Intratumoral microorganisms in tumors of the digestive system

Xuan, Mengjuan; Gu, Xinyu; Liu, Yingru; Yang, Li; Li, Yi; Huang, Di; Li, Juan; Xue, Chen

doi:10.1186/s12964-023-01425-5

Cell Communication and Signaling

Table 1 Intratumoral microbiome in different digestive system tumors

From: Intratumoral microorganisms in tumors of the digestive system

Cancer type	Year	Included samples	Methods	Enriched microorganism	Reduced microorganism	Implications	Ref
Esophageal cancer	2016	325 pairs of EC samples and adjacent normal tissue samples	qPCR	Fusobacterium nucleatum	/	predicting shorter survival	[48]
	2018	45 esophageal squamous cell carcinoma tissue samples from N+ (positive lymph node) patients and N- (negative lymph node) controls	16 S rRNA sequencing	Phylum Bacteroidetes, Firmicutes, and Spirochetes, Streptococcus, Prevotella	Proteobacteria	associated with unfavorable survival	[49]
	2019	551 patients with esophageal squamous cell carcinoma from two independent cohorts	qPCR	Fusobacterium nucleatum	/	predicting poor recurrence-free survival	[50]
	2019	16 controls, 14 Barrett’s esophagus without dysplasia, 6 low-grade dysplasia, 5 high-grade dysplasia, and 4 esophageal adenocarcinoma samples	16 S rRNA sequencing	Proteobacteria, Enterobacteriaceae, Akkermansia, muciniphila	Firmicutes, Veillonella	promoting carcinogenesis	[12]
	2021	120 esophageal squamous cell carcinoma resected samples and 30 pre-treatment biopsy samples	qPCR	Fusobacterium nucleatum	/	inducing chemoresistance	[51]
	2021	42 pairs of tumors and nontumor tissues, 69 only tumor tissues	16 S rRNA sequencing	Bacteroidetes, Fusobacteria, Spirochetes	Butyrivibrio, Lactobacillus	predicting prognosis and metastasis	[52]
	2021	40 tumor samples of esophageal squamous cell carcinoma, 20 tumor samples of esophageal adenocarcinoma, and 22 adjacent normal samples	/	Firmicutes, Fusobacteria	Proteobacteria	associated with clinical features	[28]
Gastric cancer	2015	212 chronic gastritis tissue and 103 gastric cancer tissue	qPCR	/	/	increasing bacterial load	[53]
	2017	160 pairs of non-malignant and tumor tissues	16 S rRNA sequencing	Bacteriodetes, Firmicutes, Fusobacteria, Spirochetes	Proteobacteria	altering non- Helicobacter pylori bacteria abundance	[39]
	2018	54 gastric carcinoma and 81 chronic gastritis tissues	16 S rRNA sequencing, qPCR	Actinobacteria, Firmicutes	Bacteroidetes, Fusobacteria	distinguishing between gastritis and gastric cancer	[54]
	2019	230 normal, 247 peritumor, and 229 tumor tissues	16 S rRNA sequencing	Prevotella melaninogenica, Streptococcus anginosus, Propionibacterium acnes	Helicobacter pylori, Prevotella copri, Bacteroides uniformis	/	[55]
	2023	20 gastric biopsy tissue samples	Whole metagenomic shotgun sequencing	/	/	revealing changes in composition and function	[56]
Colorectal cancer	2012	11 pairs of colorectal carcinoma and adjacent normal tissue specimens	qPCR	Fusobacterium	/	revealing the prevalence of Fusobacterium infection in colorectal cancer	[57]
	2012	9 tumor and normal pairs, 95 carcinoma and normal DNA pairs	whole genome sequences, qPCR, 16 S rDNA sequencing, FISH	Fusobacterium	Bacteroidetes, Firmicutes	revealing Fusobacterium associated with colorectal cancer	[58]
	2013	65 pairs of colorectal carcinoma and matched normal control tissues	Metatranscriptomic analysis	Fusobacterium, Leptotrichia, Campylobacter spp	/	revealing Fusobacterium associated with colorectal cancer	[59]
	2014	49 tumor and 32 matched normal tissue samples, 45 pairs of tumors tissue and matched normal tissue samples, 28 tumor and 52 adenoma samples	qPCR	Fusobacterium	/	promoting tumor progression	[60]
