Skip to main content

In vitro detection of common rhinosinusitis bacteria by the eNose utilising differential mobility spectrometry

Abstract

Acute rhinosinusitis (ARS) is a sudden, symptomatic inflammation of the nasal and paranasal mucosa. It is usually caused by respiratory virus infection, but bacteria complicate for a small number of ARS patients. The differential diagnostics between viral and bacterial pathogens is difficult and currently no rapid methodology exists, so antibiotics are overprescribed. The electronic nose (eNose) has shown the ability to detect diseases from gas mixtures. Differential mobility spectrometry (DMS) is a next-generation device that can separate ions based on their different mobility in high and low electric fields. Five common rhinosinusitis bacteria (Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, Staphylococcus aureus, and Pseudomonas aeruginosa) were analysed in vitro with DMS. Classification was done using linear discriminant analysis (LDA) and k-nearest neighbour (KNN). The results were validated using leave-one-out cross-validation and separate train and test sets. With the latter, 77% of the bacteria were classified correctly with LDA. The comparative figure with KNN was 79%. In one train-test set, P. aeruginosa was excluded and the four most common ARS bacteria were analysed with LDA and KNN; the correct classification rate was 83 and 85%, respectively. DMS has shown its potential in detecting rhinosinusitis bacteria in vitro. The applicability of DMS needs to be studied with rhinosinusitis patients.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Dingle J, Badger G, Jordan WJ (1964) Illness in the home: a study of 25,000 illness in a group of Cleveland families. The Press of Western Reserve University, Cleveland

    Google Scholar 

  2. Berg O, Carenfelt C, Rystedt G, Änggård A (1986) Occurrence of asymptomatic sinusitis in common cold and other acute ENT-infections. Rhinology 24:223–225

    PubMed  CAS  Google Scholar 

  3. Smith SS, Ference EH, Evans CT, Tan BK, Kern RC, Chandra RK (2015) The prevalence of bacterial infection in acute rhinosinusitis: a Systematic review and meta-analysis. Laryngoscope 125:57–69. https://doi.org/10.1002/lary.24709

    Article  PubMed  Google Scholar 

  4. Autio T, Tapiainen T, Koskenkorva T, Närkiö M, Lappalainen M, Nikkari S, Hemmilä H, Koskela KA, Koskela M, Koivunen P, Alho OP (2015) The role of microbes in the pathogenesis of acute rhinosinusitis in young adults. Laryngoscope 125:1–7. https://doi.org/10.1002/lary.24862

    Article  Google Scholar 

  5. National Institute for Health and Welfare. Out-patient treatment notifications in primary care in 2016. https://www.thl.fi/fi/tilastot/tiedonkeruut/perusterveydenhuollon-avohoidon-hoitoilmoitus-avohilmo/raportit. Accessed 18 Oct 2017

  6. Wang D, Wardani R, Sinqh K, Thanaviratananich S, Vicente G, Xu G, Zia M, Gulati A, Fang S, Shi L, Chan Y, Price D, Lund V, Mullol J, Fokkens W (2011) A survey on the management of acute rhinosinusitis among Asian physicians. Rhinology 49:264–271. https://doi.org/10.4193/Rhino10.169

    Article  PubMed  CAS  Google Scholar 

  7. Lemiengre MB, van Driel ML, Merenstein D, Young J, De Sutter AI (2012) Antibiotics for clinically diagnosed acute rhinosinusitis in adults. Cochrane Database Syst Rev 10:CD006089. https://doi.org/10.1002/14651858.CD006089.pub4

    Article  PubMed  Google Scholar 

  8. Payne SC, Benninger MS (2007) Staphylococcus aureus is a major pathogen in acute bacterial rhinosinusitis: a meta-analysis. Clin Infect Dis 45:121–127

