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Pages D19-D28 | Accepted author version posted online: 20 Nov 2017, Published online:26 Feb 2018

ABSTRACT

The professional work of small animal veterinary staff encompasses a wide diversity of demanding tasks. This has prompted a number of studies covering physical, chemical, biological, ergonomic, or psychological hazards, as well as their health effects upon veterinary workers. However, such results were obtained from self-reported surveys (via paper or online). This study reports the identification of potential hazards and provides a risk assessment of 15 veterinary clinics based on data from walk-through surveys, interviews with workers, and quantification of indoor air quality parameters including concentration of volatile organic compounds (total, isoflurane, and glutaraldehyde). The risk arising from X-ray exposure was unacceptable in seven clinics; X-ray examination should be discontinued in the absence of isolated radiation rooms, poor safety practices, and lack of personal protective equipment. Ergonomic-related hazards and work practices should be revised as soon as possible, considering that improper postures, as well as moving and lifting heavy animals are major causes of musculoskeletal disorders. The risk levels were, in general, small or medium (acceptable) with regard to exposure to physical hazards (such as bites, scratches, cuts, and burns) and biological hazards. It was observed that the indoor air quality parameters including temperature, respirable particulate matter and total volatile organic compounds do not indicate a comfortable workplace environment, requiring clinics' attention to keep the safe environment. The veterinarians and nurses were exposed to isoflurane (above 2 ppm) during surgery if an extractor system for waste gas was used instead of a scavenging system. Finally, veterinary workers did not possess any type of training on occupational safety and health issues, even though they recognized its importance.

Introduction

The veterinary profession differs in a number of ways from the physician to health technician. Animal patients vary in size and behavior, and in anatomical, physiological, and other characteristics. In human medicine, most patients cooperate with their physicians; whereas, in the veterinary world uncooperative and aggressive animal patients often resist handling and inflict injuries to their handlers.

The activities of veterinary workers are characterized by a high level of risk and high prevalence of injury.[1Lucas, M., L. Day, A. Shirangi, and L. Fritschi: Significant injuries in Australian veterinarians and use of safety precautions. Occup. Med. 59:327333 (2009). [Crossref][Google Scholar],2Reijula, K., K. Räsänen, M. Hämäläinen, et al.: Work environment and occupational health of Finnish veterinarians. Am. J. Ind. Med. 44:4657 (2003). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] Indeed, the risk of occurrence of an occupational accident in veterinary practice is lower than in the construction or the metal industry, but higher than in the chemical industry.[3Nienhaus, A., C. Skudlik, and A. Seidler: Work-related accidents and occupational diseases in veterinarians and their staff. Int. Arch. Occup. Environ. Health 78:230238 (2005). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] Moreover, due to their own educational program and training, most veterinarians prescribe self-medication (such as antibiotics and analgesics) and self-suture lacerations so the total number of cases reported may be underestimated.[4–7Bonini, S., A. Buonacucina, L. Selis, A. Peli, A. Mutti, and M. Corradi: Occupational hazards in veterinarians: An updating. J. Vet. Sci. Technol. 7:317 (2016). [Google Scholar]Jackson, J., and A. Villarroel: A survey of the risk of zonoses for veterinarians. Zoonoses Public Health 59:193201 (2012). [Crossref], [PubMed], [Web of Science ®][Google Scholar]Jeyaretnam, J., and H. Jones: Physical, chemical and biological hazards in veterinary practice. Aust. Vet. J. 78:751758 (2000). [Crossref], [PubMed], [Web of Science ®][Google Scholar]White, S.: Prevalence and risk factors associated with musculoskeletal discomfort in spay and neuter veterinarians. Animals 3:85108 (2013). [Crossref][Google Scholar]] A study made in Ireland concluded that veterinary nurses, particularly those in management positions, were key stakeholders in health and safety in their work environment as they often received occupational safety and health (OSH) training.[8O'Kelly, C.: Health and safety and the veterinary nurse challenges. Vet. Irel. J. 4:615617 (2013). [Google Scholar]]

A number of studies have focused on injuries/trauma, ionizing radiation, noise, chemicals, zoonosis, allergies, and psychological risks pertaining to small animal veterinary activities.[4Bonini, S., A. Buonacucina, L. Selis, A. Peli, A. Mutti, and M. Corradi: Occupational hazards in veterinarians: An updating. J. Vet. Sci. Technol. 7:317 (2016). [Google Scholar]] However, most studies were based on self-reported online surveys with ambiguous information.

As far as the authors are aware, none of risk assessment studies applied to small animal veterinary activities is available in the literature. The overall goal of risk assessment is to remove hazards, or reduce the level of their risk by adding control measures (preventive and/or protective) as necessary. It is relevant to have a team work with good working knowledge of OSH issues to prevent and/or minimize job-related health risks.

