Hanna Group

Contact

Group Lead
Professor George Hanna
g.hanna@imperial.ac.uk

Our aim is to develop a single breath test to diagnose five major gastrointestinal cancers; oesophageal, gastric, pancreatic, liver and colorectal.

The problem to address

Unmet need

Late diagnosis is a common feature of major gastrointestinal cancers. Early stages are commonly associated with non-specific symptoms, often similar to benign conditions. The National Institute for Health and Care Excellence (NICE) referral guidelines are age-dependent and mainly include red-flag symptoms, resulting in cancer diagnosis at an advanced stage. Currently, the cancer yield of urgent and non-urgent referral pathways is 4.4-5% and 0.1-1.7% respectively.

Burden of gastrointestinal cancers

In the UK, 75,277 patients are diagnosed and 44,455 die annually. Diagnosing cancer at an advanced stage permits fewer curative treatment options, reducing chance of cure. Overall, 5-year survival for oesophageal, gastric, pancreatic, liver and colorectal cancer is poor (15.9%, 20.7%, 9.0%, 12.6% and 50.7% respectively) and largely stage-dependent.

Proposed solution

Low cancer yields from gastrointestinal investigations results from the lack of an intermediate tests to streamline referrals, apart from faecal immunochemical test for colorectal cancer. Breath test is our proposed solution as a triage test to direct patients with non-specific symptoms to have specialised investigations.

Overview of our work

The Hanna Group laboratory

State-of-the-art dedicated laboratory suite for breath analysis in clinical studies (Imperial College London, ICL) with non-VOC emitting infrastructure and positive pressure ventilation, encompassing four laboratories dedicated to different stages of workflow and including cell culture and tissue processing facilities for mechanistic studies underpinning VOC production.

VOC methodology

We established a reliable platform for high-throughput breath analysis with excellent VOC detection limits, quantification, reproducibility and analytical recovery. We have a validated analytical method for TD-GC-TOF-MS that adheres to European Medicines Agency guidance with VOC quantification limit at 1.25ng/L. We have developed quality assurance and control procedures to provide a high level of confidence in the complete workflow from breath sampling to data generation using a bespoke Laboratory Information Management System for logging all recorded data with full traceability. The Hanna laboratory plans to gain ISO-17025 accreditation in 2024.

VOC data Artificial Intelligence (AI) analytical pipeline

We developed an AI platform, MSHub, to process and analyse GC-MS data from breath samples using molecular network analysis to identify VOC biomarkers that separate cancer from control and other cancer types. It enables analysis of an unlimited data volume in a reproducible way since the algorithm was designed to function without user involvement. MSHub operates using out-of-core processing, with no processing limit beyond data storage capacity, allowing rollout to sites where high-performance computing is unavailable.

Mechanisms of VOC production

We showed in an experimental human model that the origin of certain VOCs within exhaled breath is derived principally from the lungs, suggesting that VOCs travel in the systemic circulation. We confirmed the endogenous origin of VOCs from cancer and its associated environment.

Biomarker discovery and clinical studies

  • Oesophageal and gastric cancers: We developed a cancer detection model with internal validation (n=210 patients), using SIFT-MS with an area under the receiver operator characteristic (AU-ROC) curve of 0.92. The biomarker panel was externally validated in a multicentre study (n=335, AU-ROC=0.85). We expanded the biomarker panel using TD-GC-MS for analytical validation (n=300, AU-ROC= 0.90).
  • Colorectal cancer: COBRA study (n=1432) identified biomarkers for colorectal cancer, achieving AU-ROC=0.91 in symptomatic patients and AU-ROC=0.87 when including asymptomatic population.
  • Pancreatic cancer: We identified biomarkers for pancreatic ductal adenocarcinoma (n=132, AU-ROC=0.90).
  • Liver cancer: VOCAL study identified biomarkers for hepatocellular carcinoma (n= 154, AU-ROC=0.94)

Human factors studies

We demonstrated breath testing at public events and conducted simulation studies and human factors experiments on different breath collection devices to examine usability and contamination levels. Stakeholders’ engagement concluded that best position for breath testing is a triage tool in primary care.

