Microbial Biomarkers for Lung Cancer: Current Understandings and Limitations
Abstract
:1. Introduction
2. Lung or Tumor-Resident Microbiome and Lung Cancers
2.1. Few Commonalities across Different Lung Microbiome Profilings
Study | Sampling Site | Disease | Experiment Design | Sequencing Methods * | Diversity Variations in LC | Microbial Associations or Biomarkers |
---|---|---|---|---|---|---|
Yuan [24] | Tumor | LC | RM LC (n = 174) vs. non-RM LC (n = 134) | TCGA | RM LC has similar α-diversity, but reduced richness | Acidovorax, Clostridioides, Succinimonas, Shewanella, Leuconostoc and Dickeya are biomarkers for RM LC |
Baranova [25] | Sputum | LUSC | Patients (n = 40) vs. healthy controls (n = 40); all male | 16S V3–V4 | Decreased β-diversity in LUSC; no changes in α-diversity | Streptococcus, Bacillus, Gemella and Haemophilus are enriched in LUSC patients |
Wu [26] | BALF; tumor | LC as GGO | BALF from diseased lung and paired contralateral healthy lung (n = 11); lung GGO and paired adjacent normal tissues (n = 26) | 16S V4/16S V3/16S V3–V4/16S V4–V5 | No changes in α- and β-diversity | Significantly reduced Proteobacteria in LC tissues; In BALF of LC patients: reduced Rothia, and increased Lachnospiraceae, Bacteroides uniforms and Faecalibacterium prausnitzii |
He [27] | Sputum | NSCLC and/or COPD | patients with NSCLC and COPD (CN, n = 67) vs. NSCLC (n = 9) vs. COPD (n = 14) | 16S V3–V4 | No significant differences in diversities | In CN patients: reduced Streptococcus, Veillonella, Moraxella and Actinomyces; and increased Neisseria and Acinetobacter |
Vogtmann [28] | Oral wash | LC | Patients (n = 1306) | 16S V4 | Higher α-diversity is associated with lower LC risk | Increased Streptococcus and Peptoniphilus abundances are associated with increased LC risk, while Peptostreptococcus, Eubacterium yurii and Aggregatibacter are associated with reduced risk |
Kim [29] | Tumor | NSCLC | Tumor tissue (n = 162) vs. adjacent normal tissue (n = 54) | 16S V4–V5 | Reduced diversity as LC progress | Increased Romboutsia, Novosphingobium, Acinetobacter and Prevotella in LC Increased Stenotrophomonas upon LC relapse |
Qian [30] | BALF; airway protected brushing | sMPLC | Patients (n = 8) | 16S V3–V4 | Increased α-diversity in BALF | Clostridium, Actinobacteria, Fusobacterium and Rothia are enriched in the BALF of sMPLC lesions |
Chen [19] | Tumor | LC | Tumor tissue (n = 34) vs. adjacent normal tissue (n = 29) | 16S | Lower α-diversity and higher β-diversity in LC tissues | In LC: increased Staphylococcus, Capnocytophaga, Lachnoanaerobaculum, Fusobacterium, Oligella, Rubellimicrobium, Marinococcus Sphingomonas and Sphingopyxis; and decreased Comamonas and Peptococcus |
Masuhiro [31] | BALF | LC | Patients under PD-1 blockade treatment (n = 12) | 16S V3–V4 | Higher diversity in responders | Responders have higher Bacteroidetes and lower Proteobacteria |
Zhang [32] | BALF; tumor | NSCLC | Patients (n = 6 for BALF; n = 37 for tumor tissues) | Pathogen-targeted sequencing (tumor and 4 BALF); 16S (2 BALF) | Higher diversity in BALF than in tumor | BALF and tumor tissues share Streptococcus pneumoniae, S. crista, S. constellatus, S. gordonii, Prevotella II, Haemophilus, H. haemolyticus, H. influenzae, Actinomyces Neesii, human herpes virus type 7 and Neisseria lactose |
Marshall [33] | Epithelial brushing | Pre-cancer | A 10-year follow-up study of 393 patients: with incidence (n = 59), prevalence (n = 21), and no cancer (313) | 16S V4 | NA | The abundances of Bacilli, Lactobacillales, Streptococcus and Paenibacillus are associated with incident LC |
