Skip to main content

Advertisement

SpringerLink
Log in

Effects of cigarette smoking on the association between respiratory muscle strength and skeletal muscle mass in middle-aged and older adults: the Wakayama Study

  • Research Paper
  • Published:
European Geriatric Medicine Aims and scope Submit manuscript

Key summary points

AbstractSection Aim

To examine the effect of cumulative smoking exposure on the association between peak expiratory flow rate (PEFR) and skeletal muscle mass in middle-aged and older adults.

AbstractSection Findings

The skeletal muscle mass progressively reduced with decreasing PEFR levels in individuals with non-smoking and light-to-moderate smoking exposure. However, the association between low PEFR level and reduced skeletal muscle mass was not clearly observed in individuals with heavy smoking exposure.

AbstractSection Message

Although decreased PEFR in the older population is associated with the age-related loss of systemic skeletal muscle mass, smoking exposure levels of individuals should be taken into consideration when using PEFR as an indicator of sarcopenia.

Abstract

Purpose

This study aimed to examine whether cumulative smoking exposure affects the association between peak expiratory flow rate (PEFR) and skeletal muscle mass in middle-aged and older adults.

Methods

The study participants comprised 832 community-dwelling individuals aged 50–89 years (mean age: 69 years) without chronic obstructive pulmonary disease. Bioelectrical impedance analysis was performed to estimate the skeletal muscle mass of each participant. PEFR was assessed using an electronic spirometer. Cumulative smoking exposure was expressed in pack years, that is a product of the average number of packs of cigarettes smoked per day and smoking duration in years.

Results

The whole-body skeletal muscle mass progressively reduced with decreasing PEFR levels in both males and females. In the multiple regression analysis, PEFR was found to be significantly associated with skeletal muscle mass, independent of the potential confounding factors. When participants were stratified based on the cumulative smoking exposure, the association between low PEFR and reduced skeletal muscle mass persisted in individuals with non-smoking and light-to-moderate smoking exposure (< 30 pack-years). However, this association was not clearly observed in individuals with heavy smoking exposure (≥ 30 pack-years).

Conclusion

The findings of this study support the notion that PEFR declines with a reduction in systemic skeletal muscle mass due to aging. However, chronic cigarette smoking induces respiratory dysfunction exceeding the expected values by age, and thus a low PEFR level may not be used as a marker of reduced muscle mass in older adults exposed to heavy smoking.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Cruz-Jentoft AJ, Bahat G, Bauer J et al (2019) Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48:16–31

    Article  Google Scholar 

  2. Chen LK, Woo J, Assantachai P et al (2020) Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J Am Med Dir Assoc 21:300–307

    Article  Google Scholar 

  3. Elliott JE, Greising SM, Mantilla CB et al (2016) Functional impact of sarcopenia in respiratory muscles. Respir Physiol Neurobiol 226:137–146

    Article  CAS  Google Scholar 

  4. Deniz O, Coteli S, Karatoprak NB et al (2021) Diaphragmatic muscle thickness in older people with and without sarcopenia. Aging Clin Exp Res 33:573–580

    Article  Google Scholar 

  5. Kera T, Kawai H, Hirano H et al (2018) Relationships among peak expiratory flow rate, body composition, physical function, and sarcopenia in community-dwelling older adults. Aging Clin Exp Res 30:331–340

    Article  Google Scholar 

  6. Ohara DG, Pegorari MS, Oliveira Dos Santos NL et al (2018) Respiratory muscle strength as a discriminator of sarcopenia in community-dwelling elderly: a cross-sectional study. J Nutr Health Aging 22:952–958

    Article  CAS  Google Scholar 

  7. Kera T, Kawai H, Hirano H et al (2019) Definition of respiratory sarcopenia with peak expiratory flow rate. J Am Med Dir Assoc 20:1021–1025

    Article  Google Scholar 

  8. Rom O, Kaisari S, Aizenbud D et al (2012) Identification of possible cigarette smoke constituents responsible for muscle catabolism. J Muscle Res Cell Motil 33:199–208

    Article  CAS  Google Scholar 

  9. Degens H, Gayan-Ramirez G, Van Hees HW (2015) Smoking-induced skeletal muscle dysfunction from evidence to mechanisms. Am J Respir Crit Care Med 191:620–625