Health economic modelling

Economic modelling projected that a breath test-assisted referral pathway for suspected oesophagogastric cancer would cost the NHS £138M compared to £293M for the current referral pathway with an annual saving of £155M.

Breath testing in the clinical environment

We demonstrated breath testing acceptability in primary care (MAGIC, n=1002) and large-scale multicentre studies (COBRA, n=1432), exceeding recruitment targets. 99% of patients consider breath test is easy/ very easy to do.

Intellectual Property

Biomarkers are protected and owned by ICL. The Hanna Group are inventors of seven patents filed worldwide.

Current translational research

Tumour

Regional hypoxia (low oxygen) and acidosis is a feature of all solid tumours, and is a consequence of rapid cellular proliferation and an inadequate blood supply. As a result, tumour cells undergo profound metabolic reprogramming to adapt to hypoxic, acidic and nutrient-deprived conditions. We speculate that these harsh conditions that are unique to the tumour microenvironment may play a role in the production of cancer-associated VOCs. Using a systems biology approach, we are investigating the influence of these factors on VOC production using cell & patient-derived organoid models. Experiments include pathway-directed genetic perturbation, functional assays to evaluate aggressive tumour biology. New clinical studies will also use state-of-the-art spatial-omic techniques and machine learning to bridge the gap between tumour metabolism and exhaled VOCs.

Microbiome

The human microbiome plays a significant role in homeostasis, immunomodulation and pathogenesis.  The dynamic and intricate relationship between bacteria and fungi within the tumour microenvironment is critical in understanding factors influencing cancer development and progression. As a result, valuable predictive information can be gathered on diagnoses, prognostication and treatment strategies. We hypothesise there is a strong symbiotic or antagonist relationship between the cancer microbes which influences clinical outcomes. Our work will use high through-put next generation sequencing platforms to define the microbiome of oesophagogastric cancer, explore their functional capabilities and comprehensive network analyses to establish drivers of disease. Evaluating the underlying mechanistic pathways responsible for cancer metabolite production will further elucidate the origin of cancer-specific volatile organic compounds.

Immune

Tissue immune surveillance and infiltration impacts prognosis and therapy response in solid cancers. To better understand the influence of the host immune response on VOC generation and carcinogenesis in gastrointestinal cancers, we utilise high-dimensional techniques including spectral flow cytometry, imaging mass cytometry, and confocal microscopy, which allows us to comprehensively characterize heterogeneous immune cell populations at a single-cell level. This knowledge guides the design of bespoke tri-culture models incorporating patient-derived immune cells, organoids and fibroblasts to more accurately mimic the tumour microenvironment. By integrating immune cells into our VOC models, we can precisely replicate in vivo immune-tumour interactions, thereby enhancing our understanding of how various components of the tumour microenvironment contribute to VOC production. Furthermore, by combining microbial analysis and the use of fluorescence in situ hybridisation, we can investigate the microbial-immune interactions which may be responsible for initiating the spread of cancer and identify profiles associated with treatment response.

Additional information

Team

Group Leader

  • Prof. George Hanna

Staff

  • Aaron Parker - Laboratory manager & senior analytical scientist
  • Ayushi Pabari - Clinical trial manager (AROMA)
  • Emma Austin - Clinical trial manager (VAPOR)
  • Jessie McClymont - Junior analytical technician
  • Jim Ellis - Stable isotope specialist & senior analytical scientist
  • Valerio Converso - Senior analytical scientist

Postdoctoral researchers

  • Bibek Das - MRC clinical research training fellow
  • Ilaria Belluomo - Research associate
  • Sara Jamel - Research associate
  • Bhamini Vadhwana - Rosetrees and BASO research associate

PhD students

  • Anuja T Mitra - MRC clinical research training fellow
  • Boyu Xie - Research postgraduate
  • Caoimhe M Walsh - Clinical research fellow
  • Guillaume B R C Lafaurie - Clinical research fellow
  • Henry D P Robb - Clinical research fellow
  • Katja Christodoulou - Guts UK doctorate research Fellow
  • Michael Fadel - NIHR doctoral fellow
  • Munir N Tarazi - Clinical research fellow
  • Pallavi Arya - Clinical research fellow
  • Philip Leung - Research postgraduate & outreach STEM fellow
  • Sameera Sharma - NIHR doctoral fellow
  • Shizhou Li - China scholarship council fellow

