Association between Asthma Control and Exposure to Greenness and Other Outdoor and Indoor Environmental Factors: A Longitudinal Study on a Cohort of Asthmatic Children

Giovanna Cilluffo, Giuliana Ferrante, Salvatore Fasola, Velia Malizia, Laura Montalbano, Andrea Ranzi, Chiara Badaloni, Giovanni Viegi, Stefania La Grutta, Giovanna Cilluffo, Giuliana Ferrante, Salvatore Fasola, Velia Malizia, Laura Montalbano, Andrea Ranzi, Chiara Badaloni, Giovanni Viegi, Stefania La Grutta

Abstract

Achieving and maintaining asthma control (AC) is the main goal of asthma management. Indoor and outdoor environmental factors may play an important role on AC. The aim of this longitudinal study was to evaluate the association between AC and exposure to greenness and other outdoor or indoor environmental factors in a cohort of asthmatic children. This study involved 179 asthmatic children (5-16 years). Parents were interviewed through a modified version of the SIDRIA questionnaire. AC was assessed at each visit. Exposure to greenness was measured using the normalized difference vegetation index (NDVI). A logistic regression model was applied for assessing risk factors for uncontrolled asthma (UA). Low NDVI exposure was a risk factor for UA (OR: 2.662, 95% CI (1.043-6.799)); children exposed to passive smoke during pregnancy had a higher risk of UA than those non-exposed to passive smoke during pregnancy (OR: 3.816, 95% CI (1.114-13.064)); and a unit increase in the crowding index was associated with an increased risk of UA (OR: 3.376, 95% CI (1.294-8.808)). In conclusion, the current study provided a comprehensive assessment of urban-related environmental exposures on asthma control in children, using multiple indicators of greenness and other outdoor or indoor environmental factors.

Trial registration: ClinicalTrials.gov NCT02433275.

Keywords: CORINE Land Cover; NDVI; asthma control; children; greenness; land use regression.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Study flowchart.
Figure 2
Figure 2
CLC category map of geo-coded children. Green points indicate the residence of each child and colored polygons identify the CORINE Land Cover categories.
Figure 3
Figure 3
ORs and 95% CI of the mixed-effect logistic regression model for asthma control.
Figure 4
Figure 4
ORs and 95% CI of the mixed-effect logistic regression model for asthma control: a sensitivity analysis after missing values imputation.
Figure 5
Figure 5
ORs and 95% CI of the mixed-effect logistic regression model for asthma control: sensitivity analysis adjusting for physical activity (>3 times per week).

