Advertisement

Clinical Reviews in Allergy & Immunology

, Volume 57, Issue 3, pp 415–426 | Cite as

Asthma and Allergies in the School Environment

  • Brittany Esty
  • Perdita Permaul
  • Kristie DeLoreto
  • Sachin N. Baxi
  • Wanda PhipatanakulEmail author
Article

Abstract

The school is a complex microenvironment of indoor allergens, pollutants, and other exposures. The school represents an occupational model for children and exposures in this environment have a significant health effect. Current research establishes an association between school exposure and asthma morbidity in children. This review will focus on common school environmental exposures (cockroach, rodents, cat, dog, classroom pets, dust mite, fungus, and pollution) and their impact on children with allergies and asthma. Understanding and evaluation of school-based environments is needed to help guide school-based interventions. School-based interventions have the potential for substantial benefit to the individual, school, community, and public health. However, there is a paucity data on school-based environmental interventions and health outcomes. The studies performed to date are small and cross-sectional with no control for home exposures. Randomized controlled school-based environmental intervention trials are needed to assess health outcomes and the cost-effectiveness of these interventions. The School Inner-City Asthma Intervention Study (SICAS 2), a NIH/NIAID randomized controlled clinical trial using environmental interventions modeled from successful home-based interventions, is currently underway with health outcome results pending. If efficacious, these interventions could potentially help further guide school-based interventions potentially with policy implications. In the meanwhile, the allergist/immunologist can continue to play a vital role in improving the quality of life in children with allergies and asthma at school through the use of the ADA policy and Section 504 of the Rehabilitation Act as well as encouraging adoption of toolkits to build successful school-based asthma programs and asthma-friendly schools.

Keywords

Asthma Allergen Environment Pediatric asthma Pollutant School School exposure School-based intervention 

Abbreviations

SICAS 1

School Inner-City Asthma Study

NIH

National Institutes of Health

NIAID

National Institute of Allergy and Infectious Disease

IPM

Integrated pest management

HEPA

High efficiency particulate arrestance

PM2.5

Particulate matter 2.5

BC

Black carbon

NO2

Nitrogen dioxide

(CO)

Carbon monoxide

O3

Ozone

SICAS 2

School Inner-City Asthma Intervention Study

Notes

Acknowledgements

This work was conducted with support from Harvard Catalyst—The Harvard Clinical and Translational Science Center—(National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health Award UL1 TR001102) and financial contributions from Harvard University and its affiliated academic healthcare centers. The content is solely the responsibility of the authors and does not necessarily represent the official views of Harvard Catalyst, Harvard University, and its affiliated academic healthcare centers or the National Institutes of Health.

Funding

This work was supported by grants: K24 AI 106822, U01 AI 110397, R01 HL 137192 (PI: Dr. Phipatanakul) from the National Institutes of Health, and the Allergy and Asthma Awareness Initiative and K23 AI 123517 and LRP #L40 AI113791 (PI: Dr. Permaul) from the National Institutes of Health. Dr. Esty was supported by the Harvard Medical School Fellowship in Patient Safety and Quality (Boston, MA).

Compliance with Ethical Standards

Conflict of Interest

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.

