Download PDF
CC BY-NC-ND 4.0 · Int Arch Otorhinolaryngol 2021; 25(01): e160-e169
DOI: 10.1055/s-0040-1702965
Systematic Review

Nasal Mucociliary Clearance in Smokers: A Systematic Review

Awal Prasetyo 
1   Department of Biomedical Science, Faculty of Medicine, Diponegoro University, Semarang, Indonesia
2   Department of Anatomic Pathology, Faculty of Medicine, Diponegoro University - Dr. Kariadi Hospital, Semarang, Indonesia
,
Udadi Sadhana
2   Department of Anatomic Pathology, Faculty of Medicine, Diponegoro University - Dr. Kariadi Hospital, Semarang, Indonesia
,
Jethro Budiman 
1   Department of Biomedical Science, Faculty of Medicine, Diponegoro University, Semarang, Indonesia
2   Department of Anatomic Pathology, Faculty of Medicine, Diponegoro University - Dr. Kariadi Hospital, Semarang, Indonesia
3   Department of Emergency Unit, Panti Wilasa Citarum Hospital, Semarang, Indonesia
› Author Affiliations
› Further Information
   Permissions and Reprints

Abstract

Introduction Smoking is one of the most important causes of mortality and morbidity in the world, as it is related to the risk factor and etiology of respiratory-tract diseases. Long-term smoking causes both structural and functional damage in the respiratory airways, leading to changes in nasal mucociliary clearance (NMC).

Objectives The aim of the present study was to look systematically into the current literature and carefully collect and analyze results to explore NMC in smokers.

Data Synthesis Two independent reviewers conducted a literature search on some Electronic database: Pubmed, Medline, Ebsco, Springer Link, Science Direct, Scopus, and Proquest searching for articles fulfilling the inclusion and exclusion criteria. The lead author independently assessed the risk of bias of each of the included studies and discussed their assessments with the other two authors to achieve consensus. Of the 1,654 articles identified in the database search, 16 met the criteria for this review. Most of the articles (15 out of 16) showed the impairment of NMC in smokers.

Conclusion The present systematic review suggests that there is an impairment of NMC in smokers. The impairment is not only observed in cigarette smoking, but also in passive smoking, bidi smoking, electronic smoking, and hookah smoking. The impairment of NMC in chronic exposure to smoking is caused by the ciliotoxic effect, hypersecretion and viscoelastic change of mucous, airway surface liquid depletion, increased oxidative stress, and deteriorations in the inflammatory and immune systems.

Keywords

nasal mucociliary clearance - smokers - smoking


Publication History

Received: 15 October 2019

Accepted: 18 December 2019

Article published online:
24 April 2020

© 2020. Fundação Otorrinolaringologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil

 

