Childhood measles contributes to post-bronchodilator airflow obstruction in middle-aged adults: A cohort study
Corresponding Author
Jennifer L. Perret
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Department of Respiratory and Sleep Medicine, Austin Hospital, Melbourne, VIC, Australia
Institute for Breathing and Sleep (IBAS), Melbourne, VIC, Australia
Correspondence: Jennifer L. Perret, Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Level 3, 207 Bouverie Street, The University of Melbourne, Melbourne, VIC 3010, Australia. Email: [email protected]Search for more papers by this authorMelanie C. Matheson
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorLyle C. Gurrin
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorDavid P. Johns
“Breathe Well” Centre of Research Excellence for Chronic Respiratory Disease and Lung Ageing, School of Medicine, University of Tasmania, Hobart, TAS, Australia
Search for more papers by this authorJohn A. Burgess
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorBruce R. Thompson
Department of Allergy, Immunology and Respiratory Medicine, The Alfred Hospital, Melbourne, VIC, Australia
Department of Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorAdrian J. Lowe
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorJames Markos
Launceston General Hospital, Hobart, TAS, Australia
Search for more papers by this authorStephen S. Morrison
Department of Medicine, University of Queensland, Brisbane, QLD, Australia
Search for more papers by this authorChristine F. McDonald
Department of Respiratory and Sleep Medicine, Austin Hospital, Melbourne, VIC, Australia
Institute for Breathing and Sleep (IBAS), Melbourne, VIC, Australia
Search for more papers by this authorRichard Wood-Baker
“Breathe Well” Centre of Research Excellence for Chronic Respiratory Disease and Lung Ageing, School of Medicine, University of Tasmania, Hobart, TAS, Australia
Search for more papers by this authorCecilie Svanes
Centre for International Health, University of Bergen, Bergen, Norway
Department of Occupational Medicine, Haukelaud University Hospital, Bergen, Norway
Search for more papers by this authorPaul S. Thomas
Prince of Wales’ Hospital Clinical School and School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia
Search for more papers by this authorJohn L. Hopper
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Department of Public Health, Seoul National University, Seoul, Republic of Korea
Search for more papers by this authorGraham G. Giles
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, VIC, Australia
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorMichael J. Abramson
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorE. Haydn Walters
“Breathe Well” Centre of Research Excellence for Chronic Respiratory Disease and Lung Ageing, School of Medicine, University of Tasmania, Hobart, TAS, Australia
E.H.W. and S.C.D. contributed equally to this studySearch for more papers by this authorShyamali C. Dharmage
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
E.H.W. and S.C.D. contributed equally to this studySearch for more papers by this authorCorresponding Author
Jennifer L. Perret
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Department of Respiratory and Sleep Medicine, Austin Hospital, Melbourne, VIC, Australia
Institute for Breathing and Sleep (IBAS), Melbourne, VIC, Australia
Correspondence: Jennifer L. Perret, Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Level 3, 207 Bouverie Street, The University of Melbourne, Melbourne, VIC 3010, Australia. Email: [email protected]Search for more papers by this authorMelanie C. Matheson
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorLyle C. Gurrin
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorDavid P. Johns
“Breathe Well” Centre of Research Excellence for Chronic Respiratory Disease and Lung Ageing, School of Medicine, University of Tasmania, Hobart, TAS, Australia
Search for more papers by this authorJohn A. Burgess
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorBruce R. Thompson
Department of Allergy, Immunology and Respiratory Medicine, The Alfred Hospital, Melbourne, VIC, Australia
Department of Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorAdrian J. Lowe
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Search for more papers by this authorJames Markos
Launceston General Hospital, Hobart, TAS, Australia
Search for more papers by this authorStephen S. Morrison
Department of Medicine, University of Queensland, Brisbane, QLD, Australia