References

  1. 1.
    National Center for Health Statistics. Centers for disease control and prevention. Asthma. Available from: https://www.cdc.gov/nchs/fastats/asthma.htm. Accessed 22 Jan 2018
  2. 2.
    Centers for Disease Control and Prevention. Asthma in schools. Available from: https://www.cdc.gov/healthyschools/asthma/. Accessed 22 Jan 2018
  3. 3.
    Barnett SB, Nurmagambetov TA (2011) Costs of asthma in the United States: 2002-2007. J Allergy Clin Immunol 127(1):145–152PubMedGoogle Scholar
  4. 4.
    Sullivan PW, Ghushchyan V, Navaratnam P, Friedman HS, Kavati A, Ortiz B et al (2017) The national cost of asthma among school-aged children in the United States. Ann Allergy Asthma Immunol 119(3):246–52.e1PubMedGoogle Scholar
  5. 5.
    Klepeis NE, Nelson WC, Ott WR, Robinson JP, Tsang AM, Switzer P et al (2001) The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants. J Expo Anal Environ Epidemiol 11(3):231–252PubMedGoogle Scholar
  6. 6.
    Rosenstreich DL, Eggleston P, Kattan M, Baker D, Slavin RG, Gergen P, Mitchell H, McNiff-Mortimer K, Lynn H, Ownby D, Malveaux F (1997) The role of cockroach allergy and exposure to cockroach allergen in causing morbidity among inner-city children with asthma. N Engl J Med 336(19):1356–1363PubMedGoogle Scholar
  7. 7.
    Crain EF, Walter M, O'Connor GT, Mitchell H, Gruchalla RS, Kattan M, Malindzak GS, Enright P, Evans R 3rd, Morgan W, Stout JW (2002) Home and allergic characteristics of children with asthma in seven U.S. urban communities and design of an environmental intervention: the Inner-City Asthma Study. Environ Health Perspect 110(9):939–945PubMedPubMedCentralGoogle Scholar
  8. 8.
    Kattan M, Mitchell H, Eggleston P, Gergen P, Crain E, Redline S, Weiss K, Evans R, Kaslow R, Kercsmar C, Leickly F, Malveaux F, Wedner HJ (1997) Characteristics of inner-city children with asthma: the National Cooperative Inner-City Asthma Study. Pediatr Pulmonol 24(4):253–262PubMedPubMedCentralGoogle Scholar
  9. 9.
    Chew GL, Correa JC, Perzanowski MS (2005) Mouse and cockroach allergens in the dust and air in northeastern United States inner-city public high schools. Indoor Air 15(4):228–234PubMedPubMedCentralGoogle Scholar
  10. 10.
    Permaul P, Hoffman E, Fu C, Sheehan W, Baxi S, Gaffin J, Lane J, Bailey A, King E, Chapman M, Gold D, Phipatanakul W (2012) Allergens in urban schools and homes of children with asthma. Pediatr Allergy Immunol 23(6):543–549PubMedPubMedCentralGoogle Scholar
  11. 11.
    Sheehan WJ, Rangsithienchai PA, Muilenberg ML, Rogers CA, Lane JP, Ghaemghami J, Rivard DV, Otsu K, Hoffman EB, Israel E, Gold DR, Phipatanakul W (2009) Mouse allergens in urban elementary schools and homes of children with asthma. Ann Allergy Asthma Immunol 102(2):125–130PubMedPubMedCentralGoogle Scholar
  12. 12.
    Baxi SN, Muilenberg ML, Rogers CA, Sheehan WJ, Gaffin J, Permaul P, Kopel LS, Lai PS, Lane JP, Bailey A, Petty CR, Fu C, Gold DR, Phipatanakul W (2013) Exposures to molds in school classrooms of children with asthma. Pediatr Allergy Immunol 24(7):697–703PubMedPubMedCentralGoogle Scholar
  13. 13.
    Gaffin JM, Hauptman M, Petty CR, Sheehan WJ, Lai PS, Wolfson JM, Gold DR, Coull BA, Koutrakis P, Phipatanakul W (2017) Nitrogen dioxide exposure in school classrooms of inner-city children with asthma. J Allergy Clin Immunol 141(6):2249–2255PubMedPubMedCentralGoogle Scholar
  14. 14.
    Kanchongkittiphon W, Sheehan WJ, Friedlander J, Chapman MD, King EM, Martirosyan K, Baxi SN, Permaul P, Gaffin JM, Kopel L, Bailey A, Fu C, Petty CR, Gold DR, Phipatanakul W (2014) Allergens on desktop surfaces in preschools and elementary schools of urban children with asthma. Allergy. 69(7):960–963PubMedPubMedCentralGoogle Scholar
  15. 15.
    Sheehan WJ, Permaul P, Petty CR, Coull BA, Baxi SN, Gaffin JM, Lai PS, Gold DR, Phipatanakul W (2017) Association between allergen exposure in inner-city schools and asthma morbidity among students. JAMA Pediatr 171(1):31–38PubMedPubMedCentralGoogle Scholar