Zeng [34] | BALF | NSCLC | LC (n = 46) vs. benign lung disease (n = 29) | 16S V3–V4 | Increased α-diversity during carcinogenesis and significant changes in β-diversity | Enrichment of phyla (Firmicutes and Bacteroidetes) and genera (Streptococcus, Prevotella and Veillonella) in NSCLC |
Chu [35] | BALF | LC | Patients under PD-1 blockade treatment: responders (n = 19) vs. non-responders (n = 27) | 16S V3–V4 | Decreased diversity upon treatment | Increased abundance of Fusobacterium is associated with poor anti-PD-1 therapy response |
Zhang [36] | Tumor | NSCLC | Patients (n = 53) | Pathogen-targeted sequencing | NA | At advanced stage: increased Serratia marcescens, Actinomyces neesii, Enterobacter cloacae and Haemophilus parainfluenzae; and decreased Staphylococcus haemolyticus and Streptococcus crista Survival prediction: Haemophilus parainfluenzae, Serratia marcescens, Acinetobacter jungii and Streptococcus constellation High PD-L1 expression: increased Acinetobacter jungii |
Huang [37] | Sputum | NSCLC | Patients (n = 85) | 16S V3–V4 | Decreased α- and β-diversity at advanced stage | Early stage: Granulicatella and Actinobacillus are enriched Advanced stage: Actinomyces is enriched |
Roy [38] | Saliva | LUAD | Patients (n = 5) and healthy control (n = 5) | 16S V3–V4 | No significant changes in α-diversity | Increased Rothia mucilaginosa, Veillonella dispar, Prevotella melaninogenica, Prevotella pallens, Prevotella copri, Haemophilus parainfluenzae, Neisseria bacilliformis and Aggregatibacter segnis in LUAD |
Dong [39] | Tumor | LC | Tumor tissues (n = 118) vs. adjacent normal tissue (n = 123) from 143 patients | 16S V3–V4 | No significant changes in α-diversity but significant differences in β-diversity | Massilia, Phenylobacterium and Pseudoxanthomonas are enriched in tumor tissue; Brevibacillus, Cupriavidus and Anaerococcus are enriched in normal tissues Massilia and Acidovorax are associated with TP53 mutation |
Jang [40] | BALF | LC | Patients under PD-1 blockade treatment (n = 84) | 16S V3–V4 | No significant changes in α-diversity and β-diversity | High-PD-L1 group: dominated by Veillonella dispar; with reduced Neisseria Responders: dominated by Veillonella dispar Non-responders: dominated by Haemophilus influenzae and Neisseria perflava |
Boesch [41] | Tumor | AdvancedNSCLC | Tumor tissues (n = 38) vs. adjacent normal tissue (n = 10) from patients with PD-1 blockade treatment | 16S V3–V4 | Increased diversity is associated with better survival | Gammaproteobacteria correlate with low PD-L1 expression and poor anti-PD-1 blockade treatment outcomes |
Lu [42] | Sputum | NSCLC | Patients (n = 87) vs. healthy controls (n = 34) | 16S V3–V4 | Decreased α-diversity in NSCLC | NSCLC: increased Haemophilus parainfluenzae and Haemophilus influenzae Distant metastasis: decreased Capnocytophaga; and increased Pseudomonas, Coriobacteriaceae and Actinomyces |
Chang [43] | Tumor | LC | Patients (n = 49) | 16S V4 | NA | Brevundimonas diminuta, Acinetobacter radioresistens Enterobacter cloacae, Mycobacterium chelonae, Mycobacterium franklinii, Staphylococcus sp., Bacillus megaterium, Pseudomonas aeruginosa and Rhodococcus erythropolis are enriched in LC and associated with poor prognosis |
Shi [44] | Mouth rinse | LC | Patients (n = 156) vs. healthy control (n = 156) | 16S V4 | No significant changes in α-diversity and β-diversity | The abundances of families Lachnospiraceae, Peptostreptococcaceae, Erysipelotrichaceae and species Parvimonas micra are associated with decreased LC risk |