References

    1. Dharmage S.C., Perret J., Custovic A. Epidemiology of asthma in children and adults. Front. Pediatr. 2019;7:246. doi: 10.3389/fped.2019.00246.
    1. Bateman E., Hurd S., Barnes P., Bousquet J., Drazen J., FitzGerald M., Gibson P., Ohta K., O’Byrne P., Pedersen S., et al. Global strategy for asthma management and prevention: GINA executive summary. Eur. Respir. J. 2008;31:143–178. doi: 10.1183/09031936.00138707.
    1. Montalbano L., Cilluffo G., Gentile M., Ferrante G., Malizia V., Cibella F., Viegi G., Passalacqua G., La Grutta S. Development of a nomogram to estimate the quality of life in asthmatic children using the Childhood Asthma Control Test. Pediatr. Allergy Immunol. 2016;27:514–520. doi: 10.1111/pai.12571.
    1. Etzel R.A. How environmental exposures influence the development and exacerbation of asthma. Pediatrics. 2003;112:233–239. doi: 10.1542/peds.112.S1.233.
    1. Ferrante G., Asta F., Cilluffo G., De Sario M., Michelozzi P., La Grutta S. The effect of residential urban greenness on allergic respiratory diseases in youth: A narrative review. World Allergy Organ. J. 2020;13:100096. doi: 10.1016/j.waojou.2019.100096.
    1. Andrusaityte S., Grazuleviciene R., Kudzyte J., Bernotiene A., Dedele A., Nieuwenhuijsen M.J. Associations between neighbourhood greenness and asthma in preschool children in Kaunas, Lithuania: A case–control study. BMJ Open. 2016;6:e010341. doi: 10.1136/bmjopen-2015-010341.
    1. Dadvand P., Villanueva C.M., Font-Ribera L., Martinez D., Basagaña X., Belmonte J., Vrijheid M., Gražulevičienė R., Kogevinas M., Nieuwenhuijsen M.J. Risks and benefits of green spaces for children: A cross-sectional study of associations with sedentary behavior, obesity, asthma, and allergy. Environ. Health Perspect. 2014;122:1329. doi: 10.1289/ehp.1308038.
    1. Wu M., Xie J., Wang Y., Tian Y. Greenness and eosinophilic asthma: Findings from the UK Biobank. Eur. Respir. J. 2021;58:2101597. doi: 10.1183/13993003.01597-2021.
    1. Hanski I., von Hertzen L., Fyhrquist N., Koskinen K., Torppa K., Laatikainen T., Karisola P., Auvinen P., Paulin L., Mäkelä M.J., et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl. Acad. Sci. USA. 2012;109:8334–8339. doi: 10.1073/pnas.1205624109.
    1. Lovasi G.S., Quinn J.W., Neckerman K.M., Perzanowski M.S., Rundle A. Children living in areas with more street trees have lower prevalence of asthma. J. Epidemiol. Community Health. 2008;62:647–649. doi: 10.1136/jech.2007.071894.
    1. Feng X., Astell-Burt T. Is neighborhood green space protective against associations between child asthma, neighborhood traffic volume and perceived lack of area safety? Multilevel analysis of 4447 Australian children. Int. J. Environ. Res. Public. Health. 2017;14:543. doi: 10.3390/ijerph14050543.
    1. Lovasi G.S., O’Neil-Dunne J.P., Lu J.W., Sheehan D., Perzanowski M.S., MacFaden S.W., King K.L., Matte T., Miller R.L., Hoepner L.A., et al. Urban tree canopy and asthma, wheeze, rhinitis, and allergic sensitization to tree pollen in a New York City birth cohort. Environ. Health Perspect. 2013;121:494. doi: 10.1289/ehp.1205513.
    1. Aerts R., Dujardin S., Nemery B., Van Nieuwenhuyse A., Van Orshoven J., Aerts J.-M., Somers B., Hendrickx M., Bruffaerts N., Bauwelinck M., et al. Residential green space and medication sales for childhood asthma: A longitudinal ecological study in Belgium. Environ. Res. 2020;189:109914. doi: 10.1016/j.envres.2020.109914.
    1. Tischer C., Gascon M., Fernández-Somoano A., Tardón A., Materola A.L., Ibarluzea J., Ferrero A., Estarlich M., Cirach M., Vrijheid M., et al. Urban green and grey space in relation to respiratory health in children. Eur. Respir. J. 2017;49:1502112. doi: 10.1183/13993003.02112-2015.
    1. Cavaleiro Rufo J., Paciência I., Hoffimann E., Moreira A., Barros H., Ribeiro A.I. The neighbourhood natural environment is associated with asthma in children: A birth cohort study. Allergy. 2021;76:348–358. doi: 10.1111/all.14493.
