REVIEW URRENT C OPINION
Occupational allergy: respiratory hazards in healthcare workers Marta Wiszniewska and Jolanta Walusiak-Skorupa
Purpose of review Allergens are one group of respiratory hazards in the workplace of healthcare workers (HCWs). The purpose of this review is to summarize the recent advances in occupational allergy as well as potential hazardous agents in HCWs. Recent findings The review covers new developments on the epidemiology, diagnosis and management of occupational allergy in HCWs. This article also provides updated information on the prevalence of work-related respiratory symptoms, as well as on respiratory hazards among healthcare providers. Summary It is established that HCWs are at risk of asthma symptoms. The growing use of cleaning products is one of the causes of occupational airway disease in that group. Among healthcare professionals, the prevalence of asthma varies depending on worksite. Recent findings indicate a need for education among HCWs concerning occupational risks. A lack of knowledge of product components as well as about exposure to cleaning/disinfecting agents has been demonstrated. Further studies are necessary to determine the relative role of individual agents versus complex workplace exposures in the development of work-related asthma in HCWs. Keywords disinfectants, healthcare workers, latex, occupational allergy, respiratory hazards
INTRODUCTION
EPIDEMIOLOGY AND CAUSE
Healthcare workers (HCWs) are exposed to a great variety of respiratory hazards at work and consequently are at risk of occupational allergy. It is estimated that the healthcare industry is the fastest-growing sector of the U.S. economy employing over 18 million workers [1]; also, around 10% of all workers throughout the European Union are employed as HCWs [2]. Potential sensitizers in healthcare settings include latex, disinfectants and sterilants, medications, sensitizing metals, acrylates and cleaning products [3,4]. These main exposures, of which many include occupational allergens, are known to play a role in development of occupational allergic diseases such as rhinoconjunctivitis, bronchial asthma, urticaria, contact dermatitis as well as angioedema or anaphylaxis [5,6]. It is established that HCWs are at an increased risk of asthma symptoms [4,7,8]. The purpose of this study is to present advances from recently published articles concerning occupational allergy as well as respiratory hazards in HCWs.
Recently, in a survey among healthcare professionals, the prevalence of work-related asthma symptoms, work-exacerbated asthma (WEA) and occupational asthma was estimated at 3.3, 1.1 and 0.8%, respectively [9 ]. Natural rubber latex (NRL) became a major cause of occupational asthma in workers using NRL gloves in the 1990s. Large follow-up studies in HCWs showed glove-related symptoms in 21.8% of the nurses, including 2.3% with asthma and/or rhinitis [10]. The prevalence of latex sensitization ranged from 3 to 17% of HCWs [11–14]. Moreover, a metaanalysis concerning NRL allergy demonstrated its &
Department of Occupational Diseases and Clinical Toxicology, Nofer Institute of Occupational Medicine, Lodz, Poland Correspondence to Marta Wiszniewska, MD, PhD, Department of Occupational Diseases and Clinical Toxicology, Nofer Institute of Occupational Medicine, 8 Teresy St., 91-348 Lodz, Poland. Tel: +48 42 631 47 76; fax: +48 42 631 47 64; e-mail: [email protected] Curr Opin Allergy Clin Immunol 2014, 14:113–118 DOI:10.1097/ACI.0000000000000039
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Occupational disease
KEY POINTS Healthcare workers are at risk of work-related respiratory symptoms. Workplace exposure to cleaning agents is associated with the development of work-related asthma symptoms in HCWs. There is a need for education among HCWs concerning workplace exposure to respiratory hazards in the healthcare sector.
frequency at 4.32% of HCWs compared with 1.37% in the general population [15]. In addition, the prevalence of latex allergy in HCWs varied depending on conditions of exposure: it was demonstrated in 4.3% of HCWs using powdered latex gloves compared with 0.4% employees who used low-allergen or powder-free latex gloves [5]. A relatively high prevalence of symptoms and sensitization was observed in the study by Risenga et al. [16] in South Africa where glove-related symptoms were found in 37.1% HCWs, although the prevalence of latex allergy was 8.3%. Generally, there was a downward trend in the annual number of cases owing to the main causes of occupational asthma (i.e. flour, isocyanates, woods and enzymes) but an apparent increase in cases of latex-induced occupational asthma as reported from Belgium in the years 1993–2002 [17]. On the contrary, a low number of occupational asthma claims due to NRL were reported among HCWs in a Canadian province from 1998 to 2002, which further illustrates the successful example of the primary prevention intervention there involving the introduction of nonpowdered, low-protein NRL gloves and nonlatex gloves [18]. A recent French study [19 ] even demonstrated no significant relationship between the use of latex gloves and reported newonset asthma probably as a result of preventive measures in healthcare settings. Nevertheless, occupational asthma among HCWs is not only latex-induced. In recent studies [4,19 ,20,21] concerning asthma prevalence among HCWs, it has been estimated that the prevalence of new-onset asthma ranged from about 6 to 10% depending on the job, although the prevalence of atopic and nonatopic asthma among dental HCWs was observed in 6.9 and 5.9% individuals, respectively [22]. A lower prevalence of 4.0% was demonstrated for WEA in dental HCWs [22]. In addition, the reported prevalence of asthma varies depending on worksite and was significantly higher among nursing professionals involved in medical instrument cleaning and exposure to cleaning products &&
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and disinfectants [21]. The study by Delclos et al. [4] reported that asthma was associated with medical instrument cleaning, general cleaning, use of powdered latex gloves between 1992 and 2000, and administration of aerosolized medications. Symptoms of bronchial hyperresponsiveness were associated with general cleaning, aerosolized medication administration, use of adhesives on patients and exposure to a chemical spill [4]. In a US population, HCWs work-related asthma was mainly reported among hospital nurses and was linked to cleaning products and latex exposures [3]. Also, operating room nurses have been identified as one of the highest exposed groups to disinfectant/ cleaning agents as compared with those working in other hospital units [23]. Occupational exposure to disinfecting/cleaning agents is common and high in hospitals, although among HCWs self-reported exposure underestimated likely exposures, especially for formaldehyde, ammonia, alcohol and quaternary ammonium components, compared with expert assessment [23]. There are other sensitizers in healthcare settings that should be mentioned, such as isocyanates in orthopaedic clinics. Suojalehto et al. [24] presented two cases of asthma due to methylene diphenyl diisocyanate (MDI) containing orthopaedic plaster casts in nurses, confirmed with placebocontrolled specific inhalation challenge and workplace measurements of MDI. Also, exposure to inhaled medications such as psillium, antibiotics, pentamidine as well as acrylates may lead to occupational allergies in HCWs [25]. It was proved that the risk of asthma, nasal symptoms and cough increased significantly with daily use of methacrylates in dental assistants’ work [26].