  • References

  • 1 World Health Organization. WHO global report on trends in prevalence of tobacco smoking 2000–2025, second edition. 2018
    Google Scholar
  • 2 Solak I, Marakoglu K, Pekgor S, Kargin NC, Alatas N, Eryilmas MA. Nasal mucociliary activity changes in smokers. Konuralp Tip Derg 2018; 10 (03) 269-275
    CrossrefGoogle Scholar
  • 3 Paul B, Menon SS, Vasthare R, Balakrishnan R, Acharya S. Effect of bidi smoking on nasal mucociliary clearance: a comparative study. J Laryngol Otol 2018; 132 (12) 1077-1082
    CrossrefPubMedGoogle Scholar
  • 4 Dülger S, Akdeniz Ö, Solmaz F, Şengören Dikiş Ö, Yildiz T. Evaluation of nasal mucociliary clearance using saccharin test in smokers: A prospective study. Clin Respir J 2018; 12 (04) 1706-1710
    CrossrefPubMedGoogle Scholar
  • 5 Arıcıgil M, Arbağ H. Hookah smoking impairs nasal mucociliary clearance. Tob Induc Dis 2018; 16 (06) 06
    PubMedGoogle Scholar
  • 6 Kumral TL, Saltürk Z, Yildirim G. et al. How does electronic cigarette smoking affect sinonasal symptoms and nasal mucociliary clearance?. B-ENT 2016; 12 (01) 17-21
    PubMedGoogle Scholar
  • 7 Yadav J, Kaushik G, Ranga RK. Passive smoking affects nasal mucociliary clearance. JIACM 2014; 15 (02) 96-99
    Google Scholar
  • 8 Kim SY, Sim S, Choi HG. Active and passive smoking impacts on asthma with quantitative and temporal relations: A Korean Community Health Survey. Sci Rep 2018; 8 (01) 8614
    CrossrefPubMedGoogle Scholar
  • 9 Chatkin JM, Dullius CR. The management of asthmatic smokers. Asthma Res Pract 2016; 2 (10) 10
    CrossrefPubMedGoogle Scholar
  • 10 Long M, Fu Z, Li P, Nie Z. Cigarette smoking and the risk of nasopharyngeal carcinoma: a meta-analysis of epidemiological studies. BMJ Open 2017; 7 (10) e016582
    CrossrefPubMedGoogle Scholar
  • 11 Utiyama DMO, Yoshida CT, Goto DM. et al. The effects of smoking and smoking cessation on nasal mucociliary clearance, mucus properties and inflammation. Clinics (São Paulo) 2016; 71 (06) 344-350
    CrossrefPubMedGoogle Scholar
  • 12 Pagliuca G, Rosato C, Martellucci S. et al. Cytologic and functional alterations of nasal mucosa in smokers: temporary or permanent damage?. Otolaryngol Head Neck Surg 2015; 152 (04) 740-745
    CrossrefPubMedGoogle Scholar
  • 13 Alekseenko SI, Skalny AV, Ajsuvakova OP, Skalnaya MG, Notova SV, Tinkov AA. Mucociliary transport as a link between chronic rhinosinusitis and trace element dysbalance. Med Hypotheses 2019; 127: 5-10
    CrossrefPubMedGoogle Scholar
  • 14 Bustamante-Marin XM, Ostrowski LE. Cilia and mucociliary clearance. Cold Spring Harb Perspect Biol 2017; 9 (04) 1-17
    CrossrefPubMedGoogle Scholar
  • 15 Munkholm M, Mortensen J. Mucociliary clearance: pathophysiological aspects. Clin Physiol Funct Imaging 2014; 34 (03) 171-177
    CrossrefPubMedGoogle Scholar
  • 16 Paul P, Johnson P, Ramaswamy P, Ramadoss S, Geetha B, Subhashini AS. The Effect of ageing on nasal mucociliary clearance in women: A pilot study. ISRN Pulmonol 2013; •••: 1-5
    CrossrefGoogle Scholar
  • 17 Baby MK, Muthu PK, Johnson P, Kannan S. Effect of cigarette smoking on nasal mucociliary clearance: A comparative analysis using saccharin test. Lung India 2014; 31 (01) 39-42
    CrossrefPubMedGoogle Scholar
  • 18 Jiao J, Zhang L. Influence of intranasal drugs on human nasal mucociliary clearance and ciliary beat frequency. Allergy Asthma Immunol Res 2019; 11 (03) 306-319