Indoor air quality encompasses a wide variety of factors; as a result, an individual's exposure will be determined by a combination of local outdoor contaminant levels and different indoor environments.[9Macedo, A., O. Magalhães, A. Brito, and O. Mayan: Characterization of indoor environmental quality in primary schools in Maia: A Portuguese case study. Hum. Ecol. Risk Assess. An Int. J. 19:126136 (2013). [Taylor & Francis Online], [Web of Science ®][Google Scholar]]

Chemical risk results mainly from the use of drugs (especially antineoplastic and antiparasitic agents), detergents, disinfectants, and gaseous anesthetics.[4Bonini, S., A. Buonacucina, L. Selis, A. Peli, A. Mutti, and M. Corradi: Occupational hazards in veterinarians: An updating. J. Vet. Sci. Technol. 7:317 (2016). [Google Scholar]] Bleach has been the most commonly used chemical agent for environmental disinfection of infectious body fluids;[10Murphy, C., R. Reid-Smith, J. Weese, and S. McEwen: Evaluation of specific infection control practices used by companion animal veterinarians in community veterinary practices in southern Ontario. Zoonoses Public Health 57:429438 (2010). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] however, it has been substituted by quaternary ammonium compounds in recent times. Halothane, isoflurane, and sevoflurane are the most common types of inhalation anesthetic gases;[11Sakhvidi, M., A. Bahrami, A. Ghiasvand, H. Mahjub, and L. Tuduri: Determination of inhalational anesthetics in field and laboratory by SPME GC/MS. Anal. Lett. 45:375385 (2012). [Taylor & Francis Online], [Web of Science ®][Google Scholar]] therefore, a large number of workers may be exposed in their workplace. Some anesthetic agents can enter the operating room atmosphere, thus exposing veterinary workers to potential risks, ranging from chronic exposure to acute inhalation of anesthetic gas.[12Friembichler, S., P. Coppens, H. Sare, and Y. Moens: A scavenging double mask to reduce workplace contamination during mask induction of inhalation anesthesia in dogs. Acta Vet. Scand. 53:17 (2011). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

Studies unfolded a high prevalence of musculoskeletal disorders (MSD) within veterinary workers, including pain, discomfort, injury, loss of productivity, and loss of quality of life. These MSDs caused from carrying out repetitive tasks, extended static postures, improper postures and hand movements, and moving and lifting heavy animals.[13–15Epp, T.: Occupational health hazards in veterinary medicine: physical, psychological and chemical hazards. Can. Vet. J. 53:151157 (2012). [PubMed], [Web of Science ®][Google Scholar]Scuffham, A., S. Legg, E. Firth, and M. Stevenson: Prevalence and risk factors associated with musculoskeletal discomfort in New Zealand veterinarians. Appl. Ergon. 41:444453 (2010). [Crossref], [PubMed], [Web of Science ®][Google Scholar]Kozak, A., G. Schedlbauer, C. Peters, and A. Nienhaus: Self-reported musculoskeletal disorders of the distal upper extremities and the neck in German veterinarians: A cross-sectional study. PLoS One 9:e89362 (2014). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

Zoonosis refers specifically to an infectious disease transmissible from animals to humans. Veterinarians are uniquely qualified and broadly trained to help prevent transmission thereof; hence, these workers play an important role in promoting public health, via recognition and treatment of diseases during examination of animals and through education of clients.[5Jackson, J., and A. Villarroel: A survey of the risk of zonoses for veterinarians. Zoonoses Public Health 59:193201 (2012). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

A few research studies claimed that the risk management system failed in the veterinary workplace due to inadequacy in personal protectiveness, as well as ineffectiveness of the intervention used; these facts are correlated to the lack of OSH training to ensure competence in those bearing the higher responsibilities.[16D'Souza, E., R. Barraclough, D. Fishwick, and A. Curran: Management of occupational health risks in small-animal veterinary practices. Occup. Med. 59:316322 (2009). [Crossref][Google Scholar],17Dowd, K., M. Taylor, J. Toribio, C. Hooker, and N. Dhand: Zoonotic disease risk perceptions and infection control practices of Australian veterinarians: Call for change in work culture. Prev. Vet. Med. 111:1724 (2013). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

The goal of this study was to perform a risk assessment at small animal veterinary clinics by monitoring indoor air quality, quantifying occupational exposures to volatile organic compounds related to surgery (namely disinfection and anesthesia), and characterizing depth of knowledge and workers' opinions regarding health and safety issues.

Methods

Study population

A descriptive-analytic and cross-sectional study was conducted in 15 small veterinary clinics located in Maia county, Portugal. We contacted each clinic owner personally to explain the study and to assure the necessary engagement of employees.

