Laboratory animal allergy (LAA) is a serious occupational hazard
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1 ORIGINAL ARTICLE Prevention of Laboratory Animal Allergy in the United States A National Survey Gregg M. Stave, MD, JD, MPH, and Dennis J. Darcey, MD, MPH, MSPH Objective: Respiratory allergy to laboratory animals is a common and preventable occupational health problem. This study documents current laboratory animal allergy (LAA) prevention programs in the United States. Methods: An online survey was ed to designated institutional officials at laboratory animal facilities identified by the National Institutes of Health Office of Laboratory Animal Welfare. Results: A total of 198 organizations responded and more than 80% required the use of uniforms and gloves to control exposure. Respirators were required by 25% of organizations. Medical surveillance was mandated by 58% of organizations (70% for organizations with at least 100 employees working with animals). Work restriction practices varied. Only 25% of organizations reported knowing the prevalence (range: 0% to 75%) and 29% reported knowing the incidence of LAA (range: 0% to 18%). Conclusions: There is broad variation in policy and practice to prevent LAA. An evidence-based consensus would ensure greater protection of workers. Laboratory animal allergy (LAA) is a serious occupational hazard for workers in research laboratories that can affect health and career options. Respiratory allergy and asthma is of the greatest concern because it is common and requires a multifaceted prevention strategy. Manifestations of respiratory allergy include allergic conjunctivitis, rhinitis, and asthma. Prevention of animal allergy depends on the control of allergenic material in the work environment. Exposure varies by job and tasks as well as various workplace factors. 1,2 Personal protective equipment (PPE) and air-purifying respirators are recommended when exposure cannot be adequately controlled using engineering control technologies, administrative controls, and work practice controls. Occupational medicine specialists play a critical role in these programs including medical surveillance, diagnosis of LAA, and determining work restrictions for workers with allergy and asthma. The objective of this study is to document current LAA prevention and control programs in animal laboratory facilities in the United States. METHODS An online survey (SurveyMonkey) was ed to the designated institutional official at all laboratory animal care facilities identified by the National Institutes of Health Office of Laboratory Animal Welfare (1033 facilities across the country). Supplemental requests to encourage completion of the survey were distributed through the American College of Occupational and Environmental Medicine Pharmaceutical Industry Section, the Pharmaceutical Safety Group, and the Campus Safety Health and Environmental Management Association. Survey responses were collected and analyzed. The survey included questions on the following: From the Division of Occupational and Environmental Medicine, Department of Community and Family Medicine, Duke University Medical Center, Durham, NC. Disclosure: The authors declare no conflict of interest. Address correspondence to: Dennis J. Darcey, MD, MPH, MSPH, DUMC 3834, Durham, NC (dennis.darcey@duke.edu). Copyright C 2012 by American College of Occupational and Environmental Medicine DOI: /JOM.0b013e318247a44a 1. the total number of employees exposed to laboratory animal allergens in each facility, 2. administrative controls, 3. engineering controls, 4. the use and availability of PPE including clothing and respirators, 5. recommended hygiene practices for employees, 6. medical surveillance for LAA, 7. criteria for LAA diagnosis, 8. the prevalence and incidence of LAA at each facility, and 9. work restrictions recommended for LAA diagnosed workers. The study protocol was approved by the Duke University institutional review board. RESULTS Surveys were sent to 1033 organizations identified by the National Institutes of Health Office of Laboratory Animal Welfare and 83 of them were returned as undeliverable. Responses were received from 198 institutions (19.2% overall response rate). Most (69%) responding organizations were classified as university/academic/medical center (Table 1). Research institutes comprised 15.2% of respondents. Pharmaceutical organizations were well represented with 14 companies. The remaining respondents include other commercial or other types of organizations. The number of employees working with laboratory animals at responding institutions ranged from 1 to Almost 40% of these institutions had between 15 and 99 employees conducting animal work, whereas 25% had between 100 and 499. One fifth of responding institutions had more than 500 employees handling animals (Table 2). Exposure Control Administrative Controls In almost all workplaces, work with