. (2020). IL-17 in pancreatic disease: Pathogenesis and pharmacotherapy. American Journal of Cancer Research, 10(11), 3551–3564.PubMedPubMedCentral Hu, F., Guo, F., Zhu, Y., Zhou, Q., Li, T., Xiang, H., & Shang, D. (2020). IL-17 in pancreatic disease: Pathogenesis and pharmacotherapy. American Journal of Cancer Research, 10(11), 3551–3564.PubMedPubMedCentral
75.
go back to reference Huang, J. Y., Luu, H. N., Butler, L. M., Midttun, Ø., Ulvik, A., Wang, R., Jin, A., Gao, Y. T., Tan, Y., Ueland, P. M., Koh, W. P., & Yuan, J. M. (2020). A prospective evaluation of serum methionine-related metabolites in relation to pancreatic cancer risk in two prospective cohort studies. International Journal of Cancer, 147(7), 1917–1927. https://doi.org/10.1002/ijc.32994CrossRefPubMed Huang, J. Y., Luu, H. N., Butler, L. M., Midttun, Ø., Ulvik, A., Wang, R., Jin, A., Gao, Y. T., Tan, Y., Ueland, P. M., Koh, W. P., & Yuan, J. M. (2020). A prospective evaluation of serum methionine-related metabolites in relation to pancreatic cancer risk in two prospective cohort studies. International Journal of Cancer, 147(7), 1917–1927. https://​doi.​org/​10.​1002/​ijc.​32994CrossRefPubMed
77.
go back to reference Tucker, O. N., Dannenberg, A. J., Yang, E. K., & Fahey, T. J. (2004). 3rd Bile acids induce cyclooxygenase-2 expression in human pancreatic cancer cell lines. Carcinogenesis, 25, 419–423.CrossRef Tucker, O. N., Dannenberg, A. J., Yang, E. K., & Fahey, T. J. (2004). 3rd Bile acids induce cyclooxygenase-2 expression in human pancreatic cancer cell lines. Carcinogenesis, 25, 419–423.CrossRef
81.
83.
go back to reference Huang, Y., Yang, W., Liu, H., Duan, J., Zhang, Y., Liu, M., Li, H., Hou, Z., & Wu, K. K. (2012). Effect of high-dose methotrexate chemotherapy on intestinal Bifidobacteria, Lactobacillus and Escherichia coli in children with acute lymphoblastic leukemia. Experimental Biology and Medicine (Maywood, N.J.), 237(3), 305–311. https://doi.org/10.1258/ebm.2011.011297CrossRef Huang, Y., Yang, W., Liu, H., Duan, J., Zhang, Y., Liu, M., Li, H., Hou, Z., & Wu, K. K. (2012). Effect of high-dose methotrexate chemotherapy on intestinal Bifidobacteria, Lactobacillus and Escherichia coli in children with acute lymphoblastic leukemia. Experimental Biology and Medicine (Maywood, N.J.), 237(3), 305–311. https://​doi.​org/​10.​1258/​ebm.​2011.​011297CrossRef
85.
89.
go back to reference Otieno, S; Jain, A.L.; Mohammed, O; Patel, J.R.; Collyer, J; Deleeuw, P; Husain, A; Weir, A.B. (2021) Positive association between Helicobacter pylori infection and pancreatic cancer: A Case control study. Journal of Clinical Oncology. e16243. Otieno, S; Jain, A.L.; Mohammed, O; Patel, J.R.; Collyer, J; Deleeuw, P; Husain, A; Weir, A.B. (2021) Positive association between Helicobacter pylori infection and pancreatic cancer: A Case control study. Journal of Clinical Oncology. e16243.
91.
go back to reference Vétizou, M., Pitt, J. M., Daillère, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M. P., Duong, C. P., Poirier-Colame, V., Roux, A., Becharef, S., Formenti, S., Golden, E., Cording, S., Eberl, G., Schlitzer, A., Ginhoux, F., Mani, S., et al. (2015). Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science (New York, N.Y.), 350(6264), 1079–1084. https://doi.org/10.1126/science.aad1329CrossRef Vétizou, M., Pitt, J. M., Daillère, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M. P., Duong, C. P., Poirier-Colame, V., Roux, A., Becharef, S., Formenti, S., Golden, E., Cording, S., Eberl, G., Schlitzer, A., Ginhoux, F., Mani, S., et al. (2015). Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science (New York, N.Y.), 350(6264), 1079–1084. https://​doi.​org/​10.​1126/​science.​aad1329CrossRef
93.