DIAGNOSIS Tools for the diagnosis of occupational allergic respiratory diseases include the medical history and examination, immunologic testing, pulmonary function studies and bronchial provocation challenge [27]. The clinical history is the first important part of diagnostic process and it is regarded as a sensitive method, but with a low specificity [28]. Information about potential respiratory hazards can be also obtained from the material safety data sheets. The assessment of sensitization, with skin prick tests (SPT) and/or specific IgE measurement, is the next important stage in diagnosis of occupational allergy. SPT with an extract of NRL has a high sensitivity (100%) but a low specificity (20%) [29]. SPT is very useful to detect IgE-mediated sensitization to NRL, but it is not as useful in confirming the Volume 14 Number 2 April 2014
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Occupational allergy Wiszniewska and Walusiak-Skorupa
diagnosis of NRL-induced occupational asthma, because 30% of the individuals with positive SPT results had negative challenge results [29]. On the contrary, a negative SPT result with a reliable NRL extract is very useful to rule out NRL-induced occupational asthma [29]. Bronchial challenges can be performed by exposing the patient to the work environment with measurement of pulmonary functions before and after exposure. Confirmation of work-relatedness of occupational asthma should include serial monitoring of peak expiratory flow for periods at work and off work [30] or/and serial measurements of nonspecific bronchial hyperresponsiveness (NSBH), as NSBH is typically worse after a period of exposure and can decrease after cessation of exposure. The nonspecific bronchoprovocation with methacholine is highly sensitive but not specific for occupational asthma [31,32]. It is also possible to perform specific inhalation challenge tests (SICTs) and these are established as the ‘gold standard’ or reference test in the diagnosis of occupational asthma [28]. On the contrary, SICT requires specialized equipment and is only performed in selected centres.
MANAGEMENT AND PREVENTION Preventing respiratory sensitization in healthcare settings includes assessment of the risk by identifying the hazards, avoiding the exposure to allergenic agents by substituting them with less dangerous substances as well minimizing the exposure concentration, time, frequency and number of workers exposed. Avoidance of NRL exposure is the primary goal for preventing sensitization. If possible, powdered latex gloves should be substituted with low-protein, powder-free latex or nitrile gloves [33 ]. The effectiveness of primary preventive strategies in healthcare settings has been demonstrated, as reduction of exposure to latex in hospitals has resulted in a significant decrease in latex-induced allergy [34,35]. Also, a follow-up study [10] among HCWs revealed that avoidance of unnecessary glove use, the use of nonpowdered latex gloves by all workers and of nonlatex gloves by sensitized ones can stop the progression of latex symptoms and incidence of new cases. On the contrary, the reduction of exposure to latex represents a reasonably well tolerated alternative that should be considered in workers with latex-induced occupational asthma when complete avoidance of exposure is not feasible or when the possibilities for nonexposed jobs are limited. Compared with complete removal, reduction of exposure &&
is associated with a substantially lower socioeconomic impact [36].
RECENT FINDINGS It is suggested that the growing use of aerosolized cleaning products increases respiratory tract exposure to the irritant and/or sensitizing agents present in these products, also resulting in occupational airway disease in HCWs (Table 1). Laborde-Caste´rot et al. [37] have reported cases of work-related asthma and/or rhinitis due to EDTA sodium aqueous solutions confirmed by positive nasal provocation tests. In healthcare professionals, the exposure to EDTA-containing products occurs in disinfectants. The authors suggest an immunoallergic response or pharmacological mechanism rather than an irritant one as the explanation of respiratory symptoms induced by inhalation of EDTA [37]. Adisesh et al. [38] described two cases of occupational asthma and four other cases of possible occupational asthma/rhinitis associated with the use of detergent enzymes for cleaning medical instruments. It was emphasized that detergent enzymes when used in healthcare settings should be recognized as potential respiratory sensitizers [38]. In a recent study, Gonzalez et al. [19 ] analysed the associations between asthma and occupational exposure to disinfectants, especially to quaternary ammonium compounds (QACs). The authors found that HCWs, particularly nursing professionals, presented an increased risk of reported physiciandiagnosed asthma and nasal symptoms at work compared with administrative staff working in healthcare sector. Among the various tasks performed, disinfection was associated with a higher risk than simple cleaning. This study highlighted the relation between reported asthma or nasal symptoms at work and the presence of QACs in the products used. The authors emphasized that workplace interventions and training programmes should be conducted to warn workers about the risks, to ensure better protection against QAC exposure and to improve disinfection procedures, especially for nurses [19 ]. In addition to the recent interest by investigators in cleaning agents as an important cause in HCWs asthma, there was special attention paid to WEA. Liss et al. [18] found that healthcare was the most frequent industry for WEA and the rate of WEA claims was 2.1 times greater than that in the rest of the workforce. There was a broad variety of agents to which the WEA cases were attributed, for example cleaning agents, bleaches, fresheners,
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construction/renovation dust, paint fumes, secondhand smoke, perfume and moulds [18]. Arif and Delclos [9 ] reported adverse respiratory health effects among HCWs using cleaning-related chemicals. They found that workplace exposures to cleaning agents were associated with the development of work-related asthma symptoms, WEA and/or occupational asthma among healthcare professionals. For example, WEA was significantly related to exposure to bleach, glutaraldehyde, ortho-phthalaldehyde, chloramines, ethylene oxide and formalin/formaldehyde, although the odds of occupational asthma were almost five-fold elevated for chloramines [9 ]. Walters et al. [39] investigated the causes and trends over time of occupational asthma in HCWs. The majority of cases of occupational asthma (75%) occurred in nursing, operating theatre, endoscopy and radiology staff, although the most frequently implicated agents (79% cases) were glutaraldehyde, latex and cleaning products. Their finding that notifications of occupational asthma in UK HCWs declined, due principally to a reduction in the number of cases of latex and glutaraldehyde-related occupational asthma, is in line with current trends observed in Europe and U.S. However, there was an increase in occupational asthma notifications due to cleaning products, so control strategies should be sought to limit such exposure [39]. Singh et al. [22] investigated the prevalence of asthma phenotypes in dental HCWs and associated risk factors. They found that atopy and work-related ocular-nasal symptoms were strong predictors of WEA. Regular use of personal protective equipment was associated with a protective effect among nonatopic asthmatic individuals, whereas glove use and respiratory protection reduced risk among atopic asthmatic individuals. It has been pointed out that sensitivity to drug allergens is more common in HCWs than in the general population. The prevalence of self-reported drug allergy among HCWs was estimated as 16.2%. At surgical departments, nurses reported allergy symptoms more frequently than doctors and nurses from medicine departments. Antibiotics and local anaesthetics were the most common medications reported to cause symptoms. In addition, sensitivity to drugs increased with duration of employment at the hospital [40]. Kim et al. [41] reported 17.4% prevalence of work-related symptoms due to cephalosporins. The sensitization rate to any cephalosporin defined by SPT was 3.1% and considerably higher when determined by measurement of serum-specific IgE antibodies: 17.4% for any cephalosporin, 10.4% for cefotiam, 6.8% for ceftriaxone and 3.7% for &
EDTA, ethylenediamine tetraacetic acid; HCWs, healthcare workers; OA, occupational asthma; SICT, specific inhalation challenge test; sIgE, specific IgE; QACs, quaternary ammonium compounds.