animals is conducted in a dedicated animal facility. However, 65% of organizations also conduct work outside of dedicated facilities where animals are housed. Access to animal rooms is restricted by 92% of employers. Eighty percent of employers restrict used (contaminated) PPE to the animal facility, 48% have separate lockers for clean clothes, and 20% of respondents require employees to shower out. Training of workers on the prevention of LAA was reported by 82% of employers (Table 3). Work Practice Controls Hand washing is the most common work practice control used by 96% of employers. Of these, two thirds limit animal density and two thirds use room-cleaning procedures that minimize exposures such as high efficiency particulate air (HEPA) filtered vacuums and a wet process. Fifty-five percent of employers use work process design to limit animal handling. Wet prep is used for shaving by 20% of employers (Table 4). Engineering Controls Various engineering controls are employed with most organizations using more than one type (Table 5). Biological safety cabinets, local exhaust ventilation, negative pressure environments, and 558 JOEM Volume 54, Number 5, May 2012
2 JOEM Volume 54, Number 5, May 2012 Prevention of Laboratory Animal Allergy in the US TABLE 1. Distribution of Survey Respondents by the Type of Institution Category of Institution N (%) University/academic/medical center 136 (68.7) Research institute 30 (15.2) Pharmaceutical 14 (7.0) Other commercial 14 (7.1) Other 4 (2.0) Total 198 TABLE 5. Engineering Controls Used to Reduce Engineering Controls % Robotic equipment 7.1 Separately ventilated caging 64.5 Biological safety cabinets 74.1 Local exhaust ventilation 76.6 Negative pressure environments 74.6 Filter top cages 75.6 Downdraft tables 37.1 None 3.0 TABLE 2. Distribution of Survey Respondents by Size of Workforce Number of Employees Working With Animals % < TABLE 3. Administrative Controls Used to Reduce Administrative Controls % Training of workers on LAA prevention 81.6 Restricting access to animal rooms 92.3 Limiting animal use to animal facilities 47.4 Restricting contaminated/used PPE to animal facility 80.6 Shower out 20.4 Separate lockers for clean clothes 48.0 None 1.0 LAA indicates laboratory animal allergy; PPE, personal protective equipment. TABLE 4. Work Practice Controls Used to Reduce Work Practice Controls % Limiting animal density 65.3 Work process design to reduce animal 55.1 handling Wet prep for shaving 19.9 Room-cleaning procedures that minimize 66.3 exposure (HEPA filter vacuum, wet process, etc) Hand washing 96.4 None 0 filter top cages are used by three fourths of respondents. Separately ventilated caging is used in 65% of institutions and 37% use downdraft tables. Robotic equipment is used by 7% of institutions. Personal Protective Equipment There is great variation in the mandated use of PPE (Table 6). At least one sixth of programs mandate the use of at least an N95 air-purifying respirator and overall 25% of respondents mandate the use of respirator for all tasks. More than 40% of respondents mandate the use of surgical masks. The masks do not function as respirators, although they can provide some protection from infection for the animals. The survey did not differentiate on the possible reasons for use. The most common forms of PPE used are gloves and uniforms/clothing covers (more than 80%). Most organizations make various forms of PPE available to employees when it is not required (Table 7). More than 80% of organizations offer respirators to employees on a mandatory or voluntary basis. Employers mandate various PPE for specific tasks (Table 8). Cage cleaning is known to generate high levels of airborne allergens and has the greatest requirements. The use of hair covers is relatively low (except for cage cleaning), despite data showing that they protect against the carriage of allergens. 3 Medical Surveillance Preplacement assessments are conducted by three fourths of respondents. Medical surveillance is conducted for at least some employees by 85% of institutions. However, only 58% of institutions make medical surveillance mandatory for all and 14% also mandate medical surveillance for some employees (Table 9). Of those institutions conducting medical surveillance, 91% incorporate questionnaires and 52% include a clinical examination (Table 10). At some institutions, a clinical assessment was performed dependent on responses to a questionnaire. A minority of respondents conducted additional testing routinely. This includes pulmonary function testing that in some cases is conducted for respirator clearance. Skin prick tests are performed by 8% and radioallergosorbent test (RAST) is reported by 6% of institutions. Organizations with larger animal handling workforces are more likely to conduct medical surveillance (Figure 1). Mandatory medical surveillance ranges from about 40% for employers with fewer than 15 employees working with animals to more than 70% for those with at least 100 animal workers. The type of organization had limited effect on whether medical surveillance was mandatory (Fig. 2). C 2012 American College of Occupational and Environmental Medicine 559