Ethics approval was not necessary in agreement with the Declaration of Helsinki,[18World Medical Association: Declaration of Helsinki – Ethical principles for medical research involving human subjects. J. Am. Med. Assoc. 310:21912194 (2013). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] since the study was focused on the collection of information related to veterinary practice and health and safety knowledge, rather than individual's parameters.

The protocol of the study was explained to all workers, and the confidentiality was assured. Upon obtaining written consent, all workers (n = 49) were encouraged to answer the questionnaire in the presence of one of our researchers to reduce chances of misinterpretation, while maximizing return rate.

Risk assessment

A team (including two public health professionals possessing OSH expertise and the director of each clinic) performed a walk-through survey to identify working areas having main veterinary activities, as well as pinpoint occupational hazards related to aforementioned activities. The same team (without the director) carried out a risk assessment based on a protocol developed by the European Agency for Safety and Health at Work.[19EU-OSHA – European Agency for Safety and Health at Work: Risk assessment essentials. Safety and health at work is everyone's concern. Available at https://osha.europe/en/tools-and-publications/publications/promotional_material/rat2007 (accessed November 9, 2016). [Google Scholar]] The risk level arising from a hazard was classified as small, medium, or high, based on the probability of occurrence (exposure to hazard at work) and severity of harm expected from a hazard. High risk was considered as unacceptable risk, which means that intervention-encompassing implementation of control measures would be encouraged. If legal requirements were not complied with, risk was not acceptable. Small and medium risks were considered acceptable.

Assessment of indoor air quality

Five clinics were randomly selected from 15 clinics for environmental and occupational monitoring. The quality of indoor air included the following parameters: respirable particulate matter (PM10), total volatile organic compounds (TVOC), carbon dioxide (CO2), temperature (T), relative humidity (RH), and fungi (as measure of bioaerosols). Indoor and outdoor sampling, as well as further methodology were described by Macedo et al.[9Macedo, A., O. Magalhães, A. Brito, and O. Mayan: Characterization of indoor environmental quality in primary schools in Maia: A Portuguese case study. Hum. Ecol. Risk Assess. An Int. J. 19:126136 (2013). [Taylor & Francis Online], [Web of Science ®][Google Scholar]]

Assessment of exposure to disinfectants

The aforementioned five clinics were also used to assess occupational exposure to disinfectants. All products used to disinfect, clean, and shine are alkaline compounds. Note that all workers wore gloves during the application of these products, and, therefore, this study did not assess the dose of dermal exposure. In addition to alkaline compounds, Mentaback composing of 47.5% (v/v) ethanol, 25% (v/v) 2-propanol, 25% (v/v) butanol, and 2.5% (v/v) glutaraldehyde is also used but only in the surgery room area due to its bactericidal, fungicidal, virucidal, and sporicidal properties. In this study, the air concentration of glutaraldehyde during the disinfection period of the surgery room was quantified. Only one worker (nurse or technician at each clinic) performs this activity (less than 5 min) with the door closed. Personal air samples were collected using a solid sorbent tube (previously impregnated with a derivatizing solution) connected to battery-powered air sampling pumps (Aircheck 2000, SKC, Ambicontrol, Lisboa, Portugal), operated at a flow rate of 200 mL/min. The air samples were collected and analyzed according to the National Institute for Occupational Safety and Health (NIOSH) 2532 method.[20National Institute for Occupational Safety and Health (NIOSH): Glutaraldehyde. Manual of Analytical Methods (Method 2532). Atlanta, GA: Center for Disease and Control, 1994. [Google Scholar]] The instrumental technique consisted of High Pressure Liquid Chromatography with UV detection (Thermo Finnigan UV2000, SpectraLab Scientific, Ontario, Canada).

Assessment of exposure to anesthetics gas

Monitoring of isoflurane was performed during dog surgeries. Personal air samples were collected in activated charcoal tubes (Coconut Shell Charcoal, Anasorb CSC, SKC, Ambicontrol, Lisboa, Portugal) connected to battery-powered air sampling pumps (Aircheck 2000, SKC) operated at a flow rate of 200 mL/min. Air samples were analyzed according to method MTA/MA-046/A00, developed by the Institut Nacional de Seguridad e Higiene en el Trabajo.[21Instituto Nacional de Seguridad e Higiene en el Trabajo (INSHT): Determinación de isoflurano en aire – Método de captación con muestreadores pasivos por difusión, desorción térmica/cromatografía de gases (Método MTA/MA-027/95) [Determination of isoflurane in air – Method of collection with passive diffusion samplers, thermal desorptiom/gas chromatography]. Madrid: Ministério de Trabajo y Assuntos Sociales, 1995 [Spanish]. [Google Scholar]] The instrumental technique consisted of 6890 N Series gas chromatography with detection by Flame Ionization (Agilent Technologies, Soquimica, Lisboa, Portugal).