Cleaning product-related OA was an emerging cause with 22 cases after 2001 and only 5 cases between 1991 and 2000. 75% of cases involved nursing, operating theatre, endoscopy and radiology staff Data on sensitizing agents from electronic database 182 notifications of OA in HCWs Notifications for 21 years from the SHIELD electronic database Walters, 2013 [39]
Serial peak-flow measurements, sIgE, SICT
Significantly elevated odds of WEA for exposure to bleach, glutaraldehyde/ortho-phthalaldehyde, chloramines and ethylene oxide and formalin/formaldehyde. Exposure to chloramines was significantly associated with OA A detailed history of the job using the questionnaire &
5600 HCWs, aged 45.3 years Population-based survey Arif, 2012 [9 ]
Questionnaire
Exposure to QACs increased significantly the risk of reported physician-diagnosed asthma and nasal symptoms at work (OR ¼ 7.5 and 3.2, respectively) Work questionnaire, workplace studies, review of products ingredients 543 HCWs, aged 18–65 years Cross-sectional study Gonzalez, 2013 && [19 ]
Self-administered questionnaire, physical examination
10 published cases of occupational asthma and/or rhinitis in patients exposed to EDTA-containing products 0.1 ml of an aqueous solution of EDTA Non-specific bronchial hyperreactivity 28 patients (cleaners or HCWs) Series of cases Laborde-Caste´rot, 2012 [37]
Study population Study design First author, year
Table 1. Recent studies on HCWs and cleaning products asthma
Assessment of asthma
Assessment of exposure
Results
Occupational disease
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ceftizoxime. A personal history of any antibiotic allergy was a risk factor for work-related symptoms, but not for the presence of specific IgE to cephalosporins [41]. A recent survey concerning the level of knowledge among HCWs of latex gloves and NRL allergy, routine prevention practice and appropriate use of gloves in patient care revealed that most HCWs are aware of the different types of gloves, but only 1% of them were able to correctly match the appropriate gloves to the specifically designed procedure. Around 74.5% HCWs were unable to recognize the presentation of NRL allergy and only 12% of them were aware of rubber accelerators as potential allergens in latex gloves. These data indicate that there is a need for education among HCWs about gloves and NRL allergy [42]. The association between worksite and the level of asthma severity/control has also been analysed. Le Moual et al. [43] observed a significant association between operating room nursing, compared with administrative nursing, and severe persistent asthma. The study [43] confirmed the hypothesis that working as an operating room nurse may induce more severe asthma or worsen asthma control. The first Chinese epidemiological survey performed among nurses revealed an 8.8% prevalence of at least one symptom associated with the latex gloves use. Among symptomatic nurses, 77.1 and 63.9% reported in questionnaire symptoms suggesting glove dermatitis and type I latex allergy (urticaria, rhinorrhoea, or chest tightness/dyspnoea occurring within 2 h of glove use), respectively. They report that employment seniority, positive history of allergic diseases and longer extent of time spent in a single hospital room were associated with reporting symptoms suggestive of type I latex allergy, although using more than five pairs of gloves per working day may be a protective factor [44]. Some aspects of the diagnosis of IgE-mediated occupational allergic diseases were also investigated. The results of serologic testing for latex-specific IgE demonstrated 35% sensitivity and 98% specificity for the CAP and ELISA assays. The performance of the FDA-cleared IgE serologic test for latex allergy has much lower sensitivity than previously reported. This finding confirms that this serologic test should be used only for patients with a history of latex allergy and not for screening a population with a low prevalence of latex sensitization [45]. In-vitro analysis of the NRL SPT solutions demonstrated high variability among different manufacturers. The protein content varied between below detection limit (Stallergenes, Lofarma, Milan, Italy) to 65 mg/ml (Allerbio, Varennes-en-Argonne,
France), although allergen content ranged from 0.6 (Lofarma) to 11.7 mg/ml (Allergopharma, Reinbek, Germany) [46]. A systematic review of the management of latex allergy demonstrated moderately strong and consistent evidence that avoidance of NRL in the workplace reduces both symptoms and markers of sensitization in latex-allergic individuals [47].
CONCLUSION In recent years, healthcare personnel have received particular attention as being at risk for occupational respiratory diseases. Some studies have confirmed an increased risk of occupational asthma and cleaning agents are currently the major respiratory hazards. An immunologic mechanism for occupational asthma due to cleaning products is suggested, but not definitely demonstrated. Large underestimation of self-reported exposure to cleaning/disinfecting agents as well as a lack of knowledge of product components has been observed among HCWs. The need for health education programmes on the occupational risks induced by these types of products is stressed [23]. Further studies are necessary to determine the relative role of individual versus complex workplace exposure in the development of the respiratory work-related diseases in HCWs. Acknowledgements None. Conflicts of interest The authors declare that they have no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. National Institute for Occupational Safety and Health (NIOSH), Centers for Disease Control and Prevention. Healthcare workers. http://www.cdc.gov/ niosh/topics/healthcare. [Accessed 1 November 2013] 2. The European Agency for Safety and Health at Work. Health and safety of healthcare staff. https://osha.europa.eu/en/sector/healthcare. [Accessed 1 November 2013] 3. Pechter E, Davis LK, Tumpowsky C, et al. Work-related asthma among healthcare workers: surveillance data from California, Massachusetts, Michigan, and New Jersey, 1993–1997. Am J Ind Med 2005; 47:265–275. 4. Delclos GL, Gimeno D, Arif AA, et al. Occupational risk factors and asthma among healthcare professionals. Am J Respir Crit Care Med 2007; 175:667– 675. 5. O’Hehir R, Sutherland M, Drew A, Rolland J. Latex allergy. In: Kay A, Kaplan A, Bousquet J, Holt P, editors. Allergy and allergic diseases, 2nd ed. WileyBlackwell; 2008. pp. 1164–1184. 6. Siracusa A, De Blay F, Folletti I, et al. Asthma and exposure to cleaning products: a European Academy of Allergy and Clinical Immunology task force consensus statement. Allergy 2013. [Epub ahead of print] 7. Fishwick D, Barber CM, Bradshaw LM, et al. Standards of care for occupational asthma: an update. Thorax 2012; 67:278–280.