Seixas [45] | BALF | LC, COPD and ILD | LC (n = 8) vs. COPD (n = 7) vs. ILD (n = 10) | 16S V4 | No significant changes in diversity between cancer and non-cancer | Streptococcus and Prevotella are associated with LC Haemophilus is associated with COPD |
Zheng [22] | BALF | NSCLC | Patients (n = 32) vs. non-cancer controls (n = 15) | 16S | Decreased diversity in NSCLC | LC: increased Lactobacillus rossiae, Burkholderia mallei and Bacteroides pyogenes; decreased Paenibacillus odorifer, Pseudomonas entomophila and Magnetospirillum gryphiswaldense |
Zhang [46] | Sputum; stool | Metastatic NSCLC | Patients (n = 75) at baseline and during immune checkpoint inhibitors treatment | 16S | α-diversity between the gut and respiratory microbiota is not related Only increased α-diversity in the gut is associated with better treatment outcomes | Streptococcus in sputum as a biomarker for good treatment response |
Dumont-Leblond [47] | Tumor | NSCLC | Tumor tissues vs. adjacent normal tissue from 29 patients | 16S V3–V4 | Higher β diversity differences among different patients than tissues from the same patient. Higher α-diversity in tumor tissues | LC has an increased abundance of pathogenic and pro-inflammatory bacteria: Escherichia-Shigella, Faecalibacterium, Pseudomonas, unclassified Enterobacteriaceae, Alloprevotella and Brevundimonas High Phascolarctobacterium in LUSC |
Ma [48] | Tumor | LUAD as SSN or SN | Tumor tissues vs. adjacent normal tissue (n = 10 pairs for SSN; n = 25 pairs for SN) | 16S V3–V4 | SSN has higher microbiome richness and diversity Tumor and normal tissues have similar diversity and richness | Increased Actinobacteria, Proteobacteria, Parvibaculales, Parvibaculaceae, Parvibaculum, Renibacterium and Ancylobacter; and decreased Firmicutes, Bacteroidetes and Lactobacillus in LUAD |
Leng [49] | Tumor; sputum | LC | Tumor tissues vs. adjacent normal tissue (n = 31 pairs); sputum from NSCLC patients (n = 17) vs. cancer-free smoker controls (n = 10) | Droplet digital PCR for 25 NSCLC-associated bacterial genera | NA | Enrichment of Acidovorax, Streptococus and Veillonella in sputum of LUSC Enrichment of Capnocytophaga in sputum of LUAD |
Druzhinin [50] | Sputum | LC | Patients (n = 66) vs. healthy controls (n = 62); all male | 16S V3–V4 | Decreased β diversity in LC patients | Increased Streptococcus, Bacillus, Gemella and Haemophilus in LC patients Chromosomal aberration frequency is positively associated with increased Bacteroides, Lachnoanaerobaculum, Porphyromonas, Mycoplasma and Fusobacterium; and decreased Granulicatella. Micronuclei frequency is negatively associated with increased Megasphaera and Selenomonas bovis |
Hosgood [51] | Oral rinse | LC | Patients (n = 114) vs. healthy controls (n = 114) | Metagenomic shotgun sequencing | Individuals with lower α-diversity had an increased risk of lung cancer No significant changes in β-diversity | Decreased risk of LC: a higher abundance of Spirochaetia and Bacteroidetes Increased risk of LC: Bacilli class and Lactobacillales order |
Tsay [52] | Lower airway brushing; buccal brushing | LC | Patients (n = 83) | 16S V4 | α-diversity is similar across different stages of NSCLC. Higher α-diversity in lower airways than in upper airways | Veillonella parvula is associated with LC progression, IL-17 expression and the activation of the immune checkpoint Increased Moraxella, Fusobacterium, Pseudomonas and Haemophilus; and decreased Actinomycetales in advanced LC Streptococcus, Prevotella and Veillonella enrichment is related to poor prognosis |
