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International Archives of Occupational and Environmental Health

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01-08-2018 | Original Article

Biomarkers of respiratory allergy in laboratory animal care workers: an observational study

Authors: Federica Tafuro, Luisella Selis, Matteo Goldoni, Mariarita Stendardo, Paola Mozzoni, Erminia Ridolo, Piera Boschetto, Massimo Corradi

Published in: International Archives of Occupational and Environmental Health | Issue 6/2018

Abstract

Objectives

Laboratory animal allergy is a highly prevalent occupational disease among exposed workers. The aim of the study was to validate the biomarkers of airway inflammation in laboratory animal (LA) care workers.

Methods

All of the participants in this observational study (63 LA care workers and 64 controls) were administered a clinical questionnaire, underwent spirometry and a skin prick or radioallergosorbent test for common and occupational aeroallergens, and the fraction of exhaled nitric oxide (FeNO₅₀), exhaled breath condensate hydrogen peroxide (EBC H₂O₂) and serum pneumoprotein levels were measured. Multivariate analysis (ANCOVA) was used to assess the interactions of the variables.

Results

FeNO₅₀ levels correlated with exposure (p = 0.002), sensitisation (p = 0.000) and age (p = 0.001), but there was no interaction between exposure and sensitisation when age was considered in the model (p = 0.146). EBC-H₂O₂ levels were higher in the sensitised workers than in the sensitised controls [0.14 (0.08–0.29) µM vs 0.07 (0.05–0.12) µM; p < 0.05]. Serum surfactant protein A (SP-A) levels were unaffected by exposure, sensitisation or age, although higher levels were observed in symptomatic workers; however, SP-D levels were influenced by exposure (p = 0.024) and age (p = 0.022), and club cell 16 levels were influenced by sensitisation (p = 0.027) and age (p = 0.019).

Conclusions

The presence of the clinical symptoms associated with LA exposure and high FeNO levels should prompt further medical assessments in LA workers. Although EBC-H₂O₂ levels do not seem to reflect eosinophilic inflammation, serum SP-A levels could be used to monitor progression from rhinitis to asthma.

Adisesh LA, Kharitonov SA, Yates DH et al (1998) Exhaled and nasal nitric oxide is increased in laboratory animal allergy. Clin Exp Allergy 28(7):876–880CrossRef

Alving K, Weitzberg E, Lundberg JM (1993) Increased amount of nitric oxide in exhaled air of asthmatics. Eur Respir J 6(9):1368–1370

American Thoracic Society, European Respiratory Society (2005) 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 171:912–930CrossRef

Antunes J, Borrego L, Romeira A et al (2009) Skin prick tests and allergy diagnosis. Allergol Immunopathol (Madr) 37(3):155–164CrossRef

Aoyama K, Ueda A, Manda F et al (1992) Allergy to laboratory animals: an epidemiological study. Br J IndMed 49(1):41–47

Bauchau V, Durham SR (2004) Prevalence and rate of diagnosis of allergic rhinitis in Europe. Eur Respir J 24(5):758–764CrossRef

Benson M, Fransson M, Martinsson T et al (2007) Inverse relation between nasal fluid Clara cell protein 16 levels and symptoms and signs of rhinitis in allergen-challenged patients with intermittent allergic rhinitis. Allergy 62(2):178–183CrossRef

Broeckaert F, Arsalane K, Hermans C et al (2000) Serum clara cell protein: a sensitive biomarker of increased lung epithelium permeability caused by ambient ozone. Environ Health Perspect 108(6):533–537CrossRef

Bush RK (2001a) Mechanism and epidemiology of laboratory animal allergy. ILAR J 42(1):4–11CrossRef

Bush RK (2001b) Assessment and treatment of laboratory animal allergy. ILAR J 42(1):55–64CrossRef

Carbonnelle S, Francaux M, Doyle I et al (2002) Changes in serum pneumoproteins caused by short-term exposures to nitrogen trichloride in indoor chlorinated swimming pools. Biomarkers 7(6):464–478CrossRef

Chérot-Kornobis N, Hulo S, de Broucker V et al (2012) Induced sputum, exhaled NO, and breath condensate in occupational medicine. J Occup Environ Med 54(8):922–927CrossRef

Chow S, Campbell C, Sandrini A, Thomas PS, Johnson AR, Yates DH (2009) Exhaled breath condensate biomarkers in asbestos-related lung disorders. Respir Med 103(8):1091–1097CrossRef

Corradi M, Mutti A (2005) Exhaled breath analysis: from occupational to respiratory medicine. Acta Biomed 76(Suppl 2):20–29

Corradi M, Alinovi R, Goldoni M et al (2002) Biomarkers of oxidative stress after controlled human exposure to ozone. Toxicol Lett 134(1–3):219–225CrossRef

Corradi M, Gergelova P, Mutti A (2010) Use of exhaled breath condensate to investigate occupational lung diseases. Curr Opin Allergy Clin Immunol 10(2):93–98CrossRef

Corradi M, Romano C, Mutti A (2011) Laboratoryanimal; allergy; asthma. Med Lav 102(5):428–444