Collaborators

Internal
External
  • Professor Linda Sharples (London School of Hygiene & Tropical Medicine)
  • Professor Patrik Spanel (J. Heyrovský Institute of Physical Chemistry)
  • Professor Lesley Hoyles (University of Nottingham)

Clinical trials

ICL is conducting large scale clinical trials in oesophageal, gastric, pancreatic, liver and colorectal; cancers (about 30,000 patients over next 3-4 years):

Publications

  1. Belluomo I, Whitlock SE, Myridakis A, Parker AG, Converso V, Perkins MJ, Langford VS, Španěl P, Hanna GB. Combining Thermal Desorption with Selected Ion Flow Tube Mass Spectrometry for Analyses of Breath Volatile Organic Compounds. Anal Chem. 2024 Jan 30;96(4):1397-1401. doi: 10.1021/acs.analchem.3c04286. PMID: 38243802.
  2. Myridakis A, Wen Q, Boshier PR, Parker AG, Belluomo I, Handakas E, Hanna GB. Global Urinary Volatolomics with (GC×)GC-TOF-MS. Anal Chem. 2023 Nov 28;95(47):17170-17176. doi: 10.1021/acs.analchem.3c02523. PMID: 37967208.
  3. Wen Q, Myridakis A, Boshier PR, Zuffa S, Belluomo I, Parker AG, Chin ST, Hakim S, Markar SR, Hanna GB. A Complete Pipeline for Untargeted Urinary Volatolomic Profiling with Sorptive Extraction and Dual Polar and Nonpolar Column Methodologies Coupled with Gas Chromatography Time-of-Flight Mass Spectrometry. Anal Chem. 2023 Jan 17;95(2):758-765. doi: 10.1021/acs.analchem.2c02873. PMID: 36602225.
  4. Woodfield G, Belluomo I, Laponogov I, Veselkov K; COBRA1 WORKING GROUP; Cross AJ, Hanna GB. Diagnostic Performance of a Noninvasive Breath Test for Colorectal Cancer: COBRA1 Study. Gastroenterology. 2022 Nov;163(5):1447-1449.e8. doi: 10.1053/j.gastro.2022.06.084. PMID: 35803311.
  5. Belluomo I, Boshier PR, Myridakis A, Vadhwana B, Markar SR, Spanel P, Hanna GB. Selected ion flow tube mass spectrometry for targeted analysis of volatile organic compounds in human breath. Nat Protoc. 2021 Jul;16(7):3419-3438. doi: 10.1038/s41596-021-00542-0. PMID: 34089020.
  6. Antonowicz S, Bodai Z, Wiggins T, Markar SR, Boshier PR, Goh YM, Adam ME, Lu H, Kudo H, Rosini F, Goldin R, Moralli D, Green CM, Peters CJ, Habib N, Gabra H, Fitzgerald RC, Takats Z, Hanna GB. Endogenous aldehyde accumulation generates genotoxicity and exhaled biomarkers in esophageal adenocarcinoma. Nat Commun. 2021 Mar 5;12(1):1454. doi: 10.1038/s41467-021-21800-5. PMID: 33674602.
  7. Aksenov AA, Laponogov I, Zhang Z, Doran SLF, Belluomo I, Veselkov D, Bittremieux W, Nothias LF, Nothias-Esposito M, Maloney KN, Misra BB, Melnik AV, Smirnov A, Du X, Jones KL 2nd, Dorrestein K, Panitchpakdi M, Ernst M, van der Hooft JJJ, Gonzalez M, Carazzone C, Amézquita A, Callewaert C, Morton JT, Quinn RA, Bouslimani A, Orio AA, Petras D, Smania AM, Couvillion SP, Burnet MC, Nicora CD, Zink E, Metz TO, Artaev V, Humston-Fulmer E, Gregor R, Meijler MM, Mizrahi I, Eyal S, Anderson B, Dutton R, Lugan R, Boulch PL, Guitton Y, Prevost S, Poirier A, Dervilly G, Le Bizec B, Fait A, Persi NS, Song C, Gashu K, Coras R, Guma M, Manasson J, Scher JU, Barupal DK, Alseekh S, Fernie AR, Mirnezami R, Vasiliou V, Schmid R, Borisov RS, Kulikova LN, Knight R, Wang M, Hanna GB, Dorrestein PC, Veselkov K. Auto-deconvolution and molecular networking of gas chromatography-mass spectrometry data. Nat Biotechnol. 2021 Feb;39(2):169-173. doi: 10.1038/s41587-020-0700-3. PMID: 33169034.