    CrossrefPubMedGoogle Scholar
  • 19 Jarosław P, Agnieszka P, Jarosław M. et al. Influence of environmental and clinical factors on nasal mucociliary clearance of the students of the medical university of silesia. Pol Przegląd Otorynolaryngol 2015; 4 (02) 45-52
    Google Scholar
  • 20 Xavier RF, Ramos D, Ito JT. et al. Effects of cigarette smoking intensity on the mucociliary clearance of active smokers. Respiration 2013; 86 (06) 479-485
    CrossrefPubMedGoogle Scholar
  • 21 Higgins J, Green S. Cochrane handbook for systematic reviews of intervention 5.2. United Kingdom: John Wiley and Sons; 2017: 1-50
    Google Scholar
  • 22 Moher D, Liberati A, Tetzlaff J, Altman DG, Group TP. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6 (07) e1000097
    CrossrefPubMedGoogle Scholar
  • 23 Herzog R, Álvarez-Pasquin MJ, Díaz C, Del Barrio JL, Estrada JM, Gil Á. Are healthcare workers' intentions to vaccinate related to their knowledge, beliefs and attitudes? A systematic review. BMC Public Health 2013; 13 (154) 154
    CrossrefPubMedGoogle Scholar
  • 24 Wells G, Shea B, O'Connell D, Peterson J, Welch V, Losos M. et al. The newcastle-ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. 2019
    Google Scholar
  • 25 Viswanathan M, Ansari MT, Berkman ND. et al. Methods guide for effectiveness and comparative effectiveness reviews, assessing the risk of bias of individual studies in systematic reviews of health care interventions. USA: AHRQ Publication; 2008
    Google Scholar
  • 26 Islam MM, Iqbal U, Walther B. et al. Benzodiazepine use and risk of dementia in the elderly population: A systematic review and meta-analysis. Neuroepidemiology 2016; 47 (3-4): 181-191
    CrossrefPubMedGoogle Scholar
  • 27 Luchini C, Stubbs B, Solmi M, Veronese N. Assessing the quality of studies in meta-analyses: Advantages and limitations of the newcastle ottawa scale. World J Metaanal 2017; 5 (04) 80-84
    Google Scholar
  • 28 Nicola ML, Carvalho HB, Yoshida CT. et al. Young “healthy” smokers have functional and inflammatory changes in the nasal and the lower airways. Chest 2014; 145 (05) 998-1005
    CrossrefPubMedGoogle Scholar
  • 29 Habesoglu TE, Kule M, Kule ZG. et al. How does parental smoking affect nasal mucociliary clearance in children?. Eur Arch Otorhinolaryngol 2015; 272 (03) 607-611
    CrossrefPubMedGoogle Scholar
  • 30 Tamashiro E, Cohen NA, Palmer JN, Lima WT, Lima A. Effects of cigarette smoking on the respiratory epithelium and its role in the pathogenesis of chronic rhinosinusitis. Rev Bras Otorrinolaringol (Engl Ed) 2009; 75 (06) 903-907
    Google Scholar
  • 31 Ramos EM, De Toledo AC, Xavier RF. et al. Reversibility of impaired nasal mucociliary clearance in smokers following a smoking cessation programme. Respirology 2011; 16 (05) 849-855
    CrossrefPubMedGoogle Scholar
  • 32 Leopold PL, O'Mahony MJ, Lian XJ, Tilley AE, Harvey BG, Crystal RG. Smoking is associated with shortened airway cilia. PLoS One 2009; 4 (12) e8157
    CrossrefPubMedGoogle Scholar
  • 33 Alexander NS, Blount A, Zhang S. et al. CFTR modulation by the tobacco smoke toxin acrolein. Laryngoscope 2012; 122 (06) 1193-1197
    CrossrefPubMedGoogle Scholar
  • 34 Cohen NA, Zhang S, Sharp DB. et al. Cigarette smoke condensate inhibits transepithelial chloride transport and ciliary beat frequency. Laryngoscope 2009; 119 (11) 2269-2274
    CrossrefPubMedGoogle Scholar