    Article  CAS  Google Scholar 

  10. Hoshino Y, Mio T, Nagai S et al (2001) Cytotoxic effects of cigarette smoke extract on an alveolar type II cell-derived cell line. Am J Physiol Lung Cell Mol Physiol 281:L509–L516

    Article  CAS  Google Scholar 

  11. Ohnishi S, Miyai N, Utsumi M et al (2019) Liver fibrosis is associated with loss of skeletal muscle mass in community-dwelling older adults with no history of liver diseases. Jpn J Hyg 74:1–10

    Article  Google Scholar 

  12. Sterling RK, Lissen E, Clumeck N et al (2006) Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 43:1317–1325

    Article  CAS  Google Scholar 

  13. McPherson S, Hardy T, Dufour JF et al (2017) Age as a confounding factor for the accurate non-invasive diagnosis of advanced NAFLD fibrosis. Am J Gastroenterol 112:740–751

    Article  Google Scholar 

  14. Brinkman GL, Coates EO Jr (1963) The effect of bronchitis, smoking, and occupation on ventilation. Am Rev Respir Dis 87:684–693

    CAS  PubMed  Google Scholar 

  15. Wood DE, Baum SL, Eapen GA et al (2018) Lung cancer screening, version 3.2018, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 16:412–441

    Article  Google Scholar 

  16. The Ministry of Health, Labor and Welfare (2012) A basic direction for comprehensive implementation of national health promotion, Japan; https://www.mhlw.go.jp/file/06-Seisakujouhou-10900000-Kenkoukyoku/0000047330.pdf. Accessed 21 Sep 2021.

  17. Van der Ploeg HP, Chey T, Korda RJ et al (2012) Sitting time and all-cause mortality risk in 222 497 Australian adults. Arch Intern Med 172:494–500

    Article  Google Scholar 

  18. Tanaka NI, Miyatani M, Masuo Y et al (2007) Applicability of a segmental bioelectrical impedance analysis for predicting the whole body skeletal muscle volume. J Appl Physiol 103:1688–1695

    Article  Google Scholar 

  19. Miyatani M, Kanehisa H, Masuo Y et al (2001) Validity of estimating limb muscle volume by bioelectrical impedance. J Appl Physiol 91:386–394

    Article  CAS  Google Scholar 

  20. American thoracic society, European respiratory society (2002) ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med 166:518–624

    Article  Google Scholar 

  21. Schaap LA, Pluijm SMF, Deeg DJH et al (2006) Inflammatory markers and loss of muscle mass (Sarcopenia) and strength. Am J Med 119:526.e9-526.e17

    Article  Google Scholar 

  22. Buchman AS, Boyle PA, Wilson RS et al (2008) Respiratory muscle strength predicts decline in mobility in older persons. Neuroepidemiology 31:174–180

    Article  CAS  Google Scholar 

  23. Nogami E, Miyai N, Zhang Y et al (2021) Association of cigarette smoking with muscle mass reduction and low muscle strength in community-dwelling elderly men. Jpn J Hyg 76:1–9

    Article  Google Scholar 

  24. Steffl M, Bohannon RW, Petr M et al (2015) Relation between cigarette smoking and sarcopenia: meta-analysis. Physiol Res 64:419–426

    Article  CAS  Google Scholar 

  25. Bian AL, Hu HY, Rong YD et al (2017) A study on relationship between elderly sarcopenia and inflammatory factors IL-6 and TNF-α. Eur J Med Res 22:25

    Article  Google Scholar 

  26. Rom O, Kaisari S, Aizenbud D et al (2013) The effects of acetaldehyde and acrolein on muscle catabolism in C2 myotubes. Free Radic Biol Med 65:190–200

    Article  CAS  Google Scholar 

  27. Bergman BC, Perreault L, Hunerdosse D et al (2012) Novel and reversible mechanisms of smoking-induced insulin resistance in humans. Diabetes 61:3156–3166

    Article  CAS  Google Scholar 

  28. Kohansal R, Martinez-Canblor P, Agusti A et al (2009) The natural history of chronic airflow obstruction revisited an analysis of the Framingham offspring cohort. Am J Respir Crit Care Med 180:3–10

    Article  Google Scholar 

  29. Harmsen L, Thomsen SF, Ingebrigtsen T et al (2010) Chronic mucus hypersecretion: prevalence and risk factors in younger individuals. Int J Tuberc Lung Dis 14:1052–1058