  16. 16.
    Chen CH, Chao HJ, Chan CC, Chen BY, Guo YL (2014) Current asthma in schoolchildren is related to fungal spores in classrooms. Chest. 146(1):123–134PubMedGoogle Scholar
  17. 17.
    Holst GJ, Host A, Doekes G, Meyer HW, Madsen AM, Plesner KB et al (2016) Allergy and respiratory health effects of dampness and dampness-related agents in schools and homes: a cross-sectional study in Danish pupils. Indoor Air 26(6):880–891PubMedPubMedCentralGoogle Scholar
  18. 18.
    Almqvist C, Wickman M, Perfetti L, Berglind N, Renstrom A, Hedren M et al (2001) Worsening of asthma in children allergic to cats, after indirect exposure to cat at school. Am J Respir Crit Care Med 163(3 Pt 1):694–698PubMedPubMedCentralGoogle Scholar
  19. 19.
    Morgan WJ, Crain EF, Gruchalla RS, O'Connor GT, Kattan M, Evans R 3rd et al (2004) Results of a home-based environmental intervention among urban children with asthma. N Engl J Med 351(11):1068–1080PubMedGoogle Scholar
  20. 20.
    Dutmer CM, Kim H, Searing DA, Zoratti EM, Liu AH (2018) Asthma in inner city children: recent insights: United States. Curr Opin Allergy Clin Immunol 18(2):139–147PubMedPubMedCentralGoogle Scholar
  21. 21.
    Poowuttikul P, Saini S, Seth D (2019) Inner-city asthma in children. Clin Rev Allergy Immunol 56(2):248–268Google Scholar
  22. 22.
    Szefler SJ, Gergen PJ, Mitchell H, Morgan W (2010) Achieving asthma control in the inner city: do the National Institutes of Health Asthma Guidelines really work? J Allergy Clin Immunol 125(3):521–526 quiz 7-8PubMedPubMedCentralGoogle Scholar
  23. 23.
    Bollinger ME, Butz A, Tsoukleris M, Lewis-Land C, Mudd S, Morphew T (2019) Characteristics of inner city children with life-threatening asthma. Ann Allergy Asthma Immunol 122(4):381–386Google Scholar
  24. 24.
    Ahluwalia SK, Peng RD, Breysse PN, Diette GB, Curtin-Brosnan J, Aloe C et al (2013) Mouse allergen is the major allergen of public health relevance in Baltimore City. J Allergy Clin Immunol 132(4):830–5.e1–2PubMedPubMedCentralGoogle Scholar
  25. 25.
    Phipatanakul W, Eggleston PA, Wright EC, Wood RA (2000) Mouse allergen. I. the prevalence of mouse allergen in inner-city homes. The National Cooperative Inner-City Asthma Study. J Allergy Clin Immunol 106(6):1070–1074PubMedGoogle Scholar
  26. 26.
    Gruchalla RS, Pongracic J, Plaut M, Evans R, Visness CM, Walter M et al (2005) Inner City Asthma Study: relationships among sensitivity, allergen exposure, and asthma morbidity. J Allergy Clin Immunol 115(3):478–485PubMedPubMedCentralGoogle Scholar
  27. 27.
    Sarpong SB, Hamilton RG, Eggleston PA, Adkinson NF Jr (1996) Socioeconomic status and race as risk factors for cockroach allergen exposure and sensitization in children with asthma. J Allergy Clin Immunol 97(6):1393–1401PubMedPubMedCentralGoogle Scholar
  28. 28.
    Olmedo O, Goldstein IF, Acosta L, Divjan A, Rundle AG, Chew GL et al (2011) Neighborhood differences in exposure and sensitization to cockroach, mouse, dust mite, cat, and dog allergens in New York City. J Allergy Clin Immunol 128(2):284–92.e7PubMedPubMedCentralGoogle Scholar
  29. 29.
    Phipatanakul W, Eggleston PA, Wright EC, Wood RA, Study NCI-CA (2000) Mouse allergen. II. The relationship of mouse allergen exposure to mouse sensitization and asthma morbidity in inner-city children with asthma. J Allergy Clin Immunol 106(6):1075–1080PubMedPubMedCentralGoogle Scholar
  30. 30.
    Grant T, Aloe C, Perzanowski M, Phipatanakul W, Bollinger ME, Miller R et al (2017) Mouse sensitization and exposure are associated with asthma severity in urban children. J Allergy Clin Immunol Pract 5(4):1008–14.e1PubMedGoogle Scholar
  31. 31.