    1. Chen E., Miller G.E., Shalowitz M.U., Story R.E., Levine C.S., Hayen R., Sbihi H., Brauer M. Difficult family relationships, residential greenspace, and childhood asthma. Pediatrics. 2017;139:e20163056. doi: 10.1542/peds.2016-3056.
    1. Cowan K.N., Qin X., Ruiz Serrano K., Sircar K., Pennington A.F. Uncontrolled asthma and household environmental exposures in Puerto Rico. J. Asthma. 2020:1–11. doi: 10.1080/02770903.2020.1858861.
    1. Matsui E.C., Abramson S.L., Sandel M.T., Dinakar C., Irani A.M., Kim J.S., Mahr T.A., Pistiner M., Wang J., Lowry J.A., et al. Indoor environmental control practices and asthma management. Pediatrics. 2016;138:e20162589. doi: 10.1542/peds.2016-2589.
    1. Guarnieri M., Balmes J.R. Outdoor air pollution and asthma. Lancet. 2014;383:1581–1592. doi: 10.1016/S0140-6736(14)60617-6.
    1. Li Z., Xu X., Thompson L.A., Gross H.E., Shenkman E.A., DeWalt D.A., Huang I.-C. Longitudinal effect of ambient air pollution and pollen exposure on asthma control: The Patient-Reported Outcomes Measurement Information System (PROMIS) pediatric asthma study. Acad. Pediatr. 2019;19:615–623. doi: 10.1016/j.acap.2019.03.010.
    1. Cilluffo G., Ferrante G., Fasola S., Montalbano L., Malizia V., Piscini A., Romaniello V., Silvestri M., Stramondo S., Stafoggia M., et al. Associations of greenness, greyness and air pollution exposure with children’s health: A cross-sectional study in Southern Italy. Environ. Health. 2018;17:86. doi: 10.1186/s12940-018-0430-x.
    1. Squillacioti G., Bellisario V., Levra S., Piccioni P., Bono R. Greenness availability and respiratory health in a population of urbanised children in North-Western Italy. Int. J. Environ. Res. Public. Health. 2019;17:108. doi: 10.3390/ijerph17010108.
    1. Maio S., Baldacci S., Tagliaferro S., Angino A., Parmes E., Pärkkä J., Pesce G., Maesano C., Annesi-Maesano I., Viegi G. Urban grey spaces are associated with increased allergy in the general population. Environ. Res. 2021:112428. doi: 10.1016/j.envres.2021.112428.
    1. Renzoni E., Sestini P., Corbo G., Biggeri A., Viegi G., Forastiere F., on behalf of the SIDRIA Collaborative Group Asthma and respiratory symptoms in 6-7 yr old Italian children: Gender, latitude, urbanization and socioeconomic factors. Eur. Respir. J. 1997;10:1780–1786. doi: 10.1183/09031936.97.10081780.
    1. Liu A.H., Zeiger R., Sorkness C., Mahr T., Ostrom N., Burgess S., Rosenzweig J.C., Manjunath R. Development and cross-sectional validation of the Childhood Asthma Control Test. J. Allergy Clin. Immunol. 2007;119:817–825. doi: 10.1016/j.jaci.2006.12.662.
    1. ATS/ERS European Respiratory Society ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am. J. Respir. Crit Care Med. 2005;171:912–930. doi: 10.1164/rccm.200406-710ST.
    1. Quanjer P.H., Hall G.L., Stanojevic S., Cole T.J., Stocks J. Age-and height-based prediction bias in spirometry reference equations. Eur. Respir. J. 2012;40:190–197. doi: 10.1183/09031936.00161011.
    1. Beelen R., Hoek G., Vienneau D., Eeftens M., Dimakopoulou K., Pedeli X., Tsai M.-Y., Künzli N., Schikowski T., Marcon A., et al. Development of NO2 and NOx land use regression models for estimating air pollution exposure in 36 study areas in Europe–the ESCAPE project. Atmos. Environ. 2013;72:10–23. doi: 10.1016/j.atmosenv.2013.02.037.
    1. Vienneau D., De Hoogh K., Beelen R., Fischer P., Hoek G., Briggs D. Comparison of land-use regression models between Great Britain and the Netherlands. Atmos. Environ. 2010;44:688–696. doi: 10.1016/j.atmosenv.2009.11.016.
    1. Weier J., Herring D. Measuring Vegetation (NDVI&EVI) [(accessed on 27 July 2017)];2011 Available online:
    1. Lüdecke D. Sjstats: Statistical Functions for Regression Models (Version 0.18.1) 2021. [(accessed on 1 September 2021)]. Available online: .
    1. Stekhoven D.J., Bühlmann P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics. 2012;28:112–118. doi: 10.1093/bioinformatics/btr597.
