Metagenomic Identification of Microbial Signatures Predicting Pancreatic Cancer From a Multinational Study

Nagata, Naoyoshi; Nishijima, Suguru; Kojima, Yasushi; Hisada, Yuya; Imbe, Koh; Miyoshi‐Akiyama, Tohru; Suda, Wataru; Kimura, Moto; Aoki, Ryo; Sekine, Katsunori; Ohsugi, Mitsuru; Miki, Kuniko; Osawa, Tsuyoshi; Ueki, Kohjiro; Oka, Shinichi; Mizokami, Masashi; Kartal, Ece; Schmidt, Thomas Sebastian Benedikt; Molina‐Montes, Esther; Estudillo, Lidia; Malats, Núria; Trebicka, Jonel; Kersting, Stephan; Langheinrich, Melanie; Bork, Peer; Uemura, Naomi; Itoi, Takao; Kawai, Takashi

doi:10.1053/j.gastro.2022.03.054

Cited by 105 publications

(124 citation statements)

References 67 publications

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“…In addition, smoking is a well-described risk factor for PDAC, and smoking cessation results in an increase in Firmicutes and Actinobacteria and a decrease in Proteobacteria and Bacteroidetes species within the intestine [ 28 ]. A recent report from Japan showed significant enrichments of Streptococcus and Veillonella spp and a depletion of Faecalibacterium prausnitzii in oral and fecal samples in PDAC patients, which are commonly observed in German and Spanish cohorts [ 29 ].…”

Section: Association Of Oral Gut and Intratumor Microbiomes With Pdacmentioning

confidence: 99%

The Role of the Microbiome in Pancreatic Cancer

Miyabayashi

Ijichi

Fujishiro

2022

Cancers

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Pancreatic ductal adenocarcinoma (PDAC) is one of the most lethal malignancies, with little improvement in outcomes in recent decades, although the molecular and phenotypic characterization of PDAC has contributed to advances in tailored therapies. PDAC is characterized by dense stroma surrounding tumor cells, which limits the efficacy of treatment due to the creation of a physical barrier and immunosuppressive environment. Emerging evidence regarding the microbiome in PDAC implies its potential role in the initiation and progression of PDAC. However, the underlying mechanisms of how the microbiome affects the local tumor microenvironment (TME) as well as the systemic immune system have not been elucidated in PDAC. In addition, therapeutic strategies based on the microbiome have not been established. In this review, we summarize the current evidence regarding the role of the microbiome in the development of PDAC and discuss a possible role for the microbiome in the early detection of PDAC in relation to premalignant pancreatic diseases, such as chronic pancreatitis and intraductal papillary mucinous neoplasm (IPMN). In addition, we discuss the potential role of the microbiome in the treatment of PDAC, especially in immunotherapy, although the biomarkers used to predict the efficacy of immunotherapy in PDAC are still unknown. A comprehensive understanding of tumor-associated immune responses, including those involving the microbiome, holds promise for new treatments in PDAC.

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Section: Association Of Oral Gut and Intratumor Microbiomes With Pdacmentioning

confidence: 99%

The Role of the Microbiome in Pancreatic Cancer

Miyabayashi

Ijichi

Fujishiro

2022

Cancers

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Section: Tumour Microenvironmentmentioning

confidence: 99%

“…Emerging evidence suggests a feasibility of non-invasive faecal microbiota-based screening for the early detection of pancreatic cancer 52 53. Pancreatic adenocarcinoma could be predicted robustly and accurately by metagenomic classifiers based on faecal microbial species 52 53 . Veillonella species ( eg , V. atypica ) and Streptococcus species were enriched, and Faecalibacterium prausnitzii was depleted in faecal samples of pancreatic adenocarcinoma patients 52 53…”

Section: Tumour Microenvironmentmentioning

confidence: 99%

Cancer as microenvironmental, systemic and environmental diseases: opportunity for transdisciplinary microbiomics science