3 Stave and Darcey JOEM Volume 54, Number 5, May 2012 Medical surveillance findings are reviewed with employees by almost all organizations conducting medical surveillance. Only 7% of these organizations perform an analysis of group data. TABLE 6. Mandatory PPE Used to Reduce Mandatory (Always Required for Animal Work) PPE % N95 air-purifying respirators 16.6 Cartridge air-purifying respirators 2.6 Powered air-purifying respirators 6.1 Surgical masks* 42.9 Shoe covers 52.6 Uniforms/clothing cover 85.7 Hair covers 37.8 Gloves 88.3 None 4.6 *Surgical masks are not actually PPE, but were included to capture this common practice. PPE indicates personal protective equipment. TABLE 7. Optional PPE Used to Reduce Exposure to Animal Allergens (Responses Are Not Mutually Exclusive) Optional (Available, Not Required) PPE % N95 air-purifying respirators 63.0 Cartridge air-purifying respirators 25.5 Powered air-purifying respirators 34.8 Surgical masks* 54.3 Shoe covers 41.8 Uniforms/clothing cover 28.3 Hair covers 40.2 Gloves 30.4 None 7.1 *Surgical masks are not actually PPE, but were included to capture this common practice. PPE indicates personal protective equipment. Work Restrictions A slight majority of employers will consider excluding workers with non-asthma LAA from continued work with animals depending on the severity of the allergy (Table 11). One third of employers allow allergic workers to continue working with restrictions. None of the organizations exclude allergic workers from animal work, although some will exclude workers from handling the type of animal that they are allergic to. For workers that develop LAA asthma, 10% of organizations exclude them from continued animal work, whereas 5% do not write any restrictions (Table 12). One eighth of organizations exclude continued work with the problematic species and slightly more than three fifths consider exclusion depending on the severity of asthma. Prevalence and Incidence of Laboratory Animal Allergy Almost 90% of respondents based their definition of respiratory LAA on self-reported symptoms (Table 13). However, most organizations supplemented their diagnosis with clinical assessments and many also utilized testing (RAST or skin prick testing). Most respondents did not know the prevalence or incidence of LAA for their organizations. Twenty-five percent of respondents reported knowledge of LAA prevalence, whereas 29% were aware of the incidence of LAA (Figure 3). Reported awareness of prevalence and incidence was the lowest among employers with 100 to 499 employees working with animals, despite the higher rate of medical surveillance in this group. Knowledge of prevalence and incidence was the lowest in the university/academic/medical center setting (Fig. 4). Pharmaceutical industry respondents indicated the highest awareness of prevalence (36%) and 43% of non-pharmaceutical commercial organizations reported knowing the incidence rate. Among organizations that said the data were available, the reported prevalence rate ranged from 0% to 75% and the 1-year incidence rate ranged from 0% to 18%. Of these, 18 organizations reported a prevalence of 0%. Some respondents indicated that they were aware of prevalence or incidence rates, but not both. Of those responding that the incidence rate was available, 37 reported an incidence of 0%. However, the survey did not query how these rates were determined. Among the organizations reporting a 1-year incidence rate of 3% or less, only 36% reported conducting mandatory medical surveillance. Most organizations that reported incidence data were available did not conduct mandatory medical surveillance. DISCUSSION Laboratory animal allergy remains a significant occupational health issue. There have been very few published studies describing the effects of prevention practices on the prevalence and incidence TABLE 8. Mandatory PPE Used to Reduce Mandatory PPE Required Only for Specific Tasks Cage Cleaning Cage Washing Animal Care Dosing Surgery Necropsy N95 air-purifying respirators Cartridge air-purifying respirators Powered air-purifying respirators Surgical masks* Shoe covers Uniforms/clothing cover Hair covers Gloves None *Surgical masks are not actually PPE, but were included to capture this common practice. PPE indicates personal protective equipment. 560 C 2012 American College of Occupational and Environmental Medicine