  8. Kamal F, Kumar S, Edwards MR, Veselkov K, Belluomo I, Kebadze T, Romano A, Trujillo-Torralbo MB, Shahridan Faiez T, Walton R, Ritchie AI, Wiseman DJ, Laponogov I, Donaldson G, Wedzicha JA, Johnston SL, Singanayagam A, Hanna GB. Virus-induced Volatile Organic Compounds Are Detectable in Exhaled Breath during Pulmonary Infection. Am J Respir Crit Care Med. 2021 Nov 1;204(9):1075-1085. doi: 10.1164/rccm.202103-0660OC. PMID: 34319857.
  9. Lin GP, Vadhwana B, Belluomo I, Boshier PR, Španěl P, Hanna GB. Cross Platform Analysis of Volatile Organic Compounds Using Selected Ion Flow Tube and Proton-Transfer-Reaction Mass Spectrometry. J Am Soc Mass Spectrom. 2021 May 5;32(5):1215-1223. doi: 10.1021/jasms.1c00027. PMID: 33831301.
  10. Woodfield G, Belluomo I, Boshier PR, Waller A, Fayyad M, von Wagner C, Cross AJ, Hanna GB. Feasibility and acceptability of breath research in primary care: a prospective, cross-sectional, observational study. BMJ Open. 2021 Apr 13;11(4):e044691. doi: 10.1136/bmjopen-2020-044691. PMID: 33849851.
  11. Hanna GB, Cross AJ. Editorial: volatile organic compound analysis to improve faecal immunochemical testing in the detection of colorectal cancer. Aliment Pharmacol Ther. 2021 Aug;54(4):504-505. doi: 10.1111/apt.16471. PMID: 34331792.
  12. Wen Q, Boshier P, Myridakis A, Belluomo I, Hanna GB. Urinary Volatile Organic Compound Analysis for the Diagnosis of Cancer: A Systematic Literature Review and Quality Assessment. Metabolites. 2020 Dec 29;11(1):17. doi: 10.3390/metabo11010017. PMID: 33383923.
  13. Goh YM, Antonowicz SS, Boshier P, Hanna GB. Metabolic Biomarkers of Squamous Cell Carcinoma of the Aerodigestive Tract: A Systematic Review and Quality Assessment. Oxid Med Cell Longev. 2020 Feb 21;2020:2930347. doi: 10.1155/2020/2930347. PMID: 32685090.
  14. Abbassi-Ghadi N, Antonowicz SS, McKenzie JS, Kumar S, Huang J, Jones EA, Strittmatter N, Petts G, Kudo H, Court S, Hoare JM, Veselkov K, Goldin R, Takáts Z, Hanna GB. De Novo Lipogenesis Alters the Phospholipidome of Esophageal Adenocarcinoma. Cancer Res. 2020 Jul 1;80(13):2764-2774. doi: 10.1158/0008-5472.CAN-19-4035. Epub 2020 Apr 28. PMID: 32345674.
  15. Vadhwana B, Belluomo I, Boshier PR, Pavlou C, Španěl P, Hanna GB. Impact of oral cleansing strategies on exhaled volatile organic compound levels. Rapid Commun Mass Spectrom. 2020 May 15;34(9):e8706. doi: 10.1002/rcm.8706. PMID: 31880852.
  16. Markar SR, Chin ST, Romano A, Wiggins T, Antonowicz S, Paraskeva P, Ziprin P, Darzi A, Hanna GB. Breath Volatile Organic Compound Profiling of Colorectal Cancer Using Selected Ion Flow-tube Mass Spectrometry. Ann Surg. 2019 May;269(5):903-910. doi: 10.1097/SLA.0000000000002539. PMID: 29194085.