Zhuo [53] | BALF | LC | From cancerous lung and the contralateral non-cancerous lung (n = 50) | 16S V3–V4 | No significant changes in α- and β-diversity | Increased risk of LC: genera Weissella and Spiroplasma Decreased risk of LC: phylum Bacteroidetes (class Bacteroidia and order Bacteroidales) |
Kovaleva [54] | Tumor | NSCLC | Tumor tissues vs. adjacent normal tissue (n = 89) | 16S V3–V4 | Tumor tissues have similar α-diversity, but reduce overall bacterial load | High bacterial load with increased iNOS expression is a favorable prognostic factor; High bacterial load with increased FOXP3+ cells is associated with poor prognosis Increased Propionibacterium is associated with lower iNOS expression |
Cheng [55] | BALF | LC | Patients (n = 32) vs. benign pulmonary diseases (n = 22) | 16S V3–V4 | Similar richness and evenness in LC | TM7-3, Gemmiger, Capnocytophaga, Sediminibacterium, Blautia and Oscillospira are enriched in LC |
Mao [56] | Tumor | LC | Tumor tissues vs. adjacent normal tissue (n = 55) | 16S V3–V4 | Reduced α-diversity in LC; but no significant changes in β-diversity | Propionibacterium is significantly reduced in tumor tissues Other reduced genera include: unclassified Comamonadaceae, unclassified Enterobacteriaceae, Rhodobacter, Psychrobacter, Phormidium, Propionibacterium, Microbacterium and Finegoldia |
Bello [57] | Bronchial biopsy; saliva | Central LC | Patients (n = 25): saliva and biopsies of affected and contralateral bronchi vs. healthy controls (n = 16): saliva and single bronchi biopsy | 16S V3–V4 | The diversity of salivary sample is comparable in patients and controls | Streptococcus has dominated in both affected and contralateral bronchi of patients Pseudomonas is dominated in control Increased abundance of Streptococcus, Rothia, Gemella and Lactobacillus in patients’ saliva |
Druzhinin [58] | Sputum | LC | Patients (n = 17) vs. healthy control (n = 17) | 16S V3–V4 | No significant differences in α-diversity | Increased genera Haemophilus and Bergeyella; and decreased genera Atopobium, Stomatobaculum, Treponema and Porphyromonas in LC patients Chromosomal aberration frequency is negatively associated with the genus Atopobium and positively associated with the species Alloprevotella |
Wong [59] | Tumor | LC | Tumor tissues vs. adjacent normal tissue (n = 497 for LUAD and 433 for LUSC) | TCGA | NA | The LC-associated microbiome is age and gender-specific Escherichia coli str. K-12 substrain W3110 is associated with the survival of aged LUAD patients |
Reinhold [21] | Tumor; PO swab; BALF | LC | Patients undergoing surgery (n = 13) | 16S V3–V4 | Decreased α-diversity in the upper airways | High Prevotella, Veillonella and Streptococcus in the upper airways and BALF High Pseudomonas, Propionibacteria, Proteobacteria and Actinobacteria in lung cancer tissues |
Bingula [60] | Saliva; BAL (from excised lobe); tumor | NSCLC | saliva, BAL, peritumoral tissues, tumor tissues and adjacent normal tissue from 18 patients | 16S V3–V4 | Unique β-diversity of BAL Diversity varies depending on lobe location | Tissue samples: dominated by Phylum Proteobacteria BAL: dominated by class Clostridia Saliva: dominated by class Bacilli |
Patnaik [61] | Saliva; BALF; tumor | Early recurrentNSCLC | Pre-surgery saliva and BALF; tumor tissues and adjacent normal tissue from 48 patients undergoing surgery | 16S | Higher diversity in saliva and BALF; Tumor tissues and adjacent normal tissue have similar diversity | Recurrence is associated with increased genus Delftia and decreased Bifidobacterium in saliva; as well as increased Staphylococcus and decreased Bacillus and Anaerobacillus in tumor tissues |