Professionals' opinions regarding OSH issues

To evaluate workers' knowledge regarding workplace hazards, an interview-administered questionnaire was tested and validated among veterinary workers (n = 17) in a hospital located in Porto city (not included in this study) before it was employed in this study. The questionnaire was divided into 3 sections with 27 questions involving simple (yes/no), closed one-choice, and open-ended type questions: (i) socio-demographic characteristics of workers and type and duration of training received in OSH issues (10 questions); (ii) worker's opinion about work conditions in terms of OSH issues (7 questions); and (iii) worker's knowledge related to OSH issues (10 questions).

Results

Risk assessment

Table 1 shows the results of risk assessment for seven main working areas.

Table 1. Identification of occupational hazards and risk level by clinic working areas.

High-risk levels were found pertaining to X-ray radiation exposure and ergonomic related hazards. Three clinics did not have an isolated room for X-raying. From those with an isolated radiation room, four clinics were not legally inspected and authorized to perform X-raying by General Direction of Ministry of Health. Moreover, although all legal requirements for installation and equipment inspection were accomplished for one clinic, all veterinary workers (veterinarians, nurses, and technicians) denied use of PPE (apron, thyroid protector, gloves, and individual X-ray dosimeter). In addition, radiography was sometimes performed with the door opened.

This study also identified four basic activities that might increase the likelihood of musculoskeletal disorders: (i) working in an improper position (dental examination, ultrasound, surgery, surgery recovery treatments, and drug administration); (ii) work in a static position with arms extended (laboratory work, diagnostic exam, wound, and other treatments); (iii) forceful exertions (moving and lifting heavy animals or food bags); and (iv) repetitive movements (bathing, brushing, computer billing, and data entry).

The risks associated to physical hazards were chiefly bites and scratches followed by needle pricks and scalpel cuts. They frequently occurred in Office and Treatment rooms, because animals were away from their owner and thus got scared; hence, unexpected aggressive behavior occurred in response to any movement by veterinary workers. After animal scratches or cuts have occurred, veterinary workers who have been vaccinated promptly cleaned the wounds to avoid infections.

The risk associated with hand contact with chemicals was considered negligible, because all workers wore appropriate gloves during surgery (latex surgical gloves, powdered, and sterilized), treatment of animal wounds (latex examination gloves powdered), and when handling disinfectants for all types of surfaces and other chemicals in the laboratory (nitrile gloves powder-free). They did not complain about hand-related injuries either.

Although all clinics had Safety Data Sheets (SDS) for chemicals used in the veterinary practice, most workers were not aware of the presence and/or location of SDS. We observed that veterinary workers frequently eat and drink in animal handling areas and often fail to wash their hands prior to and after animal contact.

Indoor air quality

As shown in Table 2, the temperature ranges measured for all areas were above the maximum limit of the legal range (18 to 22°C),[22Portuguese Legislation (PL): Regulamento geral de higiene e segurança no trabalho em estabelecimentos comerciais, de escritório e serviços. [General regulation of health and safety at work in shops, offices and service buildings] (Decreto Lei n.°243/86) [Decree-Law]. Lisboa: Ministério do Trabalho e Segurança Social, 1986. [Google Scholar]] while the relative humidity was within or close to the range of comfortableness (50 to 70%).[22Portuguese Legislation (PL): Regulamento geral de higiene e segurança no trabalho em estabelecimentos comerciais, de escritório e serviços. [General regulation of health and safety at work in shops, offices and service buildings] (Decreto Lei n.°243/86) [Decree-Law]. Lisboa: Ministério do Trabalho e Segurança Social, 1986. [Google Scholar]]

Table 2. Summary of indoor air quality by clinic working areas.