  17. Hanna GB, Boshier PR, Markar SR, Romano A. Accuracy and Methodologic Challenges of Volatile Organic Compound-Based Exhaled Breath Tests for Cancer Diagnosis: A Systematic Review and Meta-analysis. JAMA Oncol. 2019 Jan 1;5(1):e182815. doi: 10.1001/jamaoncol.2018.2815. Epub 2019 Jan 10. Erratum in: JAMA Oncol. 2019 Jul 1;5(7):1070. PMID: 30128487.
  18. Adam ME, Fehervari M, Boshier PR, Chin ST, Lin GP, Romano A, Kumar S, Hanna GB. Mass-Spectrometry Analysis of Mixed-Breath, Isolated-Bronchial-Breath, and Gastric-Endoluminal-Air Volatile Fatty Acids in Esophagogastric Cancer. Anal Chem. 2019 Mar 5;91(5):3740-3746. doi: 10.1021/acs.analchem.9b00148. PMID: 30699297.
  19. Romano A, Hanna GB. Identification and quantification of VOCs by proton transfer reaction time of flight mass spectrometry: An experimental workflow for the optimization of specificity, sensitivity, and accuracy. J Mass Spectrom. 2018 Apr;53(4):287-295. doi: 10.1002/jms.4063. PMID: 29336521.
  20. Romano A, Doran S, Belluomo I, Hanna GB. High-Throughput Breath Volatile Organic Compound Analysis Using Thermal Desorption Proton Transfer Reaction Time-of-Flight Mass Spectrometry. Anal Chem. 2018 Sep 4;90(17):10204-10210. doi: 10.1021/acs.analchem.8b01045. PMID: 30106567.
  21. Markar SR, Wiggins T, Antonowicz S, Chin ST, Romano A, Nikolic K, Evans B, Cunningham D, Mughal M, Lagergren J, Hanna GB. Assessment of a Noninvasive Exhaled Breath Test for the Diagnosis of Oesophagogastric Cancer. JAMA Oncol. 2018 Jul 1;4(7):970-976. doi: 10.1001/jamaoncol.2018.0991. PMID: 29799976.
  22. Markar SR, Brodie B, Chin ST, Romano A, Spalding D, Hanna GB. Profile of exhaled-breath volatile organic compounds to diagnose pancreatic cancer. Br J Surg. 2018 Oct;105(11):1493-1500. doi: 10.1002/bjs.10909. PMID: 30019405.
  23. Boshier PR, Fehervari M, Markar SR, Purkayastha S, Spanel P, Smith D, Hanna GB. Variation in Exhaled Acetone and Other Ketones in Patients Undergoing Bariatric Surgery: a Prospective Cross-sectional Study. Obes Surg. 2018 Aug;28(8):2439-2446. doi: 10.1007/s11695-018-3180-5. PMID: 29516396.
  24. Antonowicz S, Hanna GB, Takats Z, Bodai Z. Pragmatic and rapid analysis of carbonyl, oxidation and chlorination nucleoside-adducts in murine tissue by UPLC-ESI-MS/MS. Talanta. 2018 Dec 1;190:436-442. doi: 10.1016/j.talanta.2018.08.029. PMID: 30172530.
  25. Doran SLF, Romano A, Hanna GB. Optimisation of sampling parameters for standardised exhaled breath sampling. J Breath Res. 2017 Dec 6;12(1):016007. doi: 10.1088/1752-7163/aa8a46. PMID: 29211685.
  26. Boshier PR, Knaggs AL, Hanna GB, Marczin N. Perioperative changes in exhaled nitric oxide during oesophagectomy. J Breath Res. 2017 Nov 7;11(4):047109. doi: 10.1088/1752-7163/aa9387. PMID: 29033395.
  27. Pabary R, Huang J, Kumar S, Alton EW, Bush A, Hanna GB, Davies JC. Does mass spectrometric breath analysis detect Pseudomonas aeruginosa in cystic fibrosis? Eur Respir J. 2016 Mar;47(3):994-7. doi: 10.1183/13993003.00944-2015. PMID: 26846826.