Corradi M, Gergelova P, Di Pilato E et al (2012) Effect of exposure to detergents and other chemicals on biomarkers of pulmonary response in exhaled breath from hospital cleaners: a pilot study. Int Arch Occup Environ Health 85(4):389–396CrossRef

Corradi M, Goldoni M, Mutti A (2015) A review on airway biomarkers: exposure, effect and susceptibility. Expert Rev Respir Med 6:1–16

Crouch EC (1998) Collectins and pulmonary host defense. Am J Respir Cell Mol Biol 19:177–201CrossRef

Cullinan P, Cook A, Nieuwenhuijsen MJ et al (2001) Allergen and dust exposure as determinants of work-related symptoms and sensitization in a cohort of flour-exposed workers; a case-control analysis. Ann Occup Hyg 45(2):97–103CrossRef

Dweik RA, Boggs PB, Erzurum SC et al, American Thoracic Society Committee on Interpretation of Exhaled Nitric Oxide Levels (FENO) for Clinical Applications (2011) An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med 184(5):602–615CrossRef

Erpenbeck VJ, Krug N, Hohlfeld JM (2009) Therapeutic use of surfactant components in allergic asthma. Naunyn Schmiedebergs Arch Pharmacol 379(3):217–224CrossRef

Fireman E, Lerman Y, Stark M et al (2008) Detection of occult lung impairment in welders by induced sputum particles and breath oxidation. Am J Ind Med 51(7):503–511CrossRef

Fisher AB, Dodia C, Ruckert P et al (2010) Pathway to lamellar bodies for surfactant protein A. Am J Physiol Lung Cell Mol Physiol 299(1):L51-8CrossRef

Gautrin D, Infante-Rivard C, Ghezzo H,et al (2001) Incidence and host determinants of probable occupational asthma in apprentices exposed to laboratory animals. Am J Respir Crit Care Med 163:899–904CrossRef

Greiner AN, Hellings PW, Rotiroti G et al (2011) Allergic rhinitis. Lancet 378(9809):2112–2122CrossRef

Gube M, Ebel J, Brand P et al (2010) Biological effect markers in exhaled breath condensate and biomonitoring in welders: impact of smoking and protection equipment. Int Arch Occup Environ Health 83(7):803–811CrossRef

Hermans C, Aly O, Nyberg BI et al (1998) Determinants of Clara cell protein (CC16) concentration in serum: a reassessment with two different immunoassays. Clin Chim Acta 272(2):101–110CrossRef

Hermans C, Dong P, Robin M et al (2003) Determinants of serum levels of surfactant proteins A and B and Clara cell protein CC16. Biomarkers 8(6):461–471CrossRef

Hollander A, Doekes G, Heederik D (1996) Cat and dog allergy and total IgE as risk factors of laboratory animal allergy. J Allergy Clin Immunol 98:545–554CrossRef

Horváth I, Donnelly LE, Kiss A et al (1998) Combined use of exhaled hydrogen peroxide and nitric oxide in monitoring asthma. Am J Respir Crit Care Med 158(4):1042–1046CrossRef

Horváth I, Hunt J, Barnes PJ et al (2005) ATS/ERS Task Force on Exhaled Breath Condensate. Exhaled breath condensate: methodological recommendations and unresolved questions. Eur Respir J 26(3):523–548CrossRef

Johansson S, Keen C, Ståhl A et al (2005) Low levels of CC16 in nasal fluid of children with birch pollen-induced rhinitis. Allergy 60(5):638–642CrossRef

Konradsen JR, Fujisawa T, van Hage M et al (2015) Allergy to furry animals: new insights, diagnostic approaches, and challenges. J Allergy Clin Immunol 135(3):616–625CrossRef

Krakowiak A, Wiszniewska M, Krawczyk P et al (2007) Risk factors associated with airway allergic diseases from exposure to laboratory animal allergens among veterinarians. Int Arch Occup Environ Health 80(6):465–475CrossRef

Kurowski M, Jurczyk J, Jarzębska M et al (2014) Association of serum Clara cell protein CC16 with respiratory infections and immune response to respiratory pathogens in elite athletes. Respir Res 15:45CrossRef

Lakind JS, Holgate ST, Ownby DR et al (2007) A critical review of the use of Clara cell secretory protein (CC-16) as a biomarker of acute or chronic pulmonary effects. Biomarkers 12(5):445–467CrossRef

LareseFilon F, Siracusa A, Rui F et al (2002) Prevalence of occupational allergy to laboratory animals in two towns of northern and central Italy. Med Lav 93(2):87–94

Laszlo G (2006) Standardisation of lung function testing: helpful guidance from the ATS/ERS Task Force. Thorax 61:744–746CrossRef

Ledford JG, Pastva AM, Wright JR. Review (2010) Collectins link innate and adaptive immunity in allergic airway disease. Innate Immun 16(3):183–190CrossRef

Ledford JG, Addison KJ, Foster MW et al (2014) Eosinophil-associated lung diseases. A cry for surfactant proteins A and D help? Am J Respir Cell Mol Biol 51(5):604–614CrossRef