For all clinics, the median and mean CO2 concentrations were lower than the Portuguese Legislation (PL) limit value of 2250 mg/m3.[23Portuguese Legislation (PL): Regulamento do desempenho energético dos edifícios de habitação e dos edifícios de comércio e serviços. [Regulation of the energy performance of housing, trade and service buildings] (Portaria n.° 353-A/2013) [Ordinance]. Lisboa: Ministérios do Ambiente, Ordenamento do Território e Energia, da Saúde e da Solidariedade, Emprego e Segurança Social, 2013. [Google Scholar]] Interestingly, CO2 concentration exceeded the PL value only in one measurement at the Office area (2309 mg/m3), in which three consecutive veterinary appointments (for ca. 3 h) occurred; all of them involved three people and the dog inside, with doors closed and without windows. This situation was atypical when compared to other appointments (CO2 ranged from 320 to 1258 ppm) that were shorter (ca. 20 min), and with an interval in between when the inside door remained open. Means and medians of PM10 concentrations for all clinic working areas were higher than the PL limit value of 100 μg/m3.[23Portuguese Legislation (PL): Regulamento do desempenho energético dos edifícios de habitação e dos edifícios de comércio e serviços. [Regulation of the energy performance of housing, trade and service buildings] (Portaria n.° 353-A/2013) [Ordinance]. Lisboa: Ministérios do Ambiente, Ordenamento do Território e Energia, da Saúde e da Solidariedade, Emprego e Segurança Social, 2013. [Google Scholar]] PM10 concentrations in Treatment area tend to be higher than in the other working areas but compared to the outside, the exposure levels were generally lower.

Measurement of TVOC was made randomly; therefore, there were times with higher concentrations of TVOC following treatment of wounds, cleaning, and disinfection, and others with lower values due to natural ventilation. The mean and median TVOC concentrations were higher than that enforced by the PL limit value (600 μg/m3)[23Portuguese Legislation (PL): Regulamento do desempenho energético dos edifícios de habitação e dos edifícios de comércio e serviços. [Regulation of the energy performance of housing, trade and service buildings] (Portaria n.° 353-A/2013) [Ordinance]. Lisboa: Ministérios do Ambiente, Ordenamento do Território e Energia, da Saúde e da Solidariedade, Emprego e Segurança Social, 2013. [Google Scholar]] except for the median value in the Reception area.

The fungal counts in Office and Treatment areas were lower than outside counts, which is in agreement with the reference conditions for microorganisms in PL.[23Portuguese Legislation (PL): Regulamento do desempenho energético dos edifícios de habitação e dos edifícios de comércio e serviços. [Regulation of the energy performance of housing, trade and service buildings] (Portaria n.° 353-A/2013) [Ordinance]. Lisboa: Ministérios do Ambiente, Ordenamento do Território e Energia, da Saúde e da Solidariedade, Emprego e Segurança Social, 2013. [Google Scholar]] On the other hand, the fungal counts in Reception area were higher than other areas.

Occupational exposure to glutaraldehyde

All samples collected from the surgery room of five clinics showed masses of glutaraldehyde below the limit of detection of the analytical method (0.3 μg) (results not shown).

Occupational exposure to isoflurane

Table 3 depicts the concentrations of waste anesthetic gas based on work conditions and surgery characteristics. The scavenging system generated considerably less emissions of isoflurane than the extractor system. Similar gas concentrations in air were found for scavenging system, regardless of the presence/absence of mechanical ventilation.

Table 3. Concentration of isoflurane based on work conditions and surgery characteristics.

Veterinary workers' opinion regarding OSH issues

In this study, 49 veterinary workers (73% female and 27% male) were involved and Figure 1 shows socio-demographic characteristics of the participants. Among those, about 10% of veterinary workers had OSH-related trainings.

Figure 1. Socio-demographic characteristics of the veterinary workers (n = 49) in 15 clinics: a) age, b) academic degree, and c) years of experience.

Most workers stated that the clinics provided necessary PPE (88%) but no written OSH good practices were available (94%). In addition, 84% of workers confirmed that they used the PPE, but only 35% of them claimed that the OSH service of private (hired) enterprise was adequate to their activities; 2% stated that such an OSH service did not exist at all.

Everyone had the opinion that his/her work involves some risk of accident and development of an occupational disease. The most frequently mentioned risks were in the order of biological-related risk (49%; typically zoonosis), ergonomic-related risk (33%; typically moving and lifting heavy animals), chemical-related risk (12%; typically exposure to anesthetic gas), and physical-related risk (6%; typically scratches and bites).

The factors pointed out by Portuguese veterinary workers as deterrents for using PPE were (by decreasing order of importance): (i) adverse animal reactions; (ii) concerns about heat stress; (iii) negative client perceptions; and (iv) lack of information of how to use it properly. On the other hand, factors that promoted use of PPE were by (decreasing order of importance): (i) liability issues; (ii) perceived risk to zoonotic diseases; and (iii) health problems arising from exposure to X-rays.

Discussion

Risk assessment

From a review on occupational hazards associated with veterinarian practice,[4Bonini, S., A. Buonacucina, L. Selis, A. Peli, A. Mutti, and M. Corradi: Occupational hazards in veterinarians: An updating. J. Vet. Sci. Technol. 7:317 (2016). [Google Scholar]] only limited information was found dealing with risk assessment and indoor air quality (IAQ) evaluation. This partially justified the relevance of our study in attempts to identify hazards in veterinary activities (see Table 1).