  28. Huddy JR, Weldon SM, Ralhan S, Painter T, Hanna GB, Kneebone R, Bello F. Sequential simulation (SqS) of clinical pathways: a tool for public and patient engagement in point-of-care diagnostics. BMJ Open. 2016 Sep 13;6(9):e011043. doi: 10.1136/bmjopen-2016-011043. PMID: 27625053.
  29. Antonowicz S, Kumar S, Wiggins T, Markar SR, Hanna GB. Diagnostic Metabolomic Blood Tests for Endoluminal Gastrointestinal Cancer–A Systematic Review and Assessment of Quality. Cancer Epidemiol Biomarkers Prev. 2016 Jan;25(1):6-15. doi: 10.1158/1055-9965.EPI-15-0524. PMID: 26598534.
  30. Abbassi-Ghadi N, Jones EA, Gomez-Romero M, Golf O, Kumar S, Huang J, Kudo H, Goldin RD, Hanna GB, Takats Z. A Comparison of DESI-MS and LC-MS for the Lipidomic Profiling of Human Cancer Tissue. J Am Soc Mass Spectrom. 2016 Feb;27(2):255-64. doi: 10.1007/s13361-015-1278-8. PMID: 26466600.
  31. Abbassi-Ghadi N, Golf O, Kumar S, Antonowicz S, McKenzie JS, Huang J, Strittmatter N, Kudo H, Jones EA, Veselkov K, Goldin R, Takats Z, Hanna GB. Imaging of Esophageal Lymph Node Metastases by Desorption Electrospray Ionization Mass Spectrometry. Cancer Res. 2016 Oct 1;76(19):5647-5656. doi: 10.1158/0008-5472.CAN-16-0699. PMID: 27364550.
  32. Wiggins T, Kumar S, Markar SR, Antonowicz S, Hanna GB. Tyrosine, phenylalanine, and tryptophan in gastroesophageal malignancy: a systematic review. Cancer Epidemiol Biomarkers Prev. 2015 Jan;24(1):32-8. doi: 10.1158/1055-9965.EPI-14-0980. PMID: 25344892.
  33. Markar SR, Wiggins T, Kumar S, Hanna GB. Exhaled breath analysis for the diagnosis and assessment of endoluminal gastrointestinal diseases. J Clin Gastroenterol. 2015 Jan;49(1):1-8. doi: 10.1097/MCG.0000000000000247. PMID: 25319742.
  34. Kumar S, Huang J, Abbassi-Ghadi N, Mackenzie HA, Veselkov KA, Hoare JM, Lovat LB, Španěl P, Smith D, Hanna GB. Mass Spectrometric Analysis of Exhaled Breath for the Identification of Volatile Organic Compound Biomarkers in Esophageal and Gastric Adenocarcinoma. Ann Surg. 2015 Dec;262(6):981-90. doi: 10.1097/SLA.0000000000001101. PMID: 25575255.
  35. Hicks LC, Huang J, Kumar S, Powles ST, Orchard TR, Hanna GB, Williams HR. Analysis of Exhaled Breath Volatile Organic Compounds in Inflammatory Bowel Disease: A Pilot Study. J Crohns Colitis. 2015 Sep;9(9):731-7. doi: 10.1093/ecco-jcc/jjv102. PMID: 26071410.
  36. Chadwick G, Groene O, Riley S, Hardwick R, Crosby T, Hoare J, Hanna GB, Greenaway K, Cromwell DA. Gastric Cancers Missed During Endoscopy in England. Clin Gastroenterol Hepatol. 2015 Jul;13(7):1264-1270.e1. doi: 10.1016/j.cgh.2015.01.025. PMID: 25645877.
  37. Boshier PR, Mistry V, Cushnir JR, Kon OM, Elkin SL, Curtis S, Marczin N, Hanna GB. Breath metabolite response to major upper gastrointestinal surgery. J Surg Res. 2015 Feb;193(2):704-12. doi: 10.1016/j.jss.2014.09.004. PMID: 25282400.
  38. Huang J, Kumar S, Hanna GB. Investigation of C3-C10 aldehydes in the exhaled breath of healthy subjects using selected ion flow tube-mass spectrometry (SIFT-MS). J Breath Res. 2014 Sep;8(3):037104. doi: 10.1088/1752-7155/8/3/037104. PMID: 25190002.