Liccardi G, Bilò MB, Manzi F et al (2015) What could be the role of molecular-based allergy diagnostics in detecting the risk of developing allergic sensitization to furry animals? Eur Ann Allergy Clin Immunol 47(5):163–167

Linhares D, Jacinto T, Pereira AM et al (2011) Effects of atopy and rhinitison exhaled nitric oxide values—a systematic review. Clin Transl Allergy 1(1):8CrossRef

Madsen J, Tornoe I, Nielsen O et al (2003) Expression and localization of lung surfactant protein A in human tissues. Am J Respir Cell Mol Biol 29:591–597CrossRef

Mutti A, Corradi M, Goldoni M et al (2006) Exhaled metallic elements and serum pneumoproteins in asymptomatic smokers and patients with COPD or asthma. Chest 129(5):1288–1297CrossRef

National Institute for Occupational Safety and Health (NIOSH) (1998) NIOSH alert: preventing asthma in animal handlers. Publication no. 97-116

Olin AC, Alving K, Torén K (2004) Exhaled nitric oxide: relation to sensitization and respiratory symptoms. Clin Exp Allergy 34(2):221–226CrossRef

Pacheco KA, McCammon C, Liu AH et al (2003) Airborne endotoxin predicts symptoms in non-mouse-sensitized technicians and research scientists exposed to laboratory mice. Am J Respir Crit Care Med 167(7):983–990CrossRef

Palmberg L, Sundblad BM, Lindberg A et al (2015) Long term effect and allergic sensitization in newly employed workers in laboratory animal facilities. Respir Med 109(9):1164–1173CrossRef

Pellegrino R, Viegi G, Brusasco V et al (2005) Interpretative strategies for lung function tests. Eur Respir J 26(5):948–968CrossRef

Psathakis K, Mermigkis D, Papatheodorou G et al (2006) Exhaled markers of oxidative stress in idiopathic pulmonary fibrosis. Eur J Clin Investig 36(5):362–367CrossRef

Qaseem AS, Sonar S, Mahajan L et al (2013) Linking surfactant protein SP-D and IL-13: implications in asthma and allergy. Mol Immunol 54(1):98–107CrossRef

Quanjer PH, Stanojevic S, Cole TJ et al (2012) ERS Global Lung Function Initiative. Multi-ethnic reference values for spirometry for the 3–95-yr age range: theglobal lung function 2012 equations. Eur Respir J 40(6):1324–1343CrossRef

Ricciardolo FL, Sterk PJ, Gaston B et al (2004) Nitric oxide in health and disease of the respiratory system. Physiol Rev 84(3):731–765CrossRef

Ruoppi P, Koistinen T, Pennanen S (2005) Sensitisation to mites in laboratory animal workers with rhinitis. Occup Environ Med 62(9):612–615CrossRef

Seward JP (1999) Occupational allergy to animals. Occup Med 14(2):285–304

Shijubo N, Kawabata I, Sato N et al (2003) Clinical aspects of Clara cell 10-kDa protein/uteroglobin (secretoglobin 1A1). Curr Pharm Des 9(14):1139–1149CrossRef

Stolarek RA, Potargowicz E, Seklewska E et al (2010) Increased H₂O₂ level in exhaled breath condensate in primary breast cancer patients. J Cancer Res Clin Oncol 136(6):923–930CrossRef

Suarthana E, Meijer E, Heederik D et al (2009) The Dutch diagnostic model for laboratory animal allergen sensitization was generalizable in Canadian apprentices. J Clin Epidemiol 62:542–549CrossRef

Suresh V, Mih JD, George SC (2007) Measurement of IL-13-induced iNOS-derived gas phase nitric oxide in human bronchial epithelial cells. Am J Respir Cell Mol Biol 37(1):97–104CrossRef

Tafuro F, Ridolo E, Goldoni M et al (2015) Work-related allergies to storage mites in Parma (Italy) ham workers. BMJ Open 5(5):e007502CrossRef

Wolfle TL, Bush RK (2001) The science and pervasiveness of laboratory animal allergy. ILAR J 42(1):1–3CrossRef

Wood RA (2001) Laboratory animal allergens. ILAR J 42(1):12–16CrossRef

Ye Q, Fujita M, Ouchi H et al (2004) Serum CC-10 in inflammatory lung diseases. Respiration 71(5):505–510CrossRef

Title: Biomarkers of respiratory allergy in laboratory animal care workers: an observational study
Authors: Federica Tafuro
Luisella Selis
Matteo Goldoni
Mariarita Stendardo
Paola Mozzoni
Erminia Ridolo
Piera Boschetto
Massimo Corradi
Publication date: 01-08-2018
Publisher: Springer Berlin Heidelberg
Published in: International Archives of Occupational and Environmental Health / Issue 6/2018
Print ISSN: 0340-0131
Electronic ISSN: 1432-1246
DOI: https://doi.org/10.1007/s00420-018-1321-8

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Biomarkers of respiratory allergy in laboratory animal care workers: an observational study

Abstract

Objectives

Methods

Results

Conclusions

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Abstract

Objectives

Methods

Results

Conclusions

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