The lack of preventive measures during radiography of animals observed in this study was also reported elsewhere.[24–26Shirangi, A., L. Fritschi, and C. Holman: Prevalence of occupational exposures and protective practices in Australian female veterinarians. Aust. Vet. J. 85:3238 (2007). [Crossref], [PubMed], [Web of Science ®][Google Scholar]Hall, A., Davies Hugh, P. Demers, A. Nicol, and C. Peters: Occupational exposures to antineoplastic drugs and ionizing radiation in Canadian veterinary settings: Findings from a national surveillance project. Can. J. Public Health 104:e460e465 (2013). [Crossref], [PubMed], [Web of Science ®][Google Scholar]Fritschi, L., A. Shirangi, I. Robertson, and L. Day: Trends in exposure of veterinarians to physical and chemical hazards and use of protection practices. Int. Arch. Occup. Environ. Health 81:371378 (2008). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] A national survey made in Canada indicated that about 3%–8% of all veterinary workers were exposed to an annual ionizing radiation dose above 0.1 mSv, although still below regulatory limits.[25Hall, A., Davies Hugh, P. Demers, A. Nicol, and C. Peters: Occupational exposures to antineoplastic drugs and ionizing radiation in Canadian veterinary settings: Findings from a national surveillance project. Can. J. Public Health 104:e460e465 (2013). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] However, use of PPE for ionizing radiation has increased with recent graduates as compared to earlier ones.[26Fritschi, L., A. Shirangi, I. Robertson, and L. Day: Trends in exposure of veterinarians to physical and chemical hazards and use of protection practices. Int. Arch. Occup. Environ. Health 81:371378 (2008). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

Other studies[27–30Berry, S., P. Susitaival, A. Ahmadi, and M. Schenker: Cumulative trauma disorders among California veterinarians. Am. J. Ind. Med. 55:855861 (2012). [Crossref], [PubMed], [Web of Science ®][Google Scholar]MacDonald, K., and D. King: Work-related musculoskeletal disorders in veterinary echocardiographers: A cross-sectional study on prevalence and risk factors. J. Vet. Cardiol. 16:2737 (2014). [Crossref], [PubMed], [Web of Science ®][Google Scholar]Szeto, G., P. Ho, A. Ting, J. Poon, S. Cheng, and R. Tsang: Work-related musculoskeletal symptoms in surgeons. J. Occup. Rehabil. 19:175184 (2009). [Crossref], [PubMed], [Web of Science ®][Google Scholar]Smith, D., N. Wei, Y. Zhang, and R. Wang: Musculoskeletal complaints and psychosocial risk factors among physicians in mainland China. Int. J. Ind. Ergon. 36:599603 (2006). [Crossref], [Web of Science ®][Google Scholar]] reported similar results to those obtained in our study about ergonomic issues. Workers exhibited discomfort mainly all over the entire body. Pain associated with performing surgeries and ultrasound was recorded in 99% of surgeons and 44% of veterinary echocardiographers; their lifestyle has changed and decreased work productivity, including premature termination of career.[28MacDonald, K., and D. King: Work-related musculoskeletal disorders in veterinary echocardiographers: A cross-sectional study on prevalence and risk factors. J. Vet. Cardiol. 16:2737 (2014). [Crossref], [PubMed], [Web of Science ®][Google Scholar],29Szeto, G., P. Ho, A. Ting, J. Poon, S. Cheng, and R. Tsang: Work-related musculoskeletal symptoms in surgeons. J. Occup. Rehabil. 19:175184 (2009). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] Engineering control measures should be adopted with regard to equipment displacement and animal lifting. Training about ergonomic-related hazards and MSD should be provided to workers, especially surgeons. In addition, an implementation of workplace fitness program within clinic would help.

A study based on insurance data showed that animals are the most frequent cause of occupational accidents among veterinary workers (66%); most of them included bites or scratches.[3Nienhaus, A., C. Skudlik, and A. Seidler: Work-related accidents and occupational diseases in veterinarians and their staff. Int. Arch. Occup. Environ. Health 78:230238 (2005). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] Lucas et al.[1Lucas, M., L. Day, A. Shirangi, and L. Fritschi: Significant injuries in Australian veterinarians and use of safety precautions. Occup. Med. 59:327333 (2009). [Crossref][Google Scholar]] reported that bites from dogs accounted for 35% of the injuries associated with anesthetic procedure, which shows an agreement with our study. Practically speaking, bites and scratches are difficult to avoid in small animal veterinary practice. However, proper restraint, both manual (muzzle) and chemical (sedative) can reduce such a risk. Another physical-related risk was handling of needles. Recapping needles is significantly associated with needle stick injuries,[31Wright, J., S. Jung, R. Holman, N. Marano, and J. McQuiston: Infection control practices and zoonotic disease risks among veterinarians in the United States. J. Am. Vet. Med. Assoc. 232:18631872 (2008). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] and is necessary to ensure that approved sharp containers are available in the close proximity of where needles are used;[32Riley, C., S. McCallum, J. MacDonald, and K. Hill: A prospective observational study of needle-handling practices at a University Veterinary Teaching Hospital. N. Z. Vet. J. 64:117120 (2016). [Taylor & Francis Online], [Web of Science ®][Google Scholar]] the major causes of unsafe needle handling in this study were lack of OSH information and proper care. Burns are more likely to occur from excess heat from steam valves of autoclaves.[6Jeyaretnam, J., and H. Jones: Physical, chemical and biological hazards in veterinary practice. Aust. Vet. J. 78:751758 (2000). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] In this study, the risk level associated with handling autoclaves was acceptable because most workers used gloves.