    Pomes A, Mueller GA, Randall TA, Chapman MD, Arruda LK (2017) New insights into cockroach allergens. Curr Allergy Asthma Rep 17(4):25PubMedPubMedCentralGoogle Scholar
  32. 32.
    DiMango E, Serebrisky D, Narula S, Shim C, Keating C, Sheares B et al (2016) Individualized household allergen intervention lowers allergen level but not asthma medication use: a randomized controlled trial. J Allergy Clin Immunol Pract 4(4):671–9.e4PubMedPubMedCentralGoogle Scholar
  33. 33.
    Rabito FA, Carlson JC, He H, Werthmann D, Schal C (2017) A single intervention for cockroach control reduces cockroach exposure and asthma morbidity in children. J Allergy Clin Immunol 140(2):565–570PubMedGoogle Scholar
  34. 34.
    Matsui EC, Perzanowski M, Peng RD, Wise RA, Balcer-Whaley S, Newman M, Cunningham A, Divjan A, Bollinger ME, Zhai S, Chew G, Miller RL, Phipatanakul W (2017) Effect of an integrated pest management intervention on asthma symptoms among mouse-sensitized children and adolescents with asthma: a randomized clinical trial. JAMA. 317(10):1027–1036PubMedPubMedCentralGoogle Scholar
  35. 35.
    Gold DR, Adamkiewicz G, Arshad SH, Celedon JC, Chapman MD, Chew GL et al (2017) NIAID, NIEHS, NHLBI, and MCAN Workshop Report: the indoor environment and childhood asthma-implications for home environmental intervention in asthma prevention and management. J Allergy Clin Immunol 140(4):933–949PubMedPubMedCentralGoogle Scholar
  36. 36.
    Sarpong SB, Wood RA, Karrison T, Eggleston PA (1997) Cockroach allergen (Bla g 1) in school dust. J Allergy Clin Immunol 99(4):486–492PubMedGoogle Scholar
  37. 37.
    Amr S, Bollinger ME, Myers M, Hamilton RG, Weiss SR, Rossman M, Osborne L, Timmins S, Kimes DS, Levine ER, Blaisdell CJ (2003) Environmental allergens and asthma in urban elementary schools. Ann Allergy Asthma Immunol 90(1):34–40PubMedPubMedCentralGoogle Scholar
  38. 38.
    Phipatanakul W, Bailey A, Hoffman EB, Sheehan WJ, Lane JP, Baxi S et al (2011) The school inner-city asthma study: design, methods, and lessons learned. J Asthma. 48(10):1007–1014PubMedPubMedCentralGoogle Scholar
  39. 39.
    Abramson SL, Turner-Henson A, Anderson L, Hemstreet MP, Bartholomew LK, Joseph CL et al (2006) Allergens in school settings: results of environmental assessments in 3 city school systems. J Sch Health 76(6):246–249PubMedPubMedCentralGoogle Scholar
  40. 40.
    Custovic A, Green R, Taggart SC, Smith A, Pickering CA, Chapman MD et al (1996) Domestic allergens in public places. II: dog (can f1) and cockroach (Bla g 2) allergens in dust and mite, cat, dog and cockroach allergens in the air in public buildings. Clin Exp Allergy 26(11):1246–1252PubMedPubMedCentralGoogle Scholar
  41. 41.
    Tortolero SR, Bartholomew LK, Tyrrell S, Abramson SL, Sockrider MM, Markham CM, Whitehead LW, Parcel GS (2002) Environmental allergens and irritants in schools: a focus on asthma. J Sch Health. 72(1):33–38PubMedPubMedCentralGoogle Scholar
  42. 42.
    2017–2018 APPA National Pet Owners Survey Statistics: pet ownership & annual expenses. Available from: http://americanpetproducts.org/press_industrytrends.asp. Accessed 18 Jan 2018
  43. 43.
    Ingram JM, Sporik R, Rose G, Honsinger R, Chapman MD, Platts-Mills TA (1995) Quantitative assessment of exposure to dog (can f 1) and cat (Fel d 1) allergens: relation to sensitization and asthma among children living in Los Alamos, New Mexico. J Allergy Clin Immunol 96(4):449–456PubMedPubMedCentralGoogle Scholar
  44. 44.
    Custovic A, Fletcher A, Pickering CA, Francis HC, Green R, Smith A et al (1998) Domestic allergens in public places III: house dust mite, cat, dog and cockroach allergens in British hospitals. Clin Exp Allergy 28(1):53–59PubMedPubMedCentralGoogle Scholar
  45. 45.
    De Lucca SD, O'Meara TJ, Tovey ER (2000) Exposure to mite and cat allergens on a range of clothing items at home and the transfer of cat allergen in the workplace. J Allergy Clin Immunol 106(5):874–879PubMedPubMedCentralGoogle Scholar