	2015	31 cancerous tissues and 20 adjacent non-cancerous tissues, 15 proximal colon cancer tissues and 16 distal colon cancer tissues, 15 healthy proximal colon tissues and 15 healthy distal colon tissues	16 S rRNA sequencing	Firmicutes, Fusobacteria, Lactococcus, Fusobacterium	Proteobacteria, Pseudomonas, Escherichia– Shigella	associated with colorectal cancer risk	[61]
	2015	55 pairs of colorectal cancer samples and matched normal samples	qPCR	enterotoxigenic Bacteroides fragilis, pks-positive E. coli, Fusobacterium spp.	/	associated with clinicopathological features	[62]
	2015	44 pairs of colorectal cancer samples and matched normal samples	16 S rRNA gene sequencing, qPCR	Proteobacteria, Fusobacteria	Firmicutes, Bacteroidetes	promoting tumor progression	[63]
	2016	2 U.S. nationwide prospective cohort studies	qPCR	Fusobacteria	/	predicting shorter survival	[64]
	2017	59 samples from patients undergoing surgery for colorectal cancer, 21 polyp samples, and 56 healthy controls	16 S rRNA sequencing, qPCR	Bacteroidetes Cluster 2, Firmicutes Cluster 2, Pathogen Cluster, Prevotella Cluster	Bacteroidetes Cluster 1, Firmicutes Cluster 1	associated with distinct mucosal gene-expression profiles	[65]
	2017	160 microsatellite instability-high colorectal cancer samples	qPCR	Fusobacterium nucleatum	/	modulating the immune microenvironment	[66]
	2017	11 pairs of fresh-frozen tumor and liver metastases samples, 77 fresh-frozen tumor samples, published data from 430 resected fresh-frozen colorectal cancer and 201 resected fresh-frozen hepatocellular carcinoma samples, 101 pairs of formalin-fixed paraffin-embedded colorectal cancer and liver metastases, 13 colorectal cancer samples for xenograft	qPCR, 16 S rRNA sequencing	Fusobacterium	/	associated with liver metastasis	[67]
	2018	5 FAP resected tissues and 1 juvenile polyposis syndrome resected tissue, 20 controls	16 S rRNA sequencing, FISH	Bacteroides fragilis, Escherichia coli	Fusobacteria	inducing tumorigenesis	[68]
	2018	74 colorectal cancer samples and 92 controls	shotgun metagenomic analyses	Bacteriophage	/	predicting colorectal cancer progression	[69]
	2018	1014 tumor tissue samples	qPCR	Fusobacterium nucleatum	/	promoting tumor progression	[70]
	2019	184 colorectal cancer samples, 197 adenoma samples, 204 controls	shotgun metagenomic sequencing	Malasseziomycetes	Saccharomycetes, Pneumocystidomycetes	revealing colorectal cancer-associated mycobiome dysbiosis	[71]
	2019	91 tumor tissue samples	qPCR	Fusobacterium nucleatum	/	predicting poor prognosis	[72]
	2021	36 colorectal cancer samples, 32 adenoma samples	16 S rRNA sequencing	/	/	revealing microbial community heterogeneity	[73]
	2021	excised colons from mice, human colonic adenomas	qPCR	/	Fusobacterium nucleatum	inhibited by aspirin	[74]
	2022	1,368 samples from 7 publicly available cohorts and one new Chinese cohort	shotgun metagenomic sequencing	Candida pseudohaemulonis, Aspergillus ochraceoroseus, A. rambellii, Malassezia globosa	Aspergillus niger, Macrophomina phaseolina, Talaromyces islandicus, Sistotremastrum niveocremeum	revealing changes in fungal microbiome colorectal cancer	[75]
	2022	118 colorectal cancer samples, 140 colorectal adenomas samples, 128 controls	GC-TOFMS, whole-genome shotgun sequencing	/	/	using intestinal metabolites to diagnose colorectal cancer	[76]
	2022	116 samples of adenocarcinomas, paired adenomatous polyps, and paired normal colon tissues	16 S rRNA sequencing, qPCR	B. fragilis, Fusobacterium, Prevotella intermedia	/	predicting malignant transformation, migration and invasion	[77]
Pancreatic cancer	2006	40 pancreatic cancer samples, 14 neuroendocrine cancer samples, 8 multiple endocrine neoplasia type 1 samples, and 5 chronic pancreatitis samples; 10 benign pancreatic disease samples and 7 normal pancreatic samples	PCR	Helicobacter pylori	/	revealing the association between Helicobacter pylori and PC	[23]