Ekanayake [62] | BALF; PO swab | LC and BRS | Patients (n = 20 for LC and n = 20 for BRS) vs. healthy controls (n = 20) | 16S V3–V4 | Increased diversity in patients | Enterococcus faecalis, Corynebacterium tuberculostearicum and Keratinibaculum paraultunense are LC-specific |
Huang [63] | Bronchial washing fluid; sputum | LC | Bronchial washing fluid (n = 40) and sputum (n = 52) from LC patients | 16S V3–V4 | No significant difference in α- and β- diversity between LUAD and LUSC | All from Bronchial washing fluid samples: Genera Veillonell, Megasphaera, Actinomyces and Arthrobacter are enriched in LUAD without metastasis Genera Capnocytophaga and Rothia are enriched in LUSC with metastasis Streptococcus is decreased in LUAD upon metastasis Veillonella and Rothia are increased in LUSC upon metastasis |
Jin [64] | BALF | LC | Patients (n = 91) vs. nonmalignant pulmonary diseases (n = 29) vs. healthy controls (n = 30); a validation cohort of 85 patients | Metagenomics | Diversity and richness are reduced in LC patients β-diversity is different between LC patients and healthy controls | Haemophilus influenzae shows the greatest difference between LC patients and healthy controls |
Gomes [65] | BALF | LC | Patients (n = 49) vs. healthy controls (n = 54) | 16S V3-V6 | LUSC has a higher diversity than LUAD | Biomarkers for LUAD: Acinetobacter, Propionibacterium, Phenylobacterium, Brevundimonas and Staphylococcus Biomarkers for LUSC: Enterobacter, Serratia, Klebsiella, Kluyvera, Morganella, Achromobacter and Capnocytophaga |
Ren [66] | Tumor | LUAD as GGN | Tumor tissues (n = 10) vs. adjacent normal tissue (n = 5) | Whole genome sequencing | High β diversity variation among patients | No significant differences in microbiome compositions between GGNs and normal tissues (except LUAD) |
Zhang [67] | Saliva | NSCLC | Patients (n = 39) vs. healthy controls (n = 20) | 16S V1-V2 | A higher richness and lower diversity in NSCLC patients | In NSCLC: increased Veillonella, Streptococcus, Lautropia, Leptotrichia, Rothia and Aggregatibacter; and decreased Prevotella_7, Fusobacterium, Porphyromonas, Alloprevotella, Prevotella, Bacteroides and Faecalibacterium Veillonella is positively associated with the Neutrophil-lymphocyte ratio Streptococcus is negatively associated with the lymphocyte-monocyte ratio |
Wang [68] | Saliva; BALF | PBC | Patients (n = 51) vs. healthy controls (n = 15) | 16S V4 | Patients have lower diversity in both saliva and BALF samples | Treponema (in saliva) and Filifactor (in both saliva and BALF) are potential biomarkers for LC |
Hosgood [69] | Sputum | LC | Patients (n = 45) vs. healthy controls (n = 45) | 16S V1-V2 | Lower α-diversity is associated with an increased risk of LC | Decreased relative abundance of Fusobacteria is a risk factor for LC |
Peters [70] | Tumor | NSCLC | Tumor tissues vs. remote normal tissue (n = 19 pairs) | 16S V4 | Tumor tissues have reduced richness and diversity | Increased Koribacteraceae; and decreased Bacteroidaceae, Lachnospiraceae and Ruminococcaceae in normal tissues are associated with a better survival outcome |
Yang [71] | Saliva | LC | Patients (n = 75) vs. healthy controls (n = 172); all female | 16S V1-V2 | Tumor tissues have reduced richness and diversity | Increased Sphingomonas and Blastomonas in LC patients |
Liu [72] | Tumor | LC | LC-only (n = 11) vs. emphysema-only (n = 10) vs. both LC and emphysema (n = 19); all heavy smokers | 16S V4 | The emphysema-only group has a lower diversity | LC vs. emphysema-only: decreased Proteobacteria (primarily the genera Acinetobacter and Acidovorax); and increased Firmicutes (Streptococcus) and Bacteroidetes (Prevotella) |