  46. 46.
    Karlsson AS, Renstrom A (2005) Human hair is a potential source of cat allergen contamination of ambient air. Allergy. 60(7):961–964PubMedPubMedCentralGoogle Scholar
  47. 47.
    Perzanowski MS, Ronmark E, James HR, Hedman L, Schuyler AJ, Bjerg A, Lundback B, Platts-Mills TAE (2016) Relevance of specific IgE antibody titer to the prevalence, severity, and persistence of asthma among 19-year-olds in northern Sweden. J Allergy Clin Immunol 138(6):1582–1590PubMedPubMedCentralGoogle Scholar
  48. 48.
    Salo PM, Sever ML, Zeldin DC (2009) Indoor allergens in school and day care environments. J Allergy Clin Immunol 124(2):185–92.e9PubMedPubMedCentralGoogle Scholar
  49. 49.
    Perzanowski MS, Ronmark E, Nold B, Lundback B, Platts-Mills TA (1999) Relevance of allergens from cats and dogs to asthma in the northernmost province of Sweden: schools as a major site of exposure. J Allergy Clin Immunol 103(6):1018–1024PubMedPubMedCentralGoogle Scholar
  50. 50.
    Krop EJ, Jacobs JH, Sander I, Raulf-Heimsoth M, Heederik DJ (2014) Allergens and beta-glucans in dutch homes and schools: characterizing airborne levels. PLoS One 9(2):e88871PubMedPubMedCentralGoogle Scholar
  51. 51.
    Almqvist C, Larsson PH, Egmar AC, Hedren M, Malmberg P, Wickman M (1999) School as a risk environment for children allergic to cats and a site for transfer of cat allergen to homes. J Allergy Clin Immunol 103(6):1012–1017PubMedPubMedCentralGoogle Scholar
  52. 52.
    Litonjua AA, Milton DK, Celedon JC, Ryan L, Weiss ST, Gold DR (2002) A longitudinal analysis of wheezing in young children: the independent effects of early life exposure to house dust endotoxin, allergens, and pets. J Allergy Clin Immunol 110(5):736–742PubMedPubMedCentralGoogle Scholar
  53. 53.
    Ownby DR, Johnson CC, Peterson EL (2002) Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age. JAMA. 288(8):963–972PubMedPubMedCentralGoogle Scholar
  54. 54.
    Bufford JD, Reardon CL, Li Z, Roberg KA, DaSilva D, Eggleston PA, Liu AH, Milton D, Alwis U, Gangnon R, Lemanske RF Jr, Gern JE (2008) Effects of dog ownership in early childhood on immune development and atopic diseases. Clin Exp Allergy 38(10):1635–1643PubMedPubMedCentralGoogle Scholar
  55. 55.
    Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, Becker AB, Scott JA, Kozyrskyj AL, CHILD Study Investigators (2013) Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol 9(1):15PubMedPubMedCentralGoogle Scholar
  56. 56.
    Kanchongkittiphon W, Mendell MJ, Gaffin JM, Wang G, Phipatanakul W (2015) Indoor environmental exposures and exacerbation of asthma: an update to the 2000 review by the Institute of Medicine. Environ Health Perspect 123(1):6–20PubMedPubMedCentralGoogle Scholar
  57. 57.
    Rud AG Jr, Beck AM (2003) Companion animals in Indiana elementary schools. Anthrozoös. 16(3):241–251Google Scholar
  58. 58.
    Association AH (2015) Pets in the classroom study: phase I findings report. Author Google Scholar, Washington, DCGoogle Scholar
  59. 59.
    Portnoy J, Miller JD, Williams PB, Chew GL, Miller JD, Zaitoun F, Phipatanakul W, Kennedy K, Barnes C, Grimes C, Larenas-Linnemann D, Sublett J, Bernstein D, Blessing-Moore J, Khan D, Lang D, Nicklas R, Oppenheimer J, Randolph C, Schuller D, Spector S, Tilles SA, Wallace D, Joint Taskforce on Practice Parameters, Practice Parameter Workgroup (2013) Environmental assessment and exposure control of dust mites: a practice parameter. Ann Allergy Asthma Immunol 111(6):465–507PubMedPubMedCentralGoogle Scholar
  60. 60.
    Arlian LG, Bernstein D, Bernstein IL, Friedman S, Grant A, Lieberman P, Lopez M, Metzger J, Platts-Mills T, Schatz M, Spector S, Wasserman SI, Zeiger RS (1992) Prevalence of dust mites in the homes of people with asthma living in eight different geographic areas of the United States. J Allergy Clin Immunol 90(3 Pt 1):292–300PubMedGoogle Scholar