Search for more papers by this authorChristine F. McDonald
Department of Respiratory and Sleep Medicine, Austin Hospital, Melbourne, VIC, Australia
Institute for Breathing and Sleep (IBAS), Melbourne, VIC, Australia
Search for more papers by this authorRichard Wood-Baker
“Breathe Well” Centre of Research Excellence for Chronic Respiratory Disease and Lung Ageing, School of Medicine, University of Tasmania, Hobart, TAS, Australia
Search for more papers by this authorCecilie Svanes
Centre for International Health, University of Bergen, Bergen, Norway
Department of Occupational Medicine, Haukelaud University Hospital, Bergen, Norway
Search for more papers by this authorPaul S. Thomas
Prince of Wales’ Hospital Clinical School and School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia
Search for more papers by this authorJohn L. Hopper
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Department of Public Health, Seoul National University, Seoul, Republic of Korea
Search for more papers by this authorGraham G. Giles
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, VIC, Australia
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorMichael J. Abramson
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, VIC, Australia
Search for more papers by this authorE. Haydn Walters
“Breathe Well” Centre of Research Excellence for Chronic Respiratory Disease and Lung Ageing, School of Medicine, University of Tasmania, Hobart, TAS, Australia
E.H.W. and S.C.D. contributed equally to this studySearch for more papers by this authorShyamali C. Dharmage
Allergy and Lung Health Unit, Centre for Epidemiology and Biostatistics, The University of Melbourne, Melbourne, VIC, Australia
E.H.W. and S.C.D. contributed equally to this studySearch for more papers by this authorAbstract
Background and objective
Chronic obstructive pulmonary disease (COPD) has potential origins in childhood but an association between childhood measles and post-bronchodilator (BD) airflow obstruction (AO) has not yet been shown. We investigated whether childhood measles contributed to post-BD AO through interactions with asthma and/or smoking in a non-immunized middle-aged population.
Methods
The population-based Tasmanian Longitudinal Health Study (TAHS) cohort born in 1961 (n = 8583) underwent spirometry in 1968 before immunization was introduced. A history of childhood measles infection was obtained from school medical records. During the fifth decade follow-up (n = 5729 responses), a subgroup underwent further lung function measurements (n = 1389). Relevant main associations and interactions by asthma and/or smoking on post-BD forced expiratory volume in 1 s/forced vital capacity (FEV1/FVC; continuous variable) and AO (FEV1/FVC < lower limit of normal) were estimated by multiple regression.
Results
Sixty-nine percent (n = 950) had a history of childhood measles. Childhood measles augmented the combined adverse effect of current clinical asthma and smoking at least 10 pack-years on post-BD FEV1/FVC ratio in middle age (z-score: −0.70 (95% CI: −1.1 to −0.3) vs −1.36 (−1.6 to −1.1), three-way interaction: P = 0.009), especially for those with childhood-onset asthma. For never- and ever-smokers of <10 pack-years who had current asthma symptoms, compared with those without childhood measles, paradoxically, the odds for post-BD AO was not significant in the presence of childhood measles (OR: 12.0 (95% CI: 3.4–42) vs 2.17 (0.9–5.3)).
Conclusion
Childhood measles infection appears to compound the associations between smoking, current asthma and post-BD AO. Differences between asthma subgroups provide further insight into the complex aetiology of obstructive lung diseases for middle-aged adults.
Supporting Information
| Filename | Description |
|---|---|
| resp13297-sup-0001-Appendix.docWord document, 89 KB |
Appendix S1 Additional lung function testing details. Appendix S2 Additional clinical definitions. Appendix S3 Additional statistical methods. Appendix S4 Childhood measles and other adult lung function. Table S1 Clinical comparison with the original Tasmanian Longitudinal Health Study cohort. Table S2 Measles–asthma–smoking interaction, different reference group. Table S3 Childhood measles, asthma-ever and lung function at age 7. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1 Svanes C, Sunyer J, Plana E, Dharmage S, Heinrich J, Jarvis D, de Marco R, Norback D, Raherison C, Villani S et al. Early life origins of chronic obstructive pulmonary disease. Thorax 2010; 65: 14–20.