	2010	6 pancreatic ductal adenocarcinoma samples, 4 chronic pancreatitis samples, 5 other gastrointestinal cancers samples, 20 healthy samples	PCR	/	/	revealing the impossibility of direct infection	[78]
	2015	283 pancreatic cancer samples	qPCR	Fusobacterium	/	predicting poor prognosis	[32]
	2016	361 pancreatic ductal adenocarcinoma samples and 371 controls	16 S rRNA sequencing	P. gingivalis, A. actinomycetemcomitans, Fusobacteria	/	promoting carcinogenesis of pancreatic cancer	[79]
	2017	113 pancreatic ductal adenocarcinoma samples, 20 normal pancreatic tissue samples	qPCR, 16 S rRNA sequencing, immunohistochemistry	Gammaproteobacteria	/	mediating gemcitabine resistance	[80]
	2018	7 normal samples, 4 pancreatitis samples, 16 pancreatic ductal adenocarcinoma samples	16 S rRNA sequencing	/	/	revealing the presence of microbes in pancreas	[24]
	2019	41 mild acute pancreatitis samples, 59 moderately severe acute pancreatitis samples, 30 severe acute pancreatitis samples, 35 healthy controls	16 S rRNA sequencing	Acinetobacter, Stenotrophomonas, Geobacillus	Bacteroides, Alloprevotella, Blautia, Gemella	revealing the presence of microbes in pancreas	[81]
	2019	83 samples of pancreatic cancer patients receiving neoadjuvant therapy, 89 samples of pancreatic cancer patients who underwent surgery	/	Enterococci, Klebsiella	/	revealing the alteration in the biliary microbiome	[82]
	2019	36 long-term survival pancreatic adenocarcinoma samples, 32 short-term survival long-term survival samples	16 S rRNA sequencing	Alphaprotebacteria Sphingobacteria, Flavobacteria	Clostridia, Bacteroides	influencing pancreatic cancer outcomes	[11]
	2019	/	18 S rRNA sequencing, FISH	Malassezia	/	promoting pancreatic cancer progression	[83]
	2020	273 pancreatic adenocarcinoma samples and 285 controls	16 S rRNA sequencing	Enterobacteriaceae, Lachnospiraceae G7, Bacteroidaceae, Staphylococcaceae	Haemophilus	revealing the association between oral microbiota and pancreatic cancer	[84]
	2020	15 pairs of pancreatic adenocarcinoma samples and matched normal samples	16 S rRNA sequencing	Tepidimonas, Akkermansia	Leuconostoc, Sutterella	revealing the diversity of the microbiome in pancreatic adenocarcinoma	[85]
	2020	solid (duodenal mucosa, pancreatic tumor tissue, and stool) and liquid (bile and drainage fluid) biopsy samples from 10 patients	16 S rRNA sequencing	Enterococcus	/	associated with postoperative pancreatic fistula	[86]
	2020	74 pancreatic adenocarcinoma samples, 98 pancreatic cyst samples, 134 normal pancreas controls	16 S rRNA sequencing, 18 S rRNA sequencing	Bifidobacterium, Fusobacteria, Rothia	/	altering duodenal fluid microbiome profile in pancreatic adenocarcinoma	[87]
	2021	27 pairs of tumor samples and matched normal samples	16 S rRNA sequencing, qPCR	Enterobacteriaceae	/	promoting bacterial colonization of pancreatic adenocarcinoma tissues	[25]
Hepatocellular carcinoma	2004	20 primary liver carcinoma samples, 16 controls	16 S rRNA sequencing, PCR	/	/	detecting the 16 S rDNA of Helicobacter pylori in liver cancer tissue	[30]
	2022	156 samples: 28 normal liver, 64 peritumor, and 64 hepatocellular carcinoma tissues	16 S rRNA sequencing	Patescibacteria, Proteobacteria, Bacteroidota, Firmicutes, Actinobacteriota	/	revealing the intratumoral bacterial metataxonomic signature in hepatocellular carcinoma	[88]
	2023	78 pairs of liver tumor and paratumor tissues, 13 tumor tissues, 18 tumor tissues obtained from multiple lesions in 8 cases	FISH, 16 S rDNA sequencing	Proteobacteria, Actinobacteria	Deinococcus– Thermus	predicting the prognosis of hepatocellular carcinoma after surgery	[89]

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ISSN: 1478-811X

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