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Occupational disease 8. McHugh MK, Symanski E, Pompeii LA, Delclos GL. Prevalence of asthma by industry and occupation in the U.S. working population. Am J Ind Med 2010; 53:463–475. 9. Arif AA, Delclos GL. Association between cleaning-related chemicals and & work-related asthma and asthma symptoms among healthcare professionals. Occup Environ Med 2012; 69:35–40. An interesting study concerning relationship between work-related exposure to cleaning-related chemicals and development of WRA among HCWs. 10. Filon FL, Radman G. Latex allergy: a follow up study of 1040 healthcare workers. Occup Environ Med 2006; 63:121–125. 11. Liss G, Sussman G, Deal K, et al. Latex allergy: epidemiological study of 1351 hospital workers. Occup Environ Med 1997; 54:335–342. 12. Yassin MS, Lierl M, Fisher T, et al. Latex allergy in hospital employees. Ann Allergy 1994; 72:245–249. 13. Vila L, Sa´nchez G, An˜o M, et al. Risk factors for latex sensitization among healthcare workers. J Investig Allergol Clin Immunol 1999; 9:356–360. 14. Sussman GL, Liss GM, Deal K, et al. Incidence of latex sensitization among latex glove users. J Allergy Clin Immunol 1998; 101 (2 Pt 1):171–178. 15. Bousquet J, Flahault A, Vandenplas O, et al. Natural rubber latex allergy among healthcare workers: a systematic review of the evidence. J Allergy Clin Immunol 2006; 118:447–454. 16. Risenga SM, Shivambu GP, Rakgole MP, et al. Latex allergy and its clinical features among healthcare workers at Mankweng Hospital, Limpopo Province, South Africa. S Afr Med J 2013; 103:390–394. 17. Vandenplas O, Lantin AC, D’Alpaos V, et al. Time trends in occupational asthma in Belgium. Respir Med 2011; 105:1364–1372. 18. Liss GM, Buyantseva L, Luce CE, et al. Work-related asthma in healthcare in Ontario. Am J Ind Med 2011; 54:278–284. 19. Gonzalez M, Je´gu J, Kopferschmitt MC, et al. Asthma among workers in && healthcare settings: role of disinfection with quaternary ammonium compounds. Clin Exp Allergy 2013. [Epub ahead of print] The study analysed the associations between asthma and occupational exposure to disinfectants, especially QACs. The study demonstrates that exposure to QACs increased significantly the risk of reported physician-diagnosed asthma and nasal symptoms at work. 20. Mirabelli MC, Zock J-P, Plana E, et al. Occupational risk factors for asthma among nurses and related healthcare professionals in an international study. Occup Environ Med 2007; 64:474–479. 21. Arif AA, Delclos GL, Serra C. Occupational exposures and asthma among nursing professionals. Occup Environ Med 2009; 66:274–278. 22. Singh T, Bello B, Jeebhay MF. Risk factors associated with asthma phenotypes in dental healthcare workers. Am J Ind Med 2013; 56:90–99. 23. Donnay C, Denis MA, Magis R, et al. Under-estimation of self-reported occupational exposure by questionnaire in hospital workers. Occup Environ Med 2011; 68:611–617. 24. Suojalehto H, Linstro¨m I, Henriks-Eckerman ML, et al. Occupational asthma related to low levels of airborne methylene diphenyl diisocyanate (MDI) in orthopedic casting work. Am J Ind Med 2011; 54:906–910. 25. Piirila¨ P, Hodgson U, Estlander T, et al. Occupational respiratory hypersensitivity in dental personnel. Int Arch Occup Environ Health 2002; 75:209–216. 26. Jaakkola MS, Leino T, Tammilehto L, et al. Respiratory effects of exposure to methacrylates among dental assistants. Allergy 2007; 62:648–654. 27. Tarlo SM, Balmes J, Balkissoon R, et al. Diagnosis and management of workrelated asthma: American College Of Chest Physicians Consensus Statement. Chest 2008; 134 (Suppl 3):1–41.
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www.co-allergy.com
28. Moscato G, Malo JL, Bernstein D. Diagnosing occupational asthma: how, how much, how far? Eur Resp J 2003; 21:879–885. 29. Quirce S, Swanson MC, Ferna´ndez-Nieto M, et al. Quantified environmental challenge with absorbable dusting powder aerosol from natural rubber latex gloves. J Allergy Clin Immunol 2003; 111:788–794. 30. Tarlo SM, Liss GM. Occupational asthma: an approach to diagnosis and management. CMAJ 2003; 168:867–871. 31. Sabin BR, Grammer LC. Chapter 17: occupational immunologic lung disease. Allergy Asthma Proc 2012; 33 (Suppl 1):58–60. 32. Cowl CT. Occupational asthma: review of assessment, treatment, and compensation. Chest 2011; 139:674–681. 33. Heederik D, Henneberger PK, Redlich CA, ERS Task Force on the Manage&& ment of Work-related Asthma. Primary prevention: exposure reduction, skin exposure and respiratory protection. Eur Respir Rev 2012; 21:112–124. A good summary of the impact of controlling work exposure on the prevention of occupational asthma. 34. Allmers H, Schmengler J, Skudlik C. Primary prevention of natural rubber latex allergy in the German healthcare system through education and intervention. J Allergy Clin Immunol 2002; 110:318–323. 35. Allmers H, Schmengler J, John SM. Decreasing incidence of occupational contact urticaria caused by natural rubber latex allergy in German healthcare workers. J Allergy Clin Immunol 2004; 114:347–351. 36. Vandenplas O, Jamart J, Delwiche JP, et al. Occupational asthma caused by natural rubber latex: outcome according to cessation or reduction of exposure. J Allergy Clin Immunol 2002; 109:125–130. 37. Laborde-Caste´rot H, Villa AF, Rosenberg N, et al. Occupational rhinitis and asthma due to EDTA-containing detergents or disinfectants. Am J Ind Med 2012; 55:677–682. 38. Adisesh A, Murphy E, Barber CM, Ayres JG. Occupational asthma and rhinitis due to detergent enzymes in healthcare. Occup Med (Lond) 2011; 61:364– 369. 39. Walters GI, Moore VC, McGrath EE, et al. Agents and trends in healthcare workers’ occupational asthma. Occup Med (Lond) 2013; 63:513–516. 40. Zilinskaite L, Tamasauskas D, Kvedariene V, Sitkauskiene B. Self-reported drug allergy in healthcare workers in conservative and surgical medicine departments. J Investig Allergol Clin Immunol 2012; 22:357–362. 41. Kim JE, Kim SH, Jin HJ, et al. IgE sensitization to cephalosporins in healthcare workers. Allergy Asthma Immunol Res 2012; 4:85–91. 42. Al-Niaimi F, Chiang YZ, Chiang YN, Williams J. Latex allergy: assessment of knowledge, appropriate use of gloves and prevention practice among hospital healthcare workers. Clin Exp Dermatol 2013; 38:77–80. 43. Le Moual N, Varraso R, Zock JP, et al. Are operating room nurses at higher risk of severe persistent asthma? The Nurses’ Health Study. J Occup Environ Med 2013; 55:973–977. 44. Liu QL, He XZ, Liang K, et al. Prevalence and risk factors for latex glove allergy among female clinical nurses: a multicenter questionnaire study in China. Int J Occup Environ Health 2013; 19:29–34. 45. Accetta Pedersen DJ, Klancnik M, Elms N, et al. Analysis of available diagnostic tests for latex sensitization in an at-risk population. Ann Allergy Asthma Immunol 2012; 108:94–97. 46. van Kampen V, de Blay F, Folletti I, et al. Evaluation of commercial skin prick test solutions for selected occupational allergens. Allergy 2013; 68:651– 658. 47. Madan I, Cullinan P, Ahmed SM. Occupational management of type I latex allergy. Occup Med (Lond) 2013; 63:395–404.