Greathouse [73] | Tumor | LC | Patients (n = 143) vs. healthy controls (n = 33) TCGA was used as a validation cohort | 16S V3-V5 | Control tissues have lower α-diversity | Acidovorax, Klebsiella, Rhodoferax and Anaerococcus are enriched in LUSC only |
Tsay [74] | Lower airway brushing; buccal brushing | LC | Patients (n = 39) vs. non-cancer patients (n = 36) vs. healthy controls (n = 10) | 16S V4 | No differences (α- and β-diversity) in buccal samples Significant changes in β-diversity in Lower airway samples between LC and non-cancer/healthy controls | Streptococcus and Veillonella are highly enriched in the lower airways of LC patients and are associated with ERK and PI3K signaling pathway activation |
Liu [75] | Bronchial specimen brushing | LC | Diseased lung and paired contralateral healthy lung (n = 24 pairs) vs. healthy controls (n = 8) | 16S V3–V4 | α-diversity reduces from healthy site to noncancerous to cancerous site | Genera Streptococcus and Neisseria are significantly more abundant in LC Genera Staphylococcus and Dialister are significantly more abundant in healthy controls |
Cameron [76] | Sputum | LC | Patients (n = 4) vs. non-cancer controls (n = 6) | 16S | No significant changes in α-diversity | Streptococcus viridans and Granulicatella adiacens are significantly increased in LC patients |
Lee [77] | BALF | LC | Patients (n = 20) vs. benign diseases (n = 8) | 16S V1-V3 | Increased diversity in LC | Phyla Firmicutes and TM7 are significantly increased in LC patients |
Yu [23] | Tumor | LC | Tumor tissues (n = 31) vs. remote normal tissue (n = 165) | 16S V3–V4 | α-diversity is increased with environmental exposures, residence population, smoking and disease history LC has reduced diversity | Biomarkers for advanced LC: Genus Thermus Biomarkers for LC metastasis: Genus Legionella |
Yan [78] | Saliva | LC | Patients (n = 10 for LUAD and n = 10 for LUSC) vs. healthy controls (n = 10) | 16S V3 and V6 | NA | Capnocytophaga and Veillonella are promising biomarkers for LUSC The abundance of Capnocytophaga, Selenomonas, Veillonella and Neisseria in saliva is significantly changed in LC patients |
Hosgood [79] | Sputum; oral rinse | LC | Patients (n = 8) vs. healthy controls (n = 8) | 16S V1-V2 | The diversity between LC and control is similar in buccal samples, but significantly different in sputum | Granulicatella, Abiotrophia and Streptococcus are enriched in the sputum of LC patients |
2.2. Potential Reasons for the Few Commonalities across Studies
3. Airway or Respiratory Tract Microbiome and Lung Cancers
4. Frequently Altered Bacterial Genera in Lung Cancer Patients
4.1. Veillonella
4.2. Prevotella
4.3. Streptococcus
4.4. Acidovorax
4.5. Haemophilus
4.6. Capnocytophaga
4.7. Other Commonly Identified Lung Cancer-Associated Microbes
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
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Huang, J.; Huang, J. Microbial Biomarkers for Lung Cancer: Current Understandings and Limitations. J. Clin. Med. 2022, 11, 7298. https://doi.org/10.3390/jcm11247298
Huang J, Huang J. Microbial Biomarkers for Lung Cancer: Current Understandings and Limitations. Journal of Clinical Medicine. 2022; 11(24):7298. https://doi.org/10.3390/jcm11247298
Chicago/Turabian StyleHuang, Jiawen, and Juan Huang. 2022. "Microbial Biomarkers for Lung Cancer: Current Understandings and Limitations" Journal of Clinical Medicine 11, no. 24: 7298. https://doi.org/10.3390/jcm11247298