- 2 Perret JL, Walters H, Johns D, Gurrin L, Burgess J, Lowe A, Thompson B, Markos J, Morrison S, Thomas P et al. Mother's smoking and complex lung function of offspring in middle age: a cohort study from childhood. Respirology 2016; 21: 911–9.
- 3 Lange P, Celli B, Agusti A. Lung-function trajectories and chronic obstructive pulmonary disease. N. Engl. J. Med. 2015; 373: 1575.
- 4 Fletcher C, Peto R. The natural history of chronic airflow obstruction. Br. Med. J. 1977; 1: 1645–8.
- 5 Burrows B, Knudson RJ, Lebowitz MD. The relationship of childhood respiratory illness to adult obstructive airway disease. Am. Rev. Respir. Dis. 1977; 115: 751–60.
- 6 Mok JY, Simpson H. Outcome of acute lower respiratory tract infection in infants: preliminary report of seven-year follow-up study. Br. Med. J. (Clin. Res. Ed.) 1982; 285: 333–7.
- 7 Pullan CR, Hey EN. Wheezing, asthma, and pulmonary dysfunction 10 years after infection with respiratory syncytial virus in infancy. Br. Med. J. (Clin. Res. Ed.) 1982; 284: 1665–9.
- 8 Shaheen SO, Barker DJ, Shiell AW, Crocker FJ, Wield GA, Holgate ST. The relationship between pneumonia in early childhood and impaired lung function in late adult life. Am. J. Respir. Crit. Care Med. 1994; 149: 616–9.
- 9 Barker DJ, Godfrey KM, Fall C, Osmond C, Winter PD, Shaheen SO. Relation of birth weight and childhood respiratory infection to adult lung function and death from chronic obstructive airways disease. BMJ 1991; 303: 671–5.
- 10 Shaheen SO, Sterne JA, Tucker JS, Florey CD. Birth weight, childhood lower respiratory tract infection, and adult lung function. Thorax 1998; 53: 549–53.
- 11 Perry RT, Halsey NA. The clinical significance of measles: a review. J. Infect. Dis. 2004; 189(Suppl. 1): S4–16.
- 12 Perret JL, Dharmage SC, Matheson MC, Johns DP, Gurrin LC, Burgess JA, Marrone J, Markos J, Morrison S, Feather I et al. The interplay between the effects of lifetime asthma, smoking, and atopy on fixed airflow obstruction in middle age. Am. J. Respir. Crit. Care Med. 2013; 187: 42–8.
- 13 Aanerud M, Carsin AE, Sunyer J, Dratva J, Gislason T, Jarvis D, deMarco R, Raherison C, Wjst M, Dharmage SC et al. Interaction between asthma and smoking increases the risk of adult airway obstruction. Eur. Respir. J. 2015; 45: 635–43.
- 14 Gibson HB, Silverstone H, Gandevia B, Hall GJ. Respiratory disorders in seven-year-old children in Tasmania. Aims, methods and administration of the survey. Med. J. Aust. 1969; 2: 201–5.
- 15 Nakajima K, Dharmage SC, Carlin JB, Wharton CL, Jenkins MA, Giles GG, Abramson MJ, Haydn Walters E, Hopper JL. Is childhood immunisation associated with atopic disease from age 7 to 32 years? Thorax 2007; 62: 270–5.
- 16 Burgess JA, Abramson MJ, Gurrin LC, Byrnes GB, Matheson MC, May CL, Giles GG, Johns DP, Hopper JL, Walters EH et al. Childhood infections and the risk of asthma: a longitudinal study over 37 years. Chest 2012; 142: 647–54.
- 17 Wharton C, Dharmage S, Jenkins M, Dite G, Hopper J, Giles G, Abramson M, Walters EH. Tracing 8,600 participants 36 years after recruitment at age seven for the Tasmanian Asthma Study. Aust. N. Z. J. Public Health 2006; 30: 105–10.
- 18 Matheson MC, Abramson MJ, Allen K, Benke G, Burgess JA, Dowty JG, Erbas B, Feather IH, Frith PA, Giles GG et al.; TAHS Investigator Group. Cohort profile: the Tasmanian Longitudinal Health Study (TAHS). Int. J. Epidemiol. 2017; 46: 407–8i.