    Article  Google Scholar 

  9. Benninger MS, Payne SC, Ferguson BJ, Ahmad N (2006) Endoscopically directed middle meatal cultures versus maxillary sinus taps in acute bacterial maxillary rhinosinusitis: a meta-analysis. Otolaryngol Head Neck Surg 134:3–9

    Article  PubMed  Google Scholar 

  10. Bijland LR, Bomers MK, Smulders YM (2013) Smelling the diagnosis: a review on the use of scent in diagnosing disease. Neth J Med 71:300–307

    PubMed  CAS  Google Scholar 

  11. Sethi S, Nanda R, Chakraborty T (2013) Clinical application of volatile organic compound analysis for detecting infectious diseases. Clin Microbiol Rev 26:462–475. https://doi.org/10.1128/CMR.00020-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Shirasu M, Touhara K (2011) The scent of disease: volatile organic compounds of the human body related to disease and disorders. J Biochem 150:257–266. https://doi.org/10.1093/jb/mvr090

    Article  PubMed  CAS  Google Scholar 

  13. Wilson D (2015) Advances in electronic-nose technologies for the detection of volatile biomarker metabolites in the human breath. Metabolites 5:140–163. https://doi.org/10.3390/metabo5010140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Lourenço C, Turner C (2014) Breath analysis in disease diagnosis: methodological considerations and applications. Metabolites 4:465–498. https://doi.org/10.3390/metabo4020465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Arshak K, Moore E, Lyons GM, Harris J, Clifford S (2004) A review of gas sensors employed in electronic nose applications. Sensor Review 24:181–198. https://doi.org/10.1108/02602280410525977

    Article  Google Scholar 

  16. Wilson D, Baietto M (2011) Advances in electronic-nose technologies developed for biomedical applications. Sensors 11:1105–1176. https://doi.org/10.3390/s110101105

    Article  PubMed  CAS  Google Scholar 

  17. Kolakowski B, Mester Z (2007) Review of applications of high-field asymmetric waveform ion mobility spectrometry (FAIMS) and differential mobility spectrometry (DMS). Analyst 132:842–886. https://doi.org/10.1039/b706039d

    Article  PubMed  CAS  Google Scholar 

  18. Covington JA, van der Schee MP, Edge SL, Boyle B, Savage S, Arasaradnam RP (2015) The application of FAIMS gas analysis in medical diagnostics. Analyst 140:6775–6781. https://doi.org/10.1039/c5an00868a

    Article  PubMed  CAS  Google Scholar 

  19. Roine A, Veskimäe E, Tuokko A, Kumpulainen P, Koskimäki J, Keinänen TA, Häkkinen MR, Vepsäläinen J, Paavonen T, Lekkala J, Lehtimäki T, Tammela TL, Oksala NK (2014) Detection of prostate cancer by an electronic nose: a proof of principle study. J Urol 192:230–234. https://doi.org/10.1016/j.juro.2014.01.113

    Article  PubMed  Google Scholar 

  20. Leunis N, Boumans ML, Kremer B, Din S, Stobberingh E, Kessels AG, Kross KW (2014) Application of an electronic nose in the diagnosis of head and neck cancer. Laryngoscope 124:1377–1381. https://doi.org/10.1002/lary.24463

    Article  PubMed  CAS  Google Scholar 

  21. Kolk A, Hoelscher M, Maboko L, Jung J, Kuijper S, Cauchi M, Bessant C, van Beers S, Dutta R, Gibson T, Reither K (2010) Electronic-nose technology using sputum samples in diagnosis of patients with tuberculosis. J Clin Microbiol 48:4235–4238. https://doi.org/10.1128/JCM.00569-10

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hockstein NG, Thaler ER, Torigian D, Miller WT Jr, Deffenderfer O, Hanson CW (2004) Diagnosis of pneumonia with an electronic nose: correlation of vapor signature with chest computed tomography scan findings. Laryngoscope 114:1701–1705