Animal contact and oral exposure were the major vectors of exposure to zoonosis in our study. According to Jackson and Villarroel,[5Jackson, J., and A. Villarroel: A survey of the risk of zonoses for veterinarians. Zoonoses Public Health 59:193201 (2012). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] the exposure to biological agents via contact, oral exposure, skin breaks, and inhalation was 57%, 22%, 16%, and 5%, respectively. Additionally, training must be given to veterinary workers regarding excessive use of antimicrobial agents, considering that efforts have been taken in European countries to limit use of such chemicals.[33Törneke, K., and J. Torren-Edo: The management of risk arising from the use of antimicrobial agents in veterinary medicine in EU/EEA countries–A review. J. Vet. Pharmacol. Ther. 38:519528 (2015). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

Latex was considered the second most important allergen in a veterinary's practice due to skin reaction to latex gloves.[34Leggat, P., D. Smith, and R. Speare: Hand dermatitis among veterinarians from Queensland, Australia. Contact Dermatitis 60:336338 (2009). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] In this study, veterinary workers wore latex powdered gloves and none of them showed skin reaction or complained about it. Nevertheless, the best recommendations are to replace powdered latex gloves by powder-free ones.

Indoor air quality

The indoor air temperature was higher than the maximum comfortable limit due to the presence of humans and animals in small working areas and absence of air conditioning. For a few clinics, although the air-conditioning system exists, it was frequently off. The use of natural and mechanical ventilation, even in some with air-conditioning systems as reported by Caballero and Cartín,[35Caballero, M., and V. Cartín: Calidad del aire en dos centros hospitalarios y ocho clínicas veterinarias en Costa Rica [Air quality in two hospital centers and eight veterinary clinic in Costa Rica]. Rev. Costarricense de Salud Pública 30:1726 (2009) [Spanish]. [Google Scholar]] appears to be common in veterinary clinics. Considering that measurements were made throughout the whole year (including summer and winter periods), one would expect significant changes in temperature and relative humidity values. However, during our study, the weather conditions prevailing in Maia county (and north of Portugal at large) were not regular, because the summer was rainy and the winter drier than usual. Nevertheless, the use of appropriate clothes, air-condition system, and ventilation system can easily adjust temperature and relative humidity to better comfort levels in environmental working areas.

From the eight veterinary clinics studied in Costa Rica,[35Caballero, M., and V. Cartín: Calidad del aire en dos centros hospitalarios y ocho clínicas veterinarias en Costa Rica [Air quality in two hospital centers and eight veterinary clinic in Costa Rica]. Rev. Costarricense de Salud Pública 30:1726 (2009) [Spanish]. [Google Scholar]] similar results to this study were found: concentrations of CO2 were higher inside than outside the clinic, although lower than regulatory limit; as well as concentration means and medians of PM10 inside the clinic were higher than the regulatory limit. The main causes were occupancy of people, closed doors, and poor ventilation. Considering that the legal requirement of incoming air ventilation filters was fulfilled in all clinics,[36Portuguese Legislation: Regulamento da actividade dos Centros de Atendimento Médico-Veterinário (CAMV), como unidades de saúde ambiental onde se prestam serviços de prevenção, diagnóstico e tratamento das doenças dos animais. [Regulation of the activity of the Medical Veterinary Sevices Centers, and environmental health facilities where they provide for prevention, diagnosis and treatment of animal diseases] (Decreto Lei n.° 184/2009) [Decree-Law]. Lisboa: Ministério da Agricultura, do Desenvolvimento Rural e das Pescas, 2009. [Google Scholar]] PM10 concentrations inside of the clinics should be lower than outside. In the present study, overall, the PM10 concentrations inside and outside the clinics were not considerably different because of several veterinary activities (such as shaving, brushing, animal exercising, and brooming) generating dust and increasing the PM10 concentrations inside the clinics. Some veterinary workers complained about eye and nose itching; as a result, the following control measures were suggested to minimize contact with and inhalation of particulate matter: (i) use of semifacial mask PFF1 during cutting and drying animal hair, (ii) uniform change after these activities, and (iii) floor cleaning using vacuuming air instead of a broom.