go back to reference Lopès, A., Billard, E., Casse, A. H., Villéger, R., Veziant, J., Roche, G., Carrier, G., Sauvanet, P., Briat, A., Pagès, F., Naimi, S., Pezet, D., Barnich, N., Dumas, B., & Bonnet, M. (2020). Colibactin-positive Escherichia coli induce a procarcinogenic immune environment leading to immunotherapy resistance in colorectal cancer. International Journal of Cancer, 146(11), 3147–3159. https://doi.org/10.1002/ijc.32920CrossRefPubMed Lopès, A., Billard, E., Casse, A. H., Villéger, R., Veziant, J., Roche, G., Carrier, G., Sauvanet, P., Briat, A., Pagès, F., Naimi, S., Pezet, D., Barnich, N., Dumas, B., & Bonnet, M. (2020). Colibactin-positive Escherichia coli induce a procarcinogenic immune environment leading to immunotherapy resistance in colorectal cancer. International Journal of Cancer, 146(11), 3147–3159. https://​doi.​org/​10.​1002/​ijc.​32920CrossRefPubMed
97.
go back to reference Goradel NH, Alizadeh A, Hosseinzadeh S, Taghipour M, Ghesmati Z, Arashkia A, Negahdari B. (2021) Oncolytic virotherapy as promising immunotherapy against cancer: mechanisms of resistance to oncolytic viruses. Future Oncol. 25. https://doi.org/10.2217/fon-2021-0802 Goradel NH, Alizadeh A, Hosseinzadeh S, Taghipour M, Ghesmati Z, Arashkia A, Negahdari B. (2021) Oncolytic virotherapy as promising immunotherapy against cancer: mechanisms of resistance to oncolytic viruses. Future Oncol. 25. https://​doi.​org/​10.​2217/​fon-2021-0802
101.
go back to reference Chang, K. C., Burnham, C. A., Compton, S. M., Rasche, D. P., Mazuski, R. J., McDonough, J. S., Unsinger, J., Korman, A. J., Green, J. M., & Hotchkiss, R. S. (2013). Blockade of the negative co-stimulatory molecules PD-1 and CTLA-4 improves survival in primary and secondary fungal sepsis. Critical Care, 17(3), R85. https://doi.org/10.1186/cc12711CrossRefPubMedPubMedCentral Chang, K. C., Burnham, C. A., Compton, S. M., Rasche, D. P., Mazuski, R. J., McDonough, J. S., Unsinger, J., Korman, A. J., Green, J. M., & Hotchkiss, R. S. (2013). Blockade of the negative co-stimulatory molecules PD-1 and CTLA-4 improves survival in primary and secondary fungal sepsis. Critical Care, 17(3), R85. https://​doi.​org/​10.​1186/​cc12711CrossRefPubMedPubMedCentral
103.
go back to reference Krishnan, S., Chadha, A. S., Suh, Y., Chen, H. C., Rao, A., Das, P., Minsky, B. D., Mahmood, U., Delclos, M. E., Sawakuchi, G. O., Beddar, S., Katz, M. H., Fleming, J. B., Javle, M. M., Varadhachary, G. R., Wolff, R. A., & Crane, C. H. (2016). Focal Radiation Therapy Dose Escalation Improves Overall Survival in Locally Advanced Pancreatic Cancer Patients Receiving Induction Chemotherapy and Consolidative Chemoradiation. International Journal of Radiation Oncology, Biology, Physics, 94(4), 755–765. https://doi.org/10.1016/j.ijrobp.2015.12.003CrossRefPubMed Krishnan, S., Chadha, A. S., Suh, Y., Chen, H. C., Rao, A., Das, P., Minsky, B. D., Mahmood, U., Delclos, M. E., Sawakuchi, G. O., Beddar, S., Katz, M. H., Fleming, J. B., Javle, M. M., Varadhachary, G. R., Wolff, R. A., & Crane, C. H. (2016). Focal Radiation Therapy Dose Escalation Improves Overall Survival in Locally Advanced Pancreatic Cancer Patients Receiving Induction Chemotherapy and Consolidative Chemoradiation. International Journal of Radiation Oncology, Biology, Physics, 94(4), 755–765. https://​doi.​org/​10.​1016/​j.​ijrobp.​2015.​12.​003CrossRefPubMed
116.
go back to reference Waghray, M., Cui, Z., Horowitz, J. C., Subramanian, I. M., Martinez, F. J., Toews, G. B., et al. (2005). Hydrogen peroxide is a diffusible paracrine signal for the induction of epithelial cell death by activated myofibroblasts. The FASEB Journal, 19, 854–856.CrossRef Waghray, M., Cui, Z., Horowitz, J. C., Subramanian, I. M., Martinez, F. J., Toews, G. B., et al. (2005). Hydrogen peroxide is a diffusible paracrine signal for the induction of epithelial cell death by activated myofibroblasts. The FASEB Journal, 19, 854–856.CrossRef
119.