  • 35 Proença M, Fagundes Xavier R, Ramos D, Cavalheri V, Pitta F, Cipulo Ramos EM. [Immediate and short term effects of smoking on nasal mucociliary clearance in smokers]. Rev Port Pneumol 2011; 17 (04) 172-176
    CrossrefPubMedGoogle Scholar
  • 36 Palazzolo DL, Nelson JM, Ely EA, Crow AP, Distin J, Kunigelis SC. The effects of electronic cigarette (ECIG)-generated aerosol and conventional cigarette smoke on the mucociliary transport velocity (MTV) using the bullfrog (R. catesbiana) palate paradigm. Front Physiol 2017; 8 (1023): 1023
    CrossrefPubMedGoogle Scholar
  • 37 Elliott MK, Sisson JH, Wyatt TA. Effects of cigarette smoke and alcohol on ciliated tracheal epithelium and inflammatory cell recruitment. Am J Respir Cell Mol Biol 2007; 36 (04) 452-459
    CrossrefPubMedGoogle Scholar
  • 38 Habesoglu M, Demir K, Yumusakhuylu AC, Yilmaz AS, Oysu C. Does passive smoking have an effect on nasal mucociliary clearance?. Otolaryngol Head Neck Surg 2012; 147 (01) 152-156
    CrossrefPubMedGoogle Scholar
  • 39 Duong M, Rangarajan S, Zhang X. et al. Effects of bidi smoking on all-cause mortality and cardiorespiratory outcomes in men from south Asia: an observational community-based substudy of the Prospective Urban Rural Epidemiology Study (PURE). Lancet Glob Health 2017; 5 (02) e168-e176
    CrossrefPubMedGoogle Scholar
  • 40 Amith HV, Agrawal D, Gupta A, Shrivastava TP, Purohit BM, Bhambhani G. Assessing the nicotine content of smoked and smokeless forms of Tobacco Available in Bhopal. Indian J Dent Res 2018; 29 (03) 341-346
    CrossrefPubMedGoogle Scholar
  • 41 Yıldırım F, Çevik Y, Emektar E, Çorbacıoğlu ŞK, Katırcı Y. Evaluating ECG and carboxyhemoglobin changes due to smoking narghile. Inhal Toxicol 2016; 28 (12) 546-549
    CrossrefPubMedGoogle Scholar
  • 42 Daher N, Saleh R, Jaroudi E. et al. Comparison of carcinogen, carbon monoxide, and ultrafine particle emissions from narghile waterpipe and cigarette smoking: Sidestream smoke measurements and assessment of second-hand smoke emission factors. Atmos Environ (1994) 2010; 44 (01) 8-14
    CrossrefPubMedGoogle Scholar
  • 43 Shihadeh A, Salman R, Jaroudi E. et al. Does switching to a tobacco-free waterpipe product reduce toxicant intake? A crossover study comparing CO, NO, PAH, volatile aldehydes, “tar” and nicotine yields. Food Chem Toxicol 2012; 50 (05) 1494-1498
    CrossrefPubMedGoogle Scholar
  • 44 Jacob III P, Abu Raddaha AH, Dempsey D. et al. Nicotine, carbon monoxide, and carcinogen exposure after a single use of a water pipe. Cancer Epidemiol Biomarkers Prev 2011; 20 (11) 2345-2353
    CrossrefPubMedGoogle Scholar
  • 45 El-Zaatari ZM, Chami HA, Zaatari GS. Health effects associated with waterpipe smoking. Tob Control 2015; 24 (Suppl. 01) i31-i43
    CrossrefPubMedGoogle Scholar
  • 46 Nemmar A, Yuvaraju P, Beegam S, John A, Raza H, Ali BH. Cardiovascular effects of nose-only water-pipe smoking exposure in mice. Am J Physiol Heart Circ Physiol 2013; 305 (05) H740-H746
    CrossrefPubMedGoogle Scholar
  • 47 Chung S, Baumlin N, Dennis JS. et al. Electronic cigarette vapor with nicotine causes airway mucociliary dysfunction preferentially via TRPA1 receptors. Am J Respir Crit Care Med 2019; 200 (09) 1134-1145
    CrossrefPubMedGoogle Scholar
  • 48 Uzeloto JS, Ramos D. C F Freire AP, G D Christofaro D, Mara C Ramos E. Nasal mucociliary transportability of male and female smokers. Rev Bras Otorrinolaringol (Engl Ed) 2018; 84 (03) 311-317
    Google Scholar