- 19 Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P et al. Standardisation of spirometry. Eur. Respir. J. 2005; 26: 319–38.
- 20 Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CP, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P et al. Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur. Respir. J. 2005; 26: 720–35.
- 21 Wanger J, Clausen JL, Coates A, Pedersen OF, Brusasco V, Burgos F, Casaburi R, Crapo R, Enright P, van der Grinten CP et al. Standardisation of the measurement of lung volumes. Eur. Respir. J. 2005; 26: 511–22.
- 22 Quanjer PH, Stanojevic S, Cole TJ, Baur X, Hall GL, Culver BH, Enright PL, Hankinson JL, Ip MS, Zheng J et al. Multi-ethnic reference values for spirometry for the 3-95-yr age range: the global lung function 2012 equations. Eur. Respir. J. 2012; 40: 1324–43.
- 23 Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC. Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel And Coal. Official Statement of the European Respiratory Society. Eur. Respir. J. Suppl. 1993; 16: 5–40.
- 24 Thompson BR, Johns DP, Bailey M, Raven J, Walters EH, Abramson MJ. Prediction equations for single breath diffusing capacity (Tlco) in a middle aged Caucasian population. Thorax 2008; 63: 889–93.
- 25 Quanjer PH, Pretto JJ, Brazzale DJ, Boros PW. Grading the severity of airways obstruction: new wine in new bottles. Eur. Respir. J. 2014; 43: 505–12.
- 26 Kohn JL, Koiransky H. Successive roentgenograms of the chest of children during measles. Am. J. Dis. Child. 1929; 38: 258–70.
- 27 Scholes FVG. Diphtheria, Measles, Scarlatina, Second edn. Melbourne, William Ramsay, 1927.
- 28 Shaheen SO, Aaby P, Hall AJ, Barker DJ, Heyes CB, Shiell AW, Goudiaby A. Measles and atopy in Guinea-Bissau. Lancet 1996; 347: 1792–6.
- 29 Rennard SI, Drummond MB. Early chronic obstructive pulmonary disease: definition, assessment, and prevention. Lancet 2015; 385: 1778–88.
- 30 Burnet FM. Measles as an index of immunological function. Lancet 1968; 2: 610–3.
- 31 Rothman KJ. Causes. Am. J. Epidemiol. 1976; 104: 587–92.
- 32 van Zyl Smit RN, Pai M, Yew WW, Leung CC, Zumla A, Bateman ED, Dheda K. Global lung health: the colliding epidemics of tuberculosis, tobacco smoking, HIV and COPD. Eur. Respir. J. 2010; 35: 27–33.
- 33 Hancox RJ, Gray AR, Poulton R, Sears MR. The effect of cigarette smoking on lung function in young adults with asthma. Am. J. Respir. Crit. Care Med. 2016; 194: 276–84.
- 34 Perret J, Dharmage S. The less refined reference group of "no asthma" is related to the opposing interaction findings. Am. J. Respir. Crit. Care Med. 2016; 194: 1172–3.
- 35 Hancox RJ, Gray AR, Sears MR. Reply: The less refined reference group of "no asthma" is not related to the opposing interaction findings. Am. J. Respir. Crit. Care Med. 2016; 194: 1173–4.
- 36 Global Initiative for Asthma. Global Initiative for Chronic Obstructive Lung Disease. Diagnosis of Diseases of Chronic Airflow Limitation. Asthma COPD and Asthma-COPD Overlap Syndrome (ACOS), 2014. [Accessed 28 Oct 2014.] Available from URL: http://www.ginasthma.org
- 37 World Health Organization. Tobacco. Fact sheet no. 339. [Accessed Aug 2017.] Available from URL: http://www.who.int/mediacentre/factsheets/fs339/en/#
- 38 World Health Organization. Measles. Fact sheet no. 286. [Accessed Aug 2017.] Available from URL: http://www.who.int/mediacentre/factsheets/fs286/en/