    CAS  PubMed  Google Scholar 

  30. Quanjer PH, Lebowitz MD, Gregg I et al (1997) Peak expiratory flow: conclusions and recommendations of working party of the European Respiratory Society. Eur Respir J 24:2s–8s

    CAS  Google Scholar 

  31. Hanai T, Shiraki M, Ohnishi S et al (2016) Rapid skeletal muscle wasting predicts worse survival in patients with liver cirrhosis. Hepatol Res 46:743–751

    Article  CAS  Google Scholar 

  32. Hara N, Iwasa M, Sugimoto R et al (2016) Sarcopenia and sarcopenic obesity are prognostic factors for overall survival in patients with cirrhosis. Intern Med 55:863–870

    Article  CAS  Google Scholar 

  33. Onishi S, Miyai N, Zhang Y et al (2021) Excessive alcohol intake and liver fibrosis are associated with skeletal muscle mass reduction in elderly men: the Wakayama study. Aging Clin Exp Res 34:185–192

    Article  Google Scholar 

  34. Sánchez-Sánchez JL, Mañas A, García-García FJ et al (2019) Sedentary behaviour, physical activity, and sarcopenia among older adults in the TSHA: isotemporal substitution model. J Cachexia Sarcopenia Muscle 10:188–198

    Article  Google Scholar 

  35. Smeuninx B, Mckendry J, Wilson D et al (2017) Age-related anabolic resistance of myofibrillar protein synthesis is exacerbated in obese inactive individuals. J Clin Endocrinol Metab 102:3535–3545

    Article  Google Scholar 

  36. Breen L, Stokes KA, Churchward-Venne TA et al (2013) Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly. J Clin Endocrinol Metab 98:2604–2612

    Article  CAS  Google Scholar 

  37. Hautmann H, Hefele S, Schotten K et al (2000) Maximal inspiratory mouth pressures (PIMAX) in healthy subjects–what is the lower limit of normal? Respir Med 94:689–693

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (JSPS KAKENHI; Grant number: 17K01861).

Author information

Authors and Affiliations

  1. Graduate School of Health and Nursing Science, Wakayama Medical University, 580 Mikazura, P.O. Box 641-0011, Wakayama, Japan

    Eriko Nogami, Nobuyuki Miyai, Shuhei Onishi & Masato Sakaguchi

  2. Graduate School of Medicine, Wakayama Medical University, Wakayama, Japan

    Yan Zhang

  3. Graduate School of Comprehensive Rehabilitation, Osaka Prefecture University, Osaka, Japan

    Katsushi Yokoi

  4. Wakayama Faculty of Nursing, Tokyo Healthcare University, Wakayama, Japan

    Miyoko Utusmi

  5. Department of Cardiology, Sumiya Rehabilitation Hospital, Wakayama, Japan

    Masato Sakaguchi & Mikio Arita

Authors
  1. Eriko Nogami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nobuyuki Miyai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuhei Onishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masato Sakaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katsushi Yokoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Miyoko Utusmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mikio Arita
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EN and NM contributed to the study design, data collection, statistical analysis, interpretation, drafting, and final revision of the manuscript. YZ, SO, and MS contributed to the data collection and drafting of the manuscript. MU and MA contributed to the conception and design of the work and the final revision of the manuscript.

Corresponding author

Correspondence to Nobuyuki Miyai.

Ethics declarations

Conflict of interest

The authors declared that they have no potential conflicts of interest with respect to the research, research, authorship, and /or publication of this article.

Ethical approval

All procedures performed in this study were approved by the ethical committee of Wakayama Medical University (approval numbers: G92 and 2975).

Consent to participate

Written informed consent and clearance for the use of examination data were obtained from the participants after explaining the purpose of the study and the experimental procedure.

Consent for publication

The participants approved the manuscript and provided their consent for publication submission.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nogami, E., Miyai, N., Zhang, Y. et al. Effects of cigarette smoking on the association between respiratory muscle strength and skeletal muscle mass in middle-aged and older adults: the Wakayama Study. Eur Geriatr Med 13, 805–815 (2022). https://doi.org/10.1007/s41999-022-00662-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41999-022-00662-0

Keywords

Search

Navigation