Inamura

Hamada

Bullman

et al. 2022

Gut

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Cancer is generally regarded as a localised disease, with the well-established role of the tumour microenvironment. However, the realm of cancer goes beyond the tumour microenvironment, and cancer should also be regarded as a systemic and environmental disease. The exposome (ie, the totality of exposures), which encompasses diets, supplements, smoking, alcohol, other lifestyle factors, medications, etc, likely alters the microbiome (inclusive of bacteria, viruses, archaea, fungi, parasites, etc) and immune system in various body sites and influences tumour phenotypes. The systemic metabolic/inflammatory status, which is likely influenced by exposures and intestinal physiological changes, may affect tissue microenvironment of colorectum and any other organs. Germline genomic factors can modify disease phenotypes via gene-by-environment interactions. Although challenges exist, it is crucial to advance not only basic experimental research that can analyse the effects of exposures, microorganisms and microenvironmental components on tumour evolution but also interdisciplinary human population research that can dissect the complex pathogenic roles of the exposome, microbiome and immunome. Metagenomic, metatranscriptomic and metabolomic analyses should be integrated into well-designed population research combined with advanced methodologies of artificial intelligence and molecular pathological epidemiology. Ideally, a prospective cohort study design that enables biospecimen (such as stool) collection before disease detection should be considered to address reverse causation and recall biases. Robust experimental and observational research together can provide insights into dynamic interactions between environmental exposures, microbiota, tumour and immunity during carcinogenesis processes, thereby helping us develop precision prevention and therapeutic strategies to ultimately reduce the cancer burden.

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“…In addition to the findings above, numerous other studies have led to increased enthusiasm and expectations that oral microbiome assessment can be used for diagnostic or prognostic purposes of such distant pathologies as gastro-intestinal tract cancers. This has resulted in cross-sectional case–control studies where oral microbiome, frequently collected as salivary or an oral rinse sample or via an oral mucosal swab, is used to predict the cancer cases or cancer severity [ 18 , 19 , 20 , 21 ]. For instance, 16 bacterial OTUs (operational taxonomic units) in oral mucosal swabs (several OTUs of Prevotella, Anaerostipes, Porphyromonas, Neisseria, Haemophilus, Fusobacterium, Peptostreptococcus, Streptococcus, Alloprevotella, Megasphaera, Leptotrichia and Cardiobacterium ) were identified to classify colorectal carcinoma cases with the sensitivity of 53% and specificity of 96% [ 18 ].…”

Section: Oral Microbiome and Distant Pathologiesmentioning

confidence: 99%

“…When the same method was used with the microbiome of the fecal samples, the sensitivity of the model was only 22%, while the combination of the two samples increased the sensitivity for the detection of colorectal carcinoma cases to 76%. On the other hand, a multinational study involving saliva from pancreatic cancer cases and controls found a high false positive rate when a Japanese dataset was validated against a Spanish dataset or vice versa, or when the selected biomarker species were validated against saliva of cases and controls from other studies with diseases such as rheumatoid arthritis, colorectal carcinoma or diabetes mellitus [ 21 ]. Paradoxically, different studies identify the same species in oral samples associated with either increased or decreased risk for the same cancer type: e.g., genera Leptotrichia and Streptococcus have been associated with both decreased and increased pancreatic cancer risk [ 22 ].…”

Section: Oral Microbiome and Distant Pathologiesmentioning

confidence: 99%

A Commentary on the Potential Use of Oral Microbiome in Prediction, Diagnosis or Prognostics of a Distant Pathology

Zaura

2022

Dentistry Journal

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In health, the oral microbiome is in balance with its host. If this balance is lost, this symbiosis is replaced by dysbiotic microbial communities, which are thought to affect the rest of the body either directly or via metabolites or pro-inflammatory molecules. The association of oral microbiome with general health has led to attempts to use oral microbial biomarkers for the prediction, diagnosis or prognosis of distant pathologies such as colorectal carcinoma or pancreatic cancer. These attempts however have no chance to succeed if the complexity of the oral ecosystem and the interplay of environmental, behavioral and biological factors is not taken into account. Standardized, well-documented oral sample collection procedures together with detailed clinical oral examination and behavioral data are the prerequisites for the successful evaluation of the oral microbiome as a potential biomarker for distant pathologies.

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Metagenomic Identification of Microbial Signatures Predicting Pancreatic Cancer From a Multinational Study

Cited by 105 publications

References 67 publications

The Role of the Microbiome in Pancreatic Cancer

The Role of the Microbiome in Pancreatic Cancer

Cancer as microenvironmental, systemic and environmental diseases: opportunity for transdisciplinary microbiomics science

A Commentary on the Potential Use of Oral Microbiome in Prediction, Diagnosis or Prognostics of a Distant Pathology

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