4 JOEM Volume 54, Number 5, May 2012 Prevention of Laboratory Animal Allergy in the US TABLE 9. Medical Surveillance Policies of Respondents TABLE 11. With LAA Work Restriction Policies for Workers Medical Surveillance for LAA % Mandatory for all 58.1 Mandatory for some 14.1 Voluntary for all 11.5 Voluntary for some 0.5 Not conducted 15.7 LAA indicates laboratory animal allergy. Workers With LAA (Non-Asthma) % Are excluded from all work with animals 0 Are excluded from work with the animal species 5.9 that they are allergic to May be excluded or restricted depending on severity 55.1 of allergy Can continue to work with animals with restrictions 33.2 Can continue to work with animals without 5.9 restrictions LAA indicates laboratory animal allergy. TABLE 10. Components of Medical Surveillance Medical Surveillance for LAA Includes % Questionnaires 91 Clinical examination 52.1 RAST 6.0 Skin prick test 7.8 PFT 18.6 LAA indicates laboratory animal allergy; RAST, radioallergosorbent test; PFT, pulmonary function test. TABLE 12. Work Restriction Policies for Workers With Laboratory Animal Asthma Workers With Laboratory Animal Asthma % Are excluded from all work with animals 10.3 Are excluded from work with the animal species 12.4 that they are allergic to May be excluded or restricted depending on severity 61.6 of asthma Can continue to work with animals with restrictions 20.0 Can continue to work with animals without 5.4 restrictions TABLE 13. Components of Decision-Making Process for the Diagnosis of LAA* Respiratory LAA is Defined on the Basis of % Symptoms 89.6 Clinical examination 72.1 RAST 23.0 Skin test 16.4 FIGURE 1. Medical surveillance for laboratory animal allergy is more likely to be conducted by organizations with larger animal research workforces. *Respondents could indicate all that were applicable. LAA indicates laboratory animal allergy; RAST, radioallergosorbent test. FIGURE 2. Medical surveillance practices by type of organization. FIGURE 3. Knowledge of LAA prevalence and incidence by size of workforce. LAA indicates laboratory animal allergy. C 2012 American College of Occupational and Environmental Medicine 561
5 Stave and Darcey JOEM Volume 54, Number 5, May 2012 FIGURE 4. Knowledge of LAA prevalence and incidence by type of organization. LAA indicates laboratory animal allergy. of LAA. This study represents the first US national survey of LAA prevention practices. This study reveals that there is a wide range of practices and no consistent approach to the prevention of LAA. Although some variation would be anticipated on the basis of differences in facility design and other factors, it is likely that many of the differences in approach, policy, and practice are based on individual and institutional preferences. Variation in practice may also be based on perceived success in controlling exposure. Methods to control exposure were reviewed by Harrison. 4 Krop et al 3 have demonstrated the importance of using hair-covering caps. Schweitzer et al 5 have also shown that housing mice in ventilated cages operated under negative pressure and using ventilated changing tables reduced ambient mouse allergen (Mus m 1) concentrations tenfold, compared with the use of conventional caging and a non-ventilated changing table. Ambient allergen was not reduced when mice were housed in positively pressurized cages versus conventional cages, or when animal rooms were cleaned more frequently. Most organizations report using a combination of engineering, administrative, work practice controls along with PPE. However, even when looking at PPE required for specific tasks, there is no consensus approach among respondents. To determine the effectiveness of LAA prevention programs, knowledge of the prevalence and incidence of primary and secondary LAA is critical. Active medical surveillance is more likely to identify all incident cases than passive surveillance (relying on workers reporting). However, more than 40% of respondents did not mandate medical surveillance. Nicholson et al 6 reviewed 109 studies to determine the evidence base for medical surveillance. They recommended a baseline health assessment and periodic medical surveillance. Medical surveillance was also reviewed by Seward. 7 Prototype LAA questionnaires for initial and follow-up surveillance have been published. 8 Although most respondents did not know the prevalence or incidence of LAA, many that did report rates reported very low rates or rates of zero. Given the background prevalence in the literature of 14% to 44%, 9 the finding that a large number of programs reported such low prevalence rates was unexpected. A review of 15 cross-sectional studies and 4 longitudinal studies by Folletti et al 10 suggested a decrease in the prevalence of occupational asthma, but not occupational allergy from 1980 to That review is limited to the published literature and represents only a small minority of laboratory animal worksites. It is possible that prevalence rates have in fact fallen or that workers with LAA are choosing not to seek jobs working with animals. Another possibility is that workers with LAA are being excluded from employment, but this seems unlikely as most respondents indicated that workers with LAA could