    1. Lu N., Han Y., Chen T., Gunzler D.D., Xia Y., Julia Y., Lin J.Y., Tu X.M. Power analysis for cross-sectional and longitudinal study designs. Shanghai Arch. Psychiatry. 2013;25:259.
    1. Fuertes E., Markevych I., von Berg A., Bauer C.-P., Berdel D., Koletzko S., Sugiri D., Heinrich J. Greenness and allergies: Evidence of differential associations in two areas in Germany. J Epidemiol. Community Health. 2014;68:787–790. doi: 10.1136/jech-2014-203903.
    1. Remmers T., Thijs C., Ettema D., De Vries S., Slingerland M., Kremers S. Critical hours and important environments: Relationships between afterschool physical activity and the physical environment using GPS, GIS and accelerometers in 10–12-year-old children. Int. J. Environ. Res. Public. Health. 2019;16:3116. doi: 10.3390/ijerph16173116.
    1. Ward J.S., Duncan J.S., Jarden A., Stewart T. The impact of children’s exposure to greenspace on physical activity, cognitive development, emotional wellbeing, and ability to appraise risk. Health Place. 2016;40:44–50. doi: 10.1016/j.healthplace.2016.04.015.
    1. Matsunaga N.Y., Oliveira M.S., Morcillo A.M., Ribeiro J.D., Ribeiro M.A., Toro A.A. Physical activity and asthma control level in children and adolescents. Respirology. 2017;22:1643–1648. doi: 10.1111/resp.13093.
    1. Macaubas C., De Klerk N.H., Holt B.J., Wee C., Kendall G., on behalf of the Raine Study group. Firth M., Sly P.D., Holt P.G. Association between antenatal cytokine production and the development of atopy and asthma at age 6 years. Lancet. 2003;362:1192–1197. doi: 10.1016/S0140-6736(03)14542-4.
    1. Hollams E.M., De Klerk N.H., Holt P.G., Sly P.D. Persistent effects of maternal smoking during pregnancy on lung function and asthma in adolescents. Am. J. Respir. Crit. Care Med. 2014;189:401–407. doi: 10.1164/rccm.201302-0323OC.
    1. Li Y.-F., Gilliland F.D., Berhane K., McConnell R., James Gauderman W., Rappaport E.B., Peters J.M. Effects of in utero and environmental tobacco smoke exposure on lung function in boys and girls with and without asthma. Am. J. Respir. Crit. Care Med. 2000;162:2097–2104. doi: 10.1164/ajrccm.162.6.2004178.
    1. Zacharasiewicz A. Maternal smoking in pregnancy and its influence on childhood asthma. ERJ Open Res. 2016;2 doi: 10.1183/23120541.00042-2016.
    1. Cohen R.T., Raby B.A., Van Steen K., Fuhlbrigge A.L., Celedón J.C., Rosner B.A., Strunk R.C., Zeiger R.S., Weiss S.T., The CAMP Research Group In utero smoke exposure and impaired response to inhaled corticosteroids in children with asthma. J. Allergy Clin. Immunol. 2010;126:491–497. doi: 10.1016/j.jaci.2010.06.016.
    1. Burr J.A., Mutchler J.E., Gerst K. Patterns of residential crowding among Hispanics in later life: Immigration, assimilation, and housing market factors. J. Gerontol. B Psychol. Sci. Soc. Sci. 2010;65:772–782. doi: 10.1093/geronb/gbq069.
    1. Gray A. Definitions of Crowding and the Effects of Crowding on Health. Ministry of Social Development (MSD); Wellington, New Zealand: 2001. pp. 1–40. A Literature Review Prepared for the Ministry of Social Policy.
    1. Illi S., Depner M., Genuneit J., Horak E., Loss G., Strunz-Lehner C., Büchele G., Boznanski A., Danielewicz H., Cullinan P., et al. Protection from childhood asthma and allergy in Alpine farm environments—the GABRIEL Advanced Studies. J. Allergy Clin. Immunol. 2012;129:1470–1477. doi: 10.1016/j.jaci.2012.03.013.
    1. Kopel L.S., Phipatanakul W., Gaffin J.M. Social disadvantage and asthma control in children. Paediatr. Respir. Rev. 2014;15:256–263. doi: 10.1016/j.prrv.2014.04.017.
    1. Zhu Y., Zhong T., Ge D., Li Q., Wu J. Multi-factor analysis of single-center asthma control in Xiamen, China. Front. Pediatr. 2019;7:498. doi: 10.3389/fped.2019.00498.
    1. Ranzi A., Porta D., Badaloni C., Cesaroni G., Lauriola P., Davoli M., Forastiere F. Exposure to air pollution and respiratory symptoms during the first 7 years of life in an Italian birth cohort. Occup. Environ. Med. 2014;71:430–436. doi: 10.1136/oemed-2013-101867.

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