go back to reference Lisanti, M. P., Martinez-Outschoorn, U. E., Lin, Z., Pavlides, S., Whitaker-Menezes, D., Pestell, R. G., Howell, A., & Sotgia, F. (2011). Hydrogen peroxide fuels aging, inflammation, cancer metabolism and metastasis: the seed and soil also needs “fertilizer.” Cell cycle (Georgetown, Tex.), 10(15), 2440–2449. https://doi.org/10.4161/cc.10.15.16870CrossRef Lisanti, M. P., Martinez-Outschoorn, U. E., Lin, Z., Pavlides, S., Whitaker-Menezes, D., Pestell, R. G., Howell, A., & Sotgia, F. (2011). Hydrogen peroxide fuels aging, inflammation, cancer metabolism and metastasis: the seed and soil also needs “fertilizer.” Cell cycle (Georgetown, Tex.), 10(15), 2440–2449. https://​doi.​org/​10.​4161/​cc.​10.​15.​16870CrossRef
123.
go back to reference Graham, F. (2019) Daily briefing: Fecal Transplant linked to patient’s death. Nature Briefing. Graham, F. (2019) Daily briefing: Fecal Transplant linked to patient’s death. Nature Briefing.
126.
127.
go back to reference Oláh, A., Belágyi, T., Pótó, L., Romics, L., Jr., & Bengmark, S. (2007). Synbiotic control of inflammation and infection in severe acute pancreatitis: A prospective, randomized, double blind study. Hepato-Gastroenterology, 54(74), 590–594.PubMed Oláh, A., Belágyi, T., Pótó, L., Romics, L., Jr., & Bengmark, S. (2007). Synbiotic control of inflammation and infection in severe acute pancreatitis: A prospective, randomized, double blind study. Hepato-Gastroenterology, 54(74), 590–594.PubMed
131.
go back to reference Oliver, A., Chase, A. B., Weihe, C., Orchanian, S. B., Riedel, S F., Hendrickson, C. L., Lay, M., Sewall, J. M., Martiny, J. B. H., & Whiteson, K. (2021). High-Fiber, whole-food dietary intervention alters the human gut microbiome but not fecal short chain fatty acids. Journal of Clinical Microbiology. https://doi.org/10.1128/mSystems.00115-21 Oliver, A., Chase, A. B., Weihe, C., Orchanian, S. B., Riedel, S F., Hendrickson, C. L., Lay, M., Sewall, J. M., Martiny, J. B. H., & Whiteson, K. (2021). High-Fiber, whole-food dietary intervention alters the human gut microbiome but not fecal short chain fatty acids. Journal of Clinical Microbiology. https://​doi.​org/​10.​1128/​mSystems.​00115-21
132.
go back to reference USDA Economic Research Service. (2020). Key Statistics and Graphics. Accessed 11/30/2021. USDA Economic Research Service. (2020). Key Statistics and Graphics. Accessed 11/30/2021.
133.
go back to reference Shrider, E. A., Kollar, M., Semega, J. (2021). Income and poverty in the United States: 2020. United States Census Bureau. Accessed 11/30/2021. Shrider, E. A., Kollar, M., Semega, J. (2021). Income and poverty in the United States: 2020. United States Census Bureau. Accessed 11/30/2021.
135.
go back to reference Pandol, S. J., Apte, M. V., Wilson, J. S., Gukovskaya, A. S., & Edderkaoui, M. (2012). The burning question: why is smoking a risk factor for pancreatic cancer?. Pancreatology : official journal of the International Association of Pancreatology (IAP) ... [et al.], 12(4), 344–349. https://doi.org/10.1016/j.pan.2012.06.002 Pandol, S. J., Apte, M. V., Wilson, J. S., Gukovskaya, A. S., & Edderkaoui, M. (2012). The burning question: why is smoking a risk factor for pancreatic cancer?. Pancreatology : official journal of the International Association of Pancreatology (IAP) ... [et al.]12(4), 344–349. https://​doi.​org/​10.​1016/​j.​pan.​2012.​06.​002
Metadata
Title
Connecting the Human Microbiome and Pancreatic Cancer
Authors
Rachel E. Sexton
Md Hafiz Uddin
Sahar Bannoura
Husain Yar Khan
Yousef Mzannar
Yiwei Li
Amro Aboukameel
Mohammad Najeeb Al-Hallak
Bayan Al-Share
Amr Mohamed
Misako Nagasaka
Bassel El-Rayes
Asfar S. Azmi
Publication date
02-04-2022
Publisher
Springer US
Published in
Cancer and Metastasis Reviews / Issue 2/2022
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-022-10022-w

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