  61. 61.
    Tovey ER, Willenborg CM, Crisafulli DA, Rimmer J, Marks GB (2013) Most personal exposure to house dust mite aeroallergen occurs during the day. PLoS One 8(7):e69900PubMedPubMedCentralGoogle Scholar
  62. 62.
    Platts-Mills TA, Vervloet D, Thomas WR, Aalberse RC, Chapman MD (1997) Indoor allergens and asthma: report of the Third International Workshop. J Allergy Clin Immunol 100(6 Pt 1):S2–S24Google Scholar
  63. 63.
    (1989) Dust mite allergens and asthma--a worldwide problem. J Allergy Clin Immunol 83(2 Pt 1):416–427Google Scholar
  64. 64.
    Einarsson R, Munir AK, Dreborg SK (1995) Allergens in school dust: II. Major mite (Der p I, Der f I) allergens in dust from Swedish schools. J Allergy Clin Immunol 95(5 Pt 1):1049–1053PubMedPubMedCentralGoogle Scholar
  65. 65.
    Zock JP, Brunekreef B (1995) House dust mite allergen levels in dust from schools with smooth and carpeted classroom floors. Clin Exp Allergy 25(6):549–553PubMedPubMedCentralGoogle Scholar
  66. 66.
    Fernandez-Caldas E, Codina R, Ledford DK, Trudeau WL, Lockey RF (2001) House dust mite, cat, and cockroach allergen concentrations in daycare centers in Tampa, Florida. Ann Allergy Asthma Immunol 87(3):196–200PubMedPubMedCentralGoogle Scholar
  67. 67.
    Fisk WJ, Lei-Gomez Q, Mendell MJ (2007) Meta-analyses of the associations of respiratory health effects with dampness and mold in homes. Indoor Air 17(4):284–296PubMedPubMedCentralGoogle Scholar
  68. 68.
    Gent JF, Kezik JM, Hill ME, Tsai E, Li D-W, Leaderer BP (2012) Household mold and dust allergens: exposure, sensitization and childhood asthma morbidity. Environ Res 118:86–93PubMedPubMedCentralGoogle Scholar
  69. 69.
    Karvonen AM, Hyvarinen A, Korppi M, Haverinen-Shaughnessy U, Renz H, Pfefferle PI, Remes S, Genuneit J, Pekkanen J (2015) Moisture damage and asthma: a birth cohort study. Pediatrics. 135(3):e598–e606PubMedPubMedCentralGoogle Scholar
  70. 70.
    Mendell MJ, Mirer AG, Cheung K, Tong M, Douwes J (2011) Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environ Health Perspect 119(6):748–756PubMedPubMedCentralGoogle Scholar
  71. 71.
    Quansah R, Jaakkola MS, Hugg TT, Heikkinen SAM, Jaakkola JJ (2012) Residential dampness and molds and the risk of developing asthma: a systematic review and meta-analysis. PLoS One 7(11):e47526PubMedPubMedCentralGoogle Scholar
  72. 72.
    Simoni M, Cai GH, Norback D, Annesi-Maesano I, Lavaud F, Sigsgaard T, Wieslander G, Nystad W, Canciani M, Viegi G, Sestini P (2011) Total viable molds and fungal DNA in classrooms and association with respiratory health and pulmonary function of European schoolchildren. Pediatr Allergy Immunol 22(8):843–852PubMedGoogle Scholar
  73. 73.
    Cavaleiro Rufo J, Madureira J, Paciencia I, Aguiar L, Pereira C, Silva D et al (2017) Indoor fungal diversity in primary schools may differently influence allergic sensitization and asthma in children. Pediatr Allergy Immunol 28(4):332–339PubMedPubMedCentralGoogle Scholar
  74. 74.
    Sauni R, Verbeek JH, Uitti J, Jauhiainen M, Kreiss K, Sigsgaard T (2015) Remediating buildings damaged by dampness and mould for preventing or reducing respiratory tract symptoms, infections and asthma. Cochrane Database Syst Rev (2):Cd007897Google Scholar
  75. 75.
    Gauderman WJ, Avol E, Gilliland F, Vora H, Thomas D, Berhane K, McConnell R, Kuenzli N, Lurmann F, Rappaport E, Margolis H, Bates D, Peters J (2004) The effect of air pollution on lung development from 10 to 18 years of age. N Engl J Med 351(11):1057–1067PubMedGoogle Scholar
  76. 76.
    Gauderman WJ, Urman R, Avol E, Berhane K, McConnell R, Rappaport E, Chang R, Lurmann F, Gilliland F (2015) Association of improved air quality with lung development in children. N Engl J Med 372(10):905–913PubMedPubMedCentralGoogle Scholar
  77. 77.