  39. Chadwick G, Groene O, Hoare J, Hardwick RH, Riley S, Crosby TD, Hanna GB, Cromwell DA. A population-based, retrospective, cohort study of esophageal cancer missed at endoscopy. Endoscopy. 2014 Jul;46(7):553-60. doi: 10.1055/s-0034-1365646. Epub 2014 Jun 27. PMID: 24971624.
  40. Abbassi-Ghadi N, Veselkov K, Kumar S, Huang J, Jones E, Strittmatter N, Kudo H, Goldin R, Takáts Z, Hanna GB. Discrimination of lymph node metastases using desorption electrospray ionisation-mass spectrometry imaging. Chem Commun (Camb). 2014 Apr 11;50(28):3661-4. doi: 10.1039/c3cc48927b. PMID: 24407514.
  41. Kumar S, Huang J, Abbassi-Ghadi N, Španěl P, Smith D, Hanna GB. Selected ion flow tube mass spectrometry analysis of exhaled breath for volatile organic compound profiling of esophago-gastric cancer. Anal Chem. 2013 Jun 18;85(12):6121-8. doi: 10.1021/ac4010309. PMID: 23659180.
  42. Huang J, Kumar S, Abbassi-Ghadi N, Spaněl P, Smith D, Hanna GB. Selected ion flow tube mass spectrometry analysis of volatile metabolites in urine headspace for the profiling of gastro-esophageal cancer. Anal Chem. 2013 Mar 19;85(6):3409-16. doi: 10.1021/ac4000656. PMID: 23421902.
  43. Boshier PR, Hanna GB, Marczin N. Exhaled nitric oxide as biomarker of acute lung injury: an unfulfilled promise? J Breath Res. 2013 Mar;7(1):017118. doi: 10.1088/1752-7155/7/1/017118. PMID: 23445570.
  44. Abbassi-Ghadi N, Kumar S, Huang J, Goldin R, Takats Z, Hanna GB. Metabolomic profiling of oesophago-gastric cancer: a systematic review. Eur J Cancer. 2013 Nov;49(17):3625-37. doi: 10.1016/j.ejca.2013.07.004. PMID: 23896378.
  45. Kumar S, Huang J, Cushnir JR, Španěl P, Smith D, Hanna GB. Selected ion flow tube-MS analysis of headspace vapor from gastric content for the diagnosis of gastro-esophageal cancer. Anal Chem. 2012 Nov 6;84(21):9550-7. doi: 10.1021/ac302409a. PMID: 23035898.
  46. Boshier PR, Priest OH, Hanna GB, Marczin N. Influence of respiratory variables on the on-line detection of exhaled trace gases by PTR-MS. Thorax. 2011 Oct;66(10):919-20. doi: 10.1136/thx.2011.161208. PMID: 21474496.
  47. Boshier PR, Cushnir JR, Mistry V, Knaggs A, Španěl P, Smith D, Hanna GB. On-line, real time monitoring of exhaled trace gases by SIFT-MS in the perioperative setting: a feasibility study. Analyst. 2011 Aug 21;136(16):3233-7. doi: 10.1039/c1an15356k. PMID: 21717028.
  48. Yakoub D, Keun HC, Goldin R, Hanna GB. Metabolic profiling detects field effects in nondysplastic tissue from esophageal cancer patients. Cancer Res. 2010 Nov 15;70(22):9129-36. doi: 10.1158/0008-5472.CAN-10-1566. PMID: 20884633.
  49. Boshier PR, Marczin N, Hanna GB. Repeatability of the measurement of exhaled volatile metabolites using selected ion flow tube mass spectrometry. J Am Soc Mass Spectrom. 2010 Jun;21(6):1070-4. doi: 10.1016/j.jasms.2010.02.008. PMID: 20335048.
  50. Boshier PR, Cushnir JR, Priest OH, Marczin N, Hanna GB. Variation in the levels of volatile trace gases within three hospital environments: implications for clinical breath testing. J Breath Res. 2010 Sep;4(3):031001. doi: 10.1088/1752-7155/4/3/031001. PMID: 21383476.

Funders