usually continue their work. Another hypothesis is that the reports are based on the lack of awareness, especially in organizations that do not conduct medical surveillance, or do not analyze surveillance results for all workers, or both. Group surveillance was uncommon, reported by only 7% of organizations. Similar issues surround the reporting of incidence rates. There is only one program in the published literature that described a comprehensive LAA prevention program that was able to reduce the incidence of LAA to zero. 11 Other programs that have been able to prevent LAA are encouraged to publish their prevention programs to expand understanding of factors critical to successful prevention. More than 10% of organizations incorporate testing (RAST or skin prick testing) into medical surveillance and a larger number utilize testing to help define a case of LAA. When using RAST for medical surveillance, positive results may not correlate with symptoms. Matsui et al 12 have shown that among workers with detectable mouse IgE, higher mouse IgG and mouse IgG4 levels are associated with a decreased risk of mouse-related symptoms and may be markers for clinical tolerance. In comparing tests, Sharma et al 13 reported that skin prick testing performs best in discriminating patients with and without mouse allergy. However skin prick testing requires special training, which may necessitate referral. This study has several limitations. The response rate was good for a survey distributed by ; however, slightly less than 20% of institutions responded, raising questions about generalizability. Those responding include a large number of diverse organizations and likely represent the breadth of current practices, even if the actual percentages might differ. As the survey is based on self-report, the responses may not accurately reflect full knowledge of institutional practices. To keep the questionnaire short, a number of topics were not explored. These include data on the use of industrial hygiene sampling to monitor exposure and approaches to the prevention of secondary LAA (allergy to additional species after developing LAA to one species), which can develop in settings that protect against the development of primary LAA. The variability in practices described in the survey responses indicates the need for an evidence-based consensus effort to define the essential elements of a successful prevention effort. To support this effort, there is a need for more organizations to publish descriptions of their LAA programs and experience. ACKNOWLEDGEMENTS The authors thank Rosemary Thorne for her technical assistance with the survey and Qlin Song, Ed Bernacki, Mark Upfal, and Cheryl Barbanel for their input on earlier versions of the questionnaire. REFERENCES 1. Gordon S, Tee RD, Nieuwenhuijsen MJ, Lowson D, Harris J, Newman Taylor AJ. Measurement of airborne rat urinary allergen in an epidemiological study. Clin Exp Allergy. 1994;24: Eggleston PA, Newill CA, Ansari AA, et al. Task-related variation in airborne concentrations of laboratory animal allergens: studies with Rat n I. J Allergy Clin Immunol. 1989;84: Krop EJ, Doekes G, Stone MJ, Aalberse RC, van der Zee JS. Spreading of occupational allergens: laboratory animal allergens on hair-covering caps and in mattress dust of laboratory animal workers. Occup Environ Med. 2007;64: Harrison DJ. Controlling exposure to laboratory animal allergens. ILAR J. 2001;42: Schweitzer IB, Smith E, Harrison DJ, et al. Reducing exposure to laboratory animal allergens. Comp Med. 2003;53: C 2012 American College of Occupational and Environmental Medicine
6 JOEM Volume 54, Number 5, May 2012 Prevention of Laboratory Animal Allergy in the US 6. Nicholson PJ, Mayho GV, Roomes D, Swann AB, Blackburn BS. Health surveillance of workers exposed to laboratory animal allergens. Occup Med (Lond). 2010;60: Seward JP. Medical surveillance of allergy in laboratory animal handlers. ILAR J. 2001;42: Bush RK, Stave GM. Laboratory animal allergy: an update. ILAR J. 2003;44: Bush RK. Mechanisms and etiology of laboratory animal allergy. ILAR J. 2001;42: Folletti I, Forcina A, Marabini A, Bussetti A, Siracusa A. Have the prevalence and incidence of occupational asthma and rhinitis because of laboratory animals declined in the last 25 years? Allergy. 2008;63: Goodno LE, Stave GM. Primary and secondary allergies to laboratory animals. J Occup Environ Med. 2002;44: Matsui EC, Diette GB, Krop EJM, et al. Mouse allergen-specific immunoglobulin G and immunoglobulin G4 and allergic symptoms in immunoglobulin E-sensitized laboratory animal workers. Clin Exp Allergy. 2005;35: Sharma HP, Wood RA, Bravo AR, Matsui EC. A comparison of skin prick tests, intradermal skin tests, and specific IgE in the diagnosis of mouse allergy. J Allergy Clin Immunol. 2008;121: C 2012 American College of Occupational and Environmental Medicine 563
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