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Occupational allergy: respiratory hazards in healthcare workers Marta Wiszniewska and Jolanta Walusiak-Skorupa
Purpose of review Allergens are one group of respiratory hazards in the workplace of healthcare workers (HCWs). The purpose of this review is to summarize the recent advances in occupational allergy as well as potential hazardous agents in HCWs. Recent findings The review covers new developments on the epidemiology, diagnosis and management of occupational allergy in HCWs. This article also provides updated information on the prevalence of work-related respiratory symptoms, as well as on respiratory hazards among healthcare providers. Summary It is established that HCWs are at risk of asthma symptoms. The growing use of cleaning products is one of the causes of occupational airway disease in that group. Among healthcare professionals, the prevalence of asthma varies depending on worksite. Recent findings indicate a need for education among HCWs concerning occupational risks. A lack of knowledge of product components as well as about exposure to cleaning/disinfecting agents has been demonstrated. Further studies are necessary to determine the relative role of individual agents versus complex workplace exposures in the development of work-related asthma in HCWs. Keywords disinfectants, healthcare workers, latex, occupational allergy, respiratory hazards
INTRODUCTION
EPIDEMIOLOGY AND CAUSE
Healthcare workers (HCWs) are exposed to a great variety of respiratory hazards at work and consequently are at risk of occupational allergy. It is estimated that the healthcare industry is the fastest-growing sector of the U.S. economy employing over 18 million workers [1]; also, around 10% of all workers throughout the European Union are employed as HCWs [2]. Potential sensitizers in healthcare settings include latex, disinfectants and sterilants, medications, sensitizing metals, acrylates and cleaning products [3,4]. These main exposures, of which many include occupational allergens, are known to play a role in development of occupational allergic diseases such as rhinoconjunctivitis, bronchial asthma, urticaria, contact dermatitis as well as angioedema or anaphylaxis [5,6]. It is established that HCWs are at an increased risk of asthma symptoms [4,7,8]. The purpose of this study is to present advances from recently published articles concerning occupational allergy as well as respiratory hazards in HCWs.
Recently, in a survey among healthcare professionals, the prevalence of work-related asthma symptoms, work-exacerbated asthma (WEA) and occupational asthma was estimated at 3.3, 1.1 and 0.8%, respectively [9 ]. Natural rubber latex (NRL) became a major cause of occupational asthma in workers using NRL gloves in the 1990s. Large follow-up studies in HCWs showed glove-related symptoms in 21.8% of the nurses, including 2.3% with asthma and/or rhinitis [10]. The prevalence of latex sensitization ranged from 3 to 17% of HCWs [11–14]. Moreover, a metaanalysis concerning NRL allergy demonstrated its &
Department of Occupational Diseases and Clinical Toxicology, Nofer Institute of Occupational Medicine, Lodz, Poland Correspondence to Marta Wiszniewska, MD, PhD, Department of Occupational Diseases and Clinical Toxicology, Nofer Institute of Occupational Medicine, 8 Teresy St., 91-348 Lodz, Poland. Tel: +48 42 631 47 76; fax: +48 42 631 47 64; e-mail: [email protected] Curr Opin Allergy Clin Immunol 2014, 14:113–118 DOI:10.1097/ACI.0000000000000039
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Occupational disease
KEY POINTS Healthcare workers are at risk of work-related respiratory symptoms. Workplace exposure to cleaning agents is associated with the development of work-related asthma symptoms in HCWs. There is a need for education among HCWs concerning workplace exposure to respiratory hazards in the healthcare sector.
frequency at 4.32% of HCWs compared with 1.37% in the general population [15]. In addition, the prevalence of latex allergy in HCWs varied depending on conditions of exposure: it was demonstrated in 4.3% of HCWs using powdered latex gloves compared with 0.4% employees who used low-allergen or powder-free latex gloves [5]. A relatively high prevalence of symptoms and sensitization was observed in the study by Risenga et al. [16] in South Africa where glove-related symptoms were found in 37.1% HCWs, although the prevalence of latex allergy was 8.3%. Generally, there was a downward trend in the annual number of cases owing to the main causes of occupational asthma (i.e. flour, isocyanates, woods and enzymes) but an apparent increase in cases of latex-induced occupational asthma as reported from Belgium in the years 1993–2002 [17]. On the contrary, a low number of occupational asthma claims due to NRL were reported among HCWs in a Canadian province from 1998 to 2002, which further illustrates the successful example of the primary prevention intervention there involving the introduction of nonpowdered, low-protein NRL gloves and nonlatex gloves [18]. A recent French study [19 ] even demonstrated no significant relationship between the use of latex gloves and reported newonset asthma probably as a result of preventive measures in healthcare settings. Nevertheless, occupational asthma among HCWs is not only latex-induced. In recent studies [4,19 ,20,21] concerning asthma prevalence among HCWs, it has been estimated that the prevalence of new-onset asthma ranged from about 6 to 10% depending on the job, although the prevalence of atopic and nonatopic asthma among dental HCWs was observed in 6.9 and 5.9% individuals, respectively [22]. A lower prevalence of 4.0% was demonstrated for WEA in dental HCWs [22]. In addition, the reported prevalence of asthma varies depending on worksite and was significantly higher among nursing professionals involved in medical instrument cleaning and exposure to cleaning products &&
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and disinfectants [21]. The study by Delclos et al. [4] reported that asthma was associated with medical instrument cleaning, general cleaning, use of powdered latex gloves between 1992 and 2000, and administration of aerosolized medications. Symptoms of bronchial hyperresponsiveness were associated with general cleaning, aerosolized medication administration, use of adhesives on patients and exposure to a chemical spill [4]. In a US population, HCWs work-related asthma was mainly reported among hospital nurses and was linked to cleaning products and latex exposures [3]. Also, operating room nurses have been identified as one of the highest exposed groups to disinfectant/ cleaning agents as compared with those working in other hospital units [23]. Occupational exposure to disinfecting/cleaning agents is common and high in hospitals, although among HCWs self-reported exposure underestimated likely exposures, especially for formaldehyde, ammonia, alcohol and quaternary ammonium components, compared with expert assessment [23]. There are other sensitizers in healthcare settings that should be mentioned, such as isocyanates in orthopaedic clinics. Suojalehto et al. [24] presented two cases of asthma due to methylene diphenyl diisocyanate (MDI) containing orthopaedic plaster casts in nurses, confirmed with placebocontrolled specific inhalation challenge and workplace measurements of MDI. Also, exposure to inhaled medications such as psillium, antibiotics, pentamidine as well as acrylates may lead to occupational allergies in HCWs [25]. It was proved that the risk of asthma, nasal symptoms and cough increased significantly with daily use of methacrylates in dental assistants’ work [26].