    Strickland MJ, Darrow LA, Klein M, Flanders WD, Sarnat JA, Waller LA, Sarnat SE, Mulholland JA, Tolbert PE (2010) Short-term associations between ambient air pollutants and pediatric asthma emergency department visits. Am J Respir Crit Care Med 182(3):307–316PubMedPubMedCentralGoogle Scholar
  78. 78.
    Silverman RA, Ito K (2010) Age-related association of fine particles and ozone with severe acute asthma in New York City. J Allergy Clin Immunol 125(2):367–73.e5PubMedGoogle Scholar
  79. 79.
    Organization WH (2005) Effects of air pollution on children's health and development: a review of the evidence.Google Scholar
  80. 80.
    World Health Organization. Effects of air pollution on children’s health and development. A review of the evidence. http://www.euro.who.int/en/health-topics/environment-and-health/airquality/publications/pre2009/effects-of-air-pollution-on-childrens-health-and-development-a-review-of-theevidence. Accessed 18 Jan 2018
  81. 81.
    Di Q, Wang Y, Zanobetti A, Wang Y, Koutrakis P, Choirat C et al (2017) Air pollution and mortality in the Medicare population. N Engl J Med 376(26):2513–2522PubMedPubMedCentralGoogle Scholar
  82. 82.
    Environmental Protection Agency. Criteria air pollutants. Available from: https://www.epa.gov/criteria-air-pollutants. Accessed 22 Jan 2018
  83. 83.
    Kingsley SL, Eliot MN, Carlson L, Finn J, MacIntosh DL, Suh HH et al (2014) Proximity of US schools to major roadways: a nationwide assessment. J Expo Sci Environ Epidemiol 24(3):253–259PubMedPubMedCentralGoogle Scholar
  84. 84.
    Hochstetler HA, Yermakov M, Reponen T, Ryan PH, Grinshpun SA (2011) Aerosol particles generated by diesel-powered school buses at urban schools as a source of children’s exposure. Atmos Environ (Oxford, England : 1994) 45(7):1444–1453Google Scholar
  85. 85.
    Annesi-Maesano I, Hulin M, Lavaud F, Raherison C, Kopferschmitt C, de Blay F, André Charpin D, Denis C (2012) Poor air quality in classrooms related to asthma and rhinitis in primary schoolchildren of the French 6 Cities Study. Thorax. 67(8):682–688PubMedPubMedCentralGoogle Scholar
  86. 86.
    Madureira J, Paciencia I, Pereira C, Teixeira JP, Fernandes Ede O (2016) Indoor air quality in Portuguese schools: levels and sources of pollutants. Indoor Air 26(4):526–537PubMedPubMedCentralGoogle Scholar
  87. 87.
    Gaffin JM, Petty CR, Hauptman M, Kang CM, Wolfson JM, Abu Awad Y, di Q, Lai PS, Sheehan WJ, Baxi S, Coull BA, Schwartz JD, Gold DR, Koutrakis P, Phipatanakul W (2017) Modeling indoor particulate exposures in inner-city school classrooms. J Expo Sci Environ Epidemiol. 27(5):451–457PubMedPubMedCentralGoogle Scholar
  88. 88.
    Pilotto LS, Nitschke M, Smith BJ, Pisaniello D, Ruffin RE, McElroy HJ, Martin J, Hiller JE (2004) Randomized controlled trial of unflued gas heater replacement on respiratory health of asthmatic schoolchildren. Int J Epidemiol 33(1):208–211PubMedPubMedCentralGoogle Scholar
  89. 89.
    Jhun I, Gaffin JM, Coull BA, Huffaker MF, Petty CR, Sheehan WJ et al (2017) School environmental intervention to reduce particulate pollutant exposures for children with asthma. J Allergy Clin Immunol Pract 5(1):154–9.e3PubMedPubMedCentralGoogle Scholar
  90. 90.
    Bernstein JA, Levin L, Crandall MS, Perez A, Lanphear B (2005) A pilot study to investigate the effects of combined dehumidification and HEPA filtration on dew point and airborne mold spore counts in day care centers. Indoor Air 15(6):402–407PubMedPubMedCentralGoogle Scholar
  91. 91.
    Lignell U, Meklin T, Putus T, Rintala H, Vepsalainen A, Kalliokoski P et al (2007) Effects of moisture damage and renovation on microbial conditions and pupils’ health in two schools--a longitudinal analysis of five years. J Environ Monit 9(3):225–233PubMedPubMedCentralGoogle Scholar
  92. 92.