    Article  PubMed  Google Scholar 

  23. Thaler ER, Hanson C (2006) Use of an electronic nose to diagnose bacterial sinusitis. Am J Rhinol 20:170–172

    Article  PubMed  Google Scholar 

  24. Lai SY, Deffenderfer OF, Hanson W, Phillips MP, Thaler ER (2002) Identification of upper respiratory bacterial pathogens with the electronic nose. Laryngoscope 112:975–979

    Article  PubMed  Google Scholar 

  25. Thaler ER, Huang D, Giebeig L, Palmer J, Lee D, Hanson CW, Cohen N (2008) Use of an electronic nose for detection of biofilms. Am J Rhinol 22:29–33. https://doi.org/10.2500/ajr.2008.22.3126

    Article  PubMed  Google Scholar 

  26. Arasaradnam RP, Covington JA, Harmston C, Nwokolos CU (2014) Review article: next generation diagnostic modalities in gastroenterology—gas phase volatile compound biomarker detection. Aliment Pharmacol Ther 39:780–789. https://doi.org/10.1111/apt.12657

    Article  PubMed  CAS  Google Scholar 

  27. Mohamed EI, Bruno E, Linder R, Alessandrini M, Di Girolamo A, Pöppl SJ, Puija A, De Lorenzo A (2003) A novel method for diagnosing chronic rhinosinusitis based on an electronic nose. An Otorrinolaringol Ibero Am 30:447–457

    PubMed  Google Scholar 

  28. Leopold JH, Bos LD, Sterk PJ, Schultz MJ, Fens N, Horvath I, Bikov A, Montuschi P, Di Natale C, Yates DH, Abu-Hanna A (2015) Comparison of classification methods in breath analysis by electronic nose. J Breath Res 9:046002. https://doi.org/10.1088/1752-7155/9/4/046002

    Article  PubMed  Google Scholar 

  29. Marco S (2014) The need for external validation in machine olfaction: emphasis on health-related applications. Anal Bioanal Chem 406:3941–3956. https://doi.org/10.1007/s00216-014-7807-7

    Article  PubMed  CAS  Google Scholar 

  30. Bomers MK, Menke FP, Savage RS, Vandenbroucke-Grauls CM, van Agtmael MA, Covington JA, Smulders YM (2015) Rapid, accurate, and on-site detection of C. difficile in stool samples. Am J Gastroenterol 110:588–594. https://doi.org/10.1038/ajg.2015.90

    Article  PubMed  Google Scholar 

  31. Saviauk T, Kiiski JP, Nieminen MK, Tamminen NN, Roine AN, Kumpulainen PS, Hokkinen LJ, Karjalainen MT, Vuento RE, Aittoniemi JJ, Lehtimäki TJ, Oksala NK (2018) Electronic nose in the detection of wound infection bacteria from bacterial cultures: a proof-of-principle study. Eur Surg Res 59:1–11. https://doi.org/10.1159/000485461

    Article  PubMed  Google Scholar 

  32. Peng G, Tisch U, Adams O, Hakim M, Shehada N, Broza YY, Billan S, Abdah-Bortnyak R, Kuten A, Haick H (2009) Diagnosing lung cancer in exhaled breath using gold nanoparticles. Nat Nanotechnol 4:669–673. https://doi.org/10.1038/nnano.2009.235

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jussi Virtanen.

Ethics declarations

Conflict of interest

Niku Oksala, Markus Karjalainen, Anton Kontunen, and Antti Roine are shareholders of Olfactomics Ltd, which is about to commercialise proprietary technology for the detection of diseases by ion mobility spectrometry. The rest of the authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Virtanen, J., Hokkinen, L., Karjalainen, M. et al. In vitro detection of common rhinosinusitis bacteria by the eNose utilising differential mobility spectrometry. Eur Arch Otorhinolaryngol 275, 2273–2279 (2018). https://doi.org/10.1007/s00405-018-5055-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00405-018-5055-8

Keywords