DIAGNOSIS Tools for the diagnosis of occupational allergic respiratory diseases include the medical history and examination, immunologic testing, pulmonary function studies and bronchial provocation challenge [27]. The clinical history is the first important part of diagnostic process and it is regarded as a sensitive method, but with a low specificity [28]. Information about potential respiratory hazards can be also obtained from the material safety data sheets. The assessment of sensitization, with skin prick tests (SPT) and/or specific IgE measurement, is the next important stage in diagnosis of occupational allergy. SPT with an extract of NRL has a high sensitivity (100%) but a low specificity (20%) [29]. SPT is very useful to detect IgE-mediated sensitization to NRL, but it is not as useful in confirming the Volume 14 Number 2 April 2014
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Occupational allergy Wiszniewska and Walusiak-Skorupa
diagnosis of NRL-induced occupational asthma, because 30% of the individuals with positive SPT results had negative challenge results [29]. On the contrary, a negative SPT result with a reliable NRL extract is very useful to rule out NRL-induced occupational asthma [29]. Bronchial challenges can be performed by exposing the patient to the work environment with measurement of pulmonary functions before and after exposure. Confirmation of work-relatedness of occupational asthma should include serial monitoring of peak expiratory flow for periods at work and off work [30] or/and serial measurements of nonspecific bronchial hyperresponsiveness (NSBH), as NSBH is typically worse after a period of exposure and can decrease after cessation of exposure. The nonspecific bronchoprovocation with methacholine is highly sensitive but not specific for occupational asthma [31,32]. It is also possible to perform specific inhalation challenge tests (SICTs) and these are established as the ‘gold standard’ or reference test in the diagnosis of occupational asthma [28]. On the contrary, SICT requires specialized equipment and is only performed in selected centres.
MANAGEMENT AND PREVENTION Preventing respiratory sensitization in healthcare settings includes assessment of the risk by identifying the hazards, avoiding the exposure to allergenic agents by substituting them with less dangerous substances as well minimizing the exposure concentration, time, frequency and number of workers exposed. Avoidance of NRL exposure is the primary goal for preventing sensitization. If possible, powdered latex gloves should be substituted with low-protein, powder-free latex or nitrile gloves [33 ]. The effectiveness of primary preventive strategies in healthcare settings has been demonstrated, as reduction of exposure to latex in hospitals has resulted in a significant decrease in latex-induced allergy [34,35]. Also, a follow-up study [10] among HCWs revealed that avoidance of unnecessary glove use, the use of nonpowdered latex gloves by all workers and of nonlatex gloves by sensitized ones can stop the progression of latex symptoms and incidence of new cases. On the contrary, the reduction of exposure to latex represents a reasonably well tolerated alternative that should be considered in workers with latex-induced occupational asthma when complete avoidance of exposure is not feasible or when the possibilities for nonexposed jobs are limited. Compared with complete removal, reduction of exposure &&
is associated with a substantially lower socioeconomic impact [36].
RECENT FINDINGS It is suggested that the growing use of aerosolized cleaning products increases respiratory tract exposure to the irritant and/or sensitizing agents present in these products, also resulting in occupational airway disease in HCWs (Table 1). Laborde-Caste´rot et al. [37] have reported cases of work-related asthma and/or rhinitis due to EDTA sodium aqueous solutions confirmed by positive nasal provocation tests. In healthcare professionals, the exposure to EDTA-containing products occurs in disinfectants. The authors suggest an immunoallergic response or pharmacological mechanism rather than an irritant one as the explanation of respiratory symptoms induced by inhalation of EDTA [37]. Adisesh et al. [38] described two cases of occupational asthma and four other cases of possible occupational asthma/rhinitis associated with the use of detergent enzymes for cleaning medical instruments. It was emphasized that detergent enzymes when used in healthcare settings should be recognized as potential respiratory sensitizers [38]. In a recent study, Gonzalez et al. [19 ] analysed the associations between asthma and occupational exposure to disinfectants, especially to quaternary ammonium compounds (QACs). The authors found that HCWs, particularly nursing professionals, presented an increased risk of reported physiciandiagnosed asthma and nasal symptoms at work compared with administrative staff working in healthcare sector. Among the various tasks performed, disinfection was associated with a higher risk than simple cleaning. This study highlighted the relation between reported asthma or nasal symptoms at work and the presence of QACs in the products used. The authors emphasized that workplace interventions and training programmes should be conducted to warn workers about the risks, to ensure better protection against QAC exposure and to improve disinfection procedures, especially for nurses [19 ]. In addition to the recent interest by investigators in cleaning agents as an important cause in HCWs asthma, there was special attention paid to WEA. Liss et al. [18] found that healthcare was the most frequent industry for WEA and the rate of WEA claims was 2.1 times greater than that in the rest of the workforce. There was a broad variety of agents to which the WEA cases were attributed, for example cleaning agents, bleaches, fresheners,
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construction/renovation dust, paint fumes, secondhand smoke, perfume and moulds [18]. Arif and Delclos [9 ] reported adverse respiratory health effects among HCWs using cleaning-related chemicals. They found that workplace exposures to cleaning agents were associated with the development of work-related asthma symptoms, WEA and/or occupational asthma among healthcare professionals. For example, WEA was significantly related to exposure to bleach, glutaraldehyde, ortho-phthalaldehyde, chloramines, ethylene oxide and formalin/formaldehyde, although the odds of occupational asthma were almost five-fold elevated for chloramines [9 ]. Walters et al. [39] investigated the causes and trends over time of occupational asthma in HCWs. The majority of cases of occupational asthma (75%) occurred in nursing, operating theatre, endoscopy and radiology staff, although the most frequently implicated agents (79% cases) were glutaraldehyde, latex and cleaning products. Their finding that notifications of occupational asthma in UK HCWs declined, due principally to a reduction in the number of cases of latex and glutaraldehyde-related occupational asthma, is in line with current trends observed in Europe and U.S. However, there was an increase in occupational asthma notifications due to cleaning products, so control strategies should be sought to limit such exposure [39]. Singh et al. [22] investigated the prevalence of asthma phenotypes in dental HCWs and associated risk factors. They found that atopy and work-related ocular-nasal symptoms were strong predictors of WEA. Regular use of personal protective equipment was associated with a protective effect among nonatopic asthmatic individuals, whereas glove use and respiratory protection reduced risk among atopic asthmatic individuals. It has been pointed out that sensitivity to drug allergens is more common in HCWs than in the general population. The prevalence of self-reported drug allergy among HCWs was estimated as 16.2%. At surgical departments, nurses reported allergy symptoms more frequently than doctors and nurses from medicine departments. Antibiotics and local anaesthetics were the most common medications reported to cause symptoms. In addition, sensitivity to drugs increased with duration of employment at the hospital [40]. Kim et al. [41] reported 17.4% prevalence of work-related symptoms due to cephalosporins. The sensitization rate to any cephalosporin defined by SPT was 3.1% and considerably higher when determined by measurement of serum-specific IgE antibodies: 17.4% for any cephalosporin, 10.4% for cefotiam, 6.8% for ceftriaxone and 3.7% for &
EDTA, ethylenediamine tetraacetic acid; HCWs, healthcare workers; OA, occupational asthma; SICT, specific inhalation challenge test; sIgE, specific IgE; QACs, quaternary ammonium compounds.