    Meklin T, Potus T, Pekkanen J, Hyvarinen A, Hirvonen MR, Nevalainen A (2005) Effects of moisture-damage repairs on microbial exposure and symptoms in schoolchildren. Indoor Air 15(Suppl 10):40–47PubMedPubMedCentralGoogle Scholar
  93. 93.
    Karlsson AS, Andersson B, Renstrom A, Svedmyr J, Larsson K, Borres MP (2004) Airborne cat allergen reduction in classrooms that use special school clothing or ban pet ownership. J Allergy Clin Immunol 113(6):1172–1177PubMedPubMedCentralGoogle Scholar
  94. 94.
    Nalyanya G, Gore JC, Linker HM, Schal C (2009) German cockroach allergen levels in North Carolina schools: comparison of integrated pest management and conventional cockroach control. J Med Entomol 46(3):420–427PubMedPubMedCentralGoogle Scholar
  95. 95.
    Karlsson AS, Renstrom A, Hedren M, Larsson K (2004) Allergen avoidance does not alter airborne cat allergen levels in classrooms. Allergy. 59(6):661–667PubMedPubMedCentralGoogle Scholar
  96. 96.
    Sublett JL (2011) Effectiveness of air filters and air cleaners in allergic respiratory diseases: a review of the recent literature. Curr Allergy Asthma Rep 11(5):395–402PubMedPubMedCentralGoogle Scholar
  97. 97.
    Munir AK, Einarsson R, Schou C, Dreborg SK (1993) Allergens in school dust. I. the amount of the major cat (Fel d I) and dog (Can f I) allergens in dust from Swedish schools is high enough to probably cause perennial symptoms in most children with asthma who are sensitized to cat and dog. J Allergy Clin Immunol 91(5):1067–1074PubMedPubMedCentralGoogle Scholar
  98. 98.
    Chew GL, Burge HA, Dockery DW, Muilenberg ML, Weiss ST, Gold DR (1998) Limitations of a home characteristics questionnaire as a predictor of indoor allergen levels. Am J Respir Crit Care Med 157(5 Pt 1):1536–1541PubMedPubMedCentralGoogle Scholar
  99. 99.
    Dotterud LK, Van TD, Kvammen B, Dybendal T, Elsayed S, Falk ES (1997) Allergen content in dust from homes and schools in northern Norway in relation to sensitization and allergy symptoms in schoolchildren. Clin Exp Allergy 27(3):252–261PubMedPubMedCentralGoogle Scholar
  100. 100.
    Phipatanakul W, Koutrakis P, Coull BA, Kang CM, Wolfson JM, Ferguson ST, Petty CR, Samnaliev M, Cunningham A, Sheehan WJ, Gaffin JM, Baxi SN, Lai PS, Permaul P, Liang L, Thorne PS, Adamkiewicz G, Brennan KJ, Baccarelli AA, Gold DR (2017) The school inner-city asthma intervention study: design, rationale, methods, and lessons learned. Contemp Clin Trials 60:14–23PubMedPubMedCentralGoogle Scholar
  101. 101.
    Jassal MS, Diette GB, Dowdy DW (2013) Cost-consequence analysis of multimodal interventions with environmental components for pediatric asthma in the state of Maryland. J Asthma 50(6):672–680PubMedPubMedCentralGoogle Scholar
  102. 102.
    Abramson SL (2018) Reducing environmental allergic triggers: policy issues. J Allergy Clin Immunol Pract 6(1):32–35PubMedPubMedCentralGoogle Scholar
  103. 103.
    Indoor air quality tools for schools action kit. Available from: https://www.epa.gov/iaq-schools/indoor-air-quality-tools-schools-action-kit. Accessed 26 May 2018
  104. 104.
    US Environmental Protection Agency. EPA Environmental awardsGoogle Scholar
  105. 105.
    Centers for Disease Control and Prevention (CDC) Healthy schools program: managing asthma in schools. Available from: https://www.cdc.gov/healthyschools/asthma/index.htm. Accessed 26 May 2018
  106. 106.
    Lemanske RF Jr, Kakumanu S, Shanovich K, Antos N, Cloutier MM, Mazyck D, Phipatanakul W, Schantz S, Szefler S, Vandlik R, Williams P (2016) Creation and implementation of SAMPRO: a school-based asthma management program. J Allergy Clin Immunol 138(3):711–723PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of ImmunologyBoston Children’s HospitalBostonUSA
  2. 2.Harvard Medical SchoolBostonUSA
  3. 3.Division of Pediatric Allergy and ImmunologyWeil Cornell Medical CollegeNew YorkUSA
  4. 4.Allergy and Asthma Awareness Initiative, Inc.PeabodyUSA

Personalised recommendations