Cleaning product-related OA was an emerging cause with 22 cases after 2001 and only 5 cases between 1991 and 2000. 75% of cases involved nursing, operating theatre, endoscopy and radiology staff Data on sensitizing agents from electronic database 182 notifications of OA in HCWs Notifications for 21 years from the SHIELD electronic database Walters, 2013 [39]
Serial peak-flow measurements, sIgE, SICT
Significantly elevated odds of WEA for exposure to bleach, glutaraldehyde/ortho-phthalaldehyde, chloramines and ethylene oxide and formalin/formaldehyde. Exposure to chloramines was significantly associated with OA A detailed history of the job using the questionnaire &
5600 HCWs, aged 45.3 years Population-based survey Arif, 2012 [9 ]
Questionnaire
Exposure to QACs increased significantly the risk of reported physician-diagnosed asthma and nasal symptoms at work (OR ¼ 7.5 and 3.2, respectively) Work questionnaire, workplace studies, review of products ingredients 543 HCWs, aged 18–65 years Cross-sectional study Gonzalez, 2013 && [19 ]
Self-administered questionnaire, physical examination
10 published cases of occupational asthma and/or rhinitis in patients exposed to EDTA-containing products 0.1 ml of an aqueous solution of EDTA Non-specific bronchial hyperreactivity 28 patients (cleaners or HCWs) Series of cases Laborde-Caste´rot, 2012 [37]
Study population Study design First author, year
Table 1. Recent studies on HCWs and cleaning products asthma
Assessment of asthma
Assessment of exposure
Results
Occupational disease
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Occupational allergy Wiszniewska and Walusiak-Skorupa
ceftizoxime. A personal history of any antibiotic allergy was a risk factor for work-related symptoms, but not for the presence of specific IgE to cephalosporins [41]. A recent survey concerning the level of knowledge among HCWs of latex gloves and NRL allergy, routine prevention practice and appropriate use of gloves in patient care revealed that most HCWs are aware of the different types of gloves, but only 1% of them were able to correctly match the appropriate gloves to the specifically designed procedure. Around 74.5% HCWs were unable to recognize the presentation of NRL allergy and only 12% of them were aware of rubber accelerators as potential allergens in latex gloves. These data indicate that there is a need for education among HCWs about gloves and NRL allergy [42]. The association between worksite and the level of asthma severity/control has also been analysed. Le Moual et al. [43] observed a significant association between operating room nursing, compared with administrative nursing, and severe persistent asthma. The study [43] confirmed the hypothesis that working as an operating room nurse may induce more severe asthma or worsen asthma control. The first Chinese epidemiological survey performed among nurses revealed an 8.8% prevalence of at least one symptom associated with the latex gloves use. Among symptomatic nurses, 77.1 and 63.9% reported in questionnaire symptoms suggesting glove dermatitis and type I latex allergy (urticaria, rhinorrhoea, or chest tightness/dyspnoea occurring within 2 h of glove use), respectively. They report that employment seniority, positive history of allergic diseases and longer extent of time spent in a single hospital room were associated with reporting symptoms suggestive of type I latex allergy, although using more than five pairs of gloves per working day may be a protective factor [44]. Some aspects of the diagnosis of IgE-mediated occupational allergic diseases were also investigated. The results of serologic testing for latex-specific IgE demonstrated 35% sensitivity and 98% specificity for the CAP and ELISA assays. The performance of the FDA-cleared IgE serologic test for latex allergy has much lower sensitivity than previously reported. This finding confirms that this serologic test should be used only for patients with a history of latex allergy and not for screening a population with a low prevalence of latex sensitization [45]. In-vitro analysis of the NRL SPT solutions demonstrated high variability among different manufacturers. The protein content varied between below detection limit (Stallergenes, Lofarma, Milan, Italy) to 65 mg/ml (Allerbio, Varennes-en-Argonne,
France), although allergen content ranged from 0.6 (Lofarma) to 11.7 mg/ml (Allergopharma, Reinbek, Germany) [46]. A systematic review of the management of latex allergy demonstrated moderately strong and consistent evidence that avoidance of NRL in the workplace reduces both symptoms and markers of sensitization in latex-allergic individuals [47].
CONCLUSION In recent years, healthcare personnel have received particular attention as being at risk for occupational respiratory diseases. Some studies have confirmed an increased risk of occupational asthma and cleaning agents are currently the major respiratory hazards. An immunologic mechanism for occupational asthma due to cleaning products is suggested, but not definitely demonstrated. Large underestimation of self-reported exposure to cleaning/disinfecting agents as well as a lack of knowledge of product components has been observed among HCWs. The need for health education programmes on the occupational risks induced by these types of products is stressed [23]. Further studies are necessary to determine the relative role of individual versus complex workplace exposure in the development of the respiratory work-related diseases in HCWs. Acknowledgements None. Conflicts of interest The authors declare that they have no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. National Institute for Occupational Safety and Health (NIOSH), Centers for Disease Control and Prevention. Healthcare workers. http://www.cdc.gov/ niosh/topics/healthcare. [Accessed 1 November 2013] 2. The European Agency for Safety and Health at Work. Health and safety of healthcare staff. https://osha.europa.eu/en/sector/healthcare. [Accessed 1 November 2013] 3. Pechter E, Davis LK, Tumpowsky C, et al. Work-related asthma among healthcare workers: surveillance data from California, Massachusetts, Michigan, and New Jersey, 1993–1997. Am J Ind Med 2005; 47:265–275. 4. Delclos GL, Gimeno D, Arif AA, et al. Occupational risk factors and asthma among healthcare professionals. Am J Respir Crit Care Med 2007; 175:667– 675. 5. O’Hehir R, Sutherland M, Drew A, Rolland J. Latex allergy. In: Kay A, Kaplan A, Bousquet J, Holt P, editors. Allergy and allergic diseases, 2nd ed. WileyBlackwell; 2008. pp. 1164–1184. 6. Siracusa A, De Blay F, Folletti I, et al. Asthma and exposure to cleaning products: a European Academy of Allergy and Clinical Immunology task force consensus statement. Allergy 2013. [Epub ahead of print] 7. Fishwick D, Barber CM, Bradshaw LM, et al. Standards of care for occupational asthma: an update. Thorax 2012; 67:278–280.
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Occupational disease 8. McHugh MK, Symanski E, Pompeii LA, Delclos GL. Prevalence of asthma by industry and occupation in the U.S. working population. Am J Ind Med 2010; 53:463–475. 9. Arif AA, Delclos GL. Association between cleaning-related chemicals and & work-related asthma and asthma symptoms among healthcare professionals. Occup Environ Med 2012; 69:35–40. An interesting study concerning relationship between work-related exposure to cleaning-related chemicals and development of WRA among HCWs. 10. Filon FL, Radman G. Latex allergy: a follow up study of 1040 healthcare workers. Occup Environ Med 2006; 63:121–125. 11. Liss G, Sussman G, Deal K, et al. Latex allergy: epidemiological study of 1351 hospital workers. Occup Environ Med 1997; 54:335–342. 12. Yassin MS, Lierl M, Fisher T, et al. Latex allergy in hospital employees. Ann Allergy 1994; 72:245–249. 13. Vila L, Sa´nchez G, An˜o M, et al. Risk factors for latex sensitization among healthcare workers. J Investig Allergol Clin Immunol 1999; 9:356–360. 14. Sussman GL, Liss GM, Deal K, et al. Incidence of latex sensitization among latex glove users. J Allergy Clin Immunol 1998; 101 (2 Pt 1):171–178. 15. Bousquet J, Flahault A, Vandenplas O, et al. Natural rubber latex allergy among healthcare workers: a systematic review of the evidence. J Allergy Clin Immunol 2006; 118:447–454. 16. Risenga SM, Shivambu GP, Rakgole MP, et al. Latex allergy and its clinical features among healthcare workers at Mankweng Hospital, Limpopo Province, South Africa. S Afr Med J 2013; 103:390–394. 17. Vandenplas O, Lantin AC, D’Alpaos V, et al. Time trends in occupational asthma in Belgium. Respir Med 2011; 105:1364–1372. 18. Liss GM, Buyantseva L, Luce CE, et al. Work-related asthma in healthcare in Ontario. Am J Ind Med 2011; 54:278–284. 19. Gonzalez M, Je´gu J, Kopferschmitt MC, et al. Asthma among workers in && healthcare settings: role of disinfection with quaternary ammonium compounds. Clin Exp Allergy 2013. [Epub ahead of print] The study analysed the associations between asthma and occupational exposure to disinfectants, especially QACs. The study demonstrates that exposure to QACs increased significantly the risk of reported physician-diagnosed asthma and nasal symptoms at work. 20. Mirabelli MC, Zock J-P, Plana E, et al. Occupational risk factors for asthma among nurses and related healthcare professionals in an international study. Occup Environ Med 2007; 64:474–479. 21. Arif AA, Delclos GL, Serra C. Occupational exposures and asthma among nursing professionals. Occup Environ Med 2009; 66:274–278. 22. Singh T, Bello B, Jeebhay MF. Risk factors associated with asthma phenotypes in dental healthcare workers. Am J Ind Med 2013; 56:90–99. 23. Donnay C, Denis MA, Magis R, et al. Under-estimation of self-reported occupational exposure by questionnaire in hospital workers. Occup Environ Med 2011; 68:611–617. 24. Suojalehto H, Linstro¨m I, Henriks-Eckerman ML, et al. Occupational asthma related to low levels of airborne methylene diphenyl diisocyanate (MDI) in orthopedic casting work. Am J Ind Med 2011; 54:906–910. 25. Piirila¨ P, Hodgson U, Estlander T, et al. Occupational respiratory hypersensitivity in dental personnel. Int Arch Occup Environ Health 2002; 75:209–216. 26. Jaakkola MS, Leino T, Tammilehto L, et al. Respiratory effects of exposure to methacrylates among dental assistants. Allergy 2007; 62:648–654. 27. Tarlo SM, Balmes J, Balkissoon R, et al. Diagnosis and management of workrelated asthma: American College Of Chest Physicians Consensus Statement. Chest 2008; 134 (Suppl 3):1–41.
118
www.co-allergy.com
28. Moscato G, Malo JL, Bernstein D. Diagnosing occupational asthma: how, how much, how far? Eur Resp J 2003; 21:879–885. 29. Quirce S, Swanson MC, Ferna´ndez-Nieto M, et al. Quantified environmental challenge with absorbable dusting powder aerosol from natural rubber latex gloves. J Allergy Clin Immunol 2003; 111:788–794. 30. Tarlo SM, Liss GM. Occupational asthma: an approach to diagnosis and management. CMAJ 2003; 168:867–871. 31. Sabin BR, Grammer LC. Chapter 17: occupational immunologic lung disease. Allergy Asthma Proc 2012; 33 (Suppl 1):58–60. 32. Cowl CT. Occupational asthma: review of assessment, treatment, and compensation. Chest 2011; 139:674–681. 33. Heederik D, Henneberger PK, Redlich CA, ERS Task Force on the Manage&& ment of Work-related Asthma. Primary prevention: exposure reduction, skin exposure and respiratory protection. Eur Respir Rev 2012; 21:112–124. A good summary of the impact of controlling work exposure on the prevention of occupational asthma. 34. Allmers H, Schmengler J, Skudlik C. Primary prevention of natural rubber latex allergy in the German healthcare system through education and intervention. J Allergy Clin Immunol 2002; 110:318–323. 35. Allmers H, Schmengler J, John SM. Decreasing incidence of occupational contact urticaria caused by natural rubber latex allergy in German healthcare workers. J Allergy Clin Immunol 2004; 114:347–351. 36. Vandenplas O, Jamart J, Delwiche JP, et al. Occupational asthma caused by natural rubber latex: outcome according to cessation or reduction of exposure. J Allergy Clin Immunol 2002; 109:125–130. 37. Laborde-Caste´rot H, Villa AF, Rosenberg N, et al. Occupational rhinitis and asthma due to EDTA-containing detergents or disinfectants. Am J Ind Med 2012; 55:677–682. 38. Adisesh A, Murphy E, Barber CM, Ayres JG. Occupational asthma and rhinitis due to detergent enzymes in healthcare. Occup Med (Lond) 2011; 61:364– 369. 39. Walters GI, Moore VC, McGrath EE, et al. Agents and trends in healthcare workers’ occupational asthma. Occup Med (Lond) 2013; 63:513–516. 40. Zilinskaite L, Tamasauskas D, Kvedariene V, Sitkauskiene B. Self-reported drug allergy in healthcare workers in conservative and surgical medicine departments. J Investig Allergol Clin Immunol 2012; 22:357–362. 41. Kim JE, Kim SH, Jin HJ, et al. IgE sensitization to cephalosporins in healthcare workers. Allergy Asthma Immunol Res 2012; 4:85–91. 42. Al-Niaimi F, Chiang YZ, Chiang YN, Williams J. Latex allergy: assessment of knowledge, appropriate use of gloves and prevention practice among hospital healthcare workers. Clin Exp Dermatol 2013; 38:77–80. 43. Le Moual N, Varraso R, Zock JP, et al. Are operating room nurses at higher risk of severe persistent asthma? The Nurses’ Health Study. J Occup Environ Med 2013; 55:973–977. 44. Liu QL, He XZ, Liang K, et al. Prevalence and risk factors for latex glove allergy among female clinical nurses: a multicenter questionnaire study in China. Int J Occup Environ Health 2013; 19:29–34. 45. Accetta Pedersen DJ, Klancnik M, Elms N, et al. Analysis of available diagnostic tests for latex sensitization in an at-risk population. Ann Allergy Asthma Immunol 2012; 108:94–97. 46. van Kampen V, de Blay F, Folletti I, et al. Evaluation of commercial skin prick test solutions for selected occupational allergens. Allergy 2013; 68:651– 658. 47. Madan I, Cullinan P, Ahmed SM. Occupational management of type I latex allergy. Occup Med (Lond) 2013; 63:395–404.
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