In the Treatment and Office working areas, treatment of wounds was frequently done; as a result, the TVOC median concentrations were higher than in the Reception area. During animal treatment, all clinics used organic volatile compounds in aqueous solutions, such as 70% (v/v) Ethanol, Betadine (10% (v/v) providone-iodine and 1% (v/v) glycerol), and Chlorhexidine (0.05% (v/v) chlorhexidine gluconate). However, there is an occupational risk associated with volatile organic compounds in cleaning and disinfection activities. Replacement of those compounds by alkalis happens in some clinics as mentioned elsewhere.[6Jeyaretnam, J., and H. Jones: Physical, chemical and biological hazards in veterinary practice. Aust. Vet. J. 78:751758 (2000). [Crossref], [PubMed], [Web of Science ®][Google Scholar],10Murphy, C., R. Reid-Smith, J. Weese, and S. McEwen: Evaluation of specific infection control practices used by companion animal veterinarians in community veterinary practices in southern Ontario. Zoonoses Public Health 57:429438 (2010). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] In this study, all clinics used alkaline compounds such as Klorkleen (sodium troclosene/adipic acid/tartazine/sodium dodecylbenzenesulfate) and Corlimp (quartz (silica)/ammonium hydrogen carbonate) in general cleaning and disinfection activities. For more efficient disinfection of the surgery room, they also used Mentaback. Additionally, occupational exposure to glutaraldehyde will be discussed in the following sections. Fungal counts in this study were lower than that reported by Caballero and Cartín.[35Caballero, M., and V. Cartín: Calidad del aire en dos centros hospitalarios y ocho clínicas veterinarias en Costa Rica [Air quality in two hospital centers and eight veterinary clinic in Costa Rica]. Rev. Costarricense de Salud Pública 30:1726 (2009) [Spanish]. [Google Scholar]] Dirty floors, bad hygiene practices, and inexistence of air circulation/filtration system were the major reasons for the high counts in Costa Rica clinics.[35Caballero, M., and V. Cartín: Calidad del aire en dos centros hospitalarios y ocho clínicas veterinarias en Costa Rica [Air quality in two hospital centers and eight veterinary clinic in Costa Rica]. Rev. Costarricense de Salud Pública 30:1726 (2009) [Spanish]. [Google Scholar]] In the Reception area, the fungal counts were similar to outside counts; this can be explained by the open door in the Reception Space (although it depended on the weather and occupancy).

Occupational exposure to glutaraldehyde

Studies reported that toxic respiratory diseases were related to disinfectant agents.[3Nienhaus, A., C. Skudlik, and A. Seidler: Work-related accidents and occupational diseases in veterinarians and their staff. Int. Arch. Occup. Environ. Health 78:230238 (2005). [Crossref], [PubMed], [Web of Science ®][Google Scholar],10Murphy, C., R. Reid-Smith, J. Weese, and S. McEwen: Evaluation of specific infection control practices used by companion animal veterinarians in community veterinary practices in southern Ontario. Zoonoses Public Health 57:429438 (2010). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] As previously explained, the most important volatile organic compound found in disinfectant formulation is glutaraldehyde. The major symptoms from the high level of toxicity in glutaraldehyde are irritation of the eye, upper-respiratory tract, and skin, as well as injury to the central nervous system. Hence, it is important to quantify the occupational exposure to this chemical. The present study shows that the concentration of glutaraldehyde is below the limit of the analytical method; as a result, we assumed that workers' exposure to this chemical was insignificant.

Occupational exposure to isoflurane

NIOSH recommends that personnel should not be exposed to halogenated anesthetic gas concentrations in excess of 2 ppm on average for any period longer than one hour.[37National Institue for Occupational Safety and Health (NIOSH): Criteria for a Recommended Standard: Occupational Exposure to Waste Anesthetic Gases and Vapors. DHHS (NIOSH) Publication Number 77–140. Atlanta, GA: Center for Disease Control and Prevention, 1977. [Google Scholar]] This statement does not imply that <2 ppm is safe or >2 ppm unsafe, since any degree of exposure would be unacceptable. The Portuguese Institute for Quality through Standard NP 1796:2014 set exposure limits only for halothane (50 ppm).[38CT42 – CERTITECNA: Valores Limites de Exposição Profissional a Agentes Químicos [Occupational Exposure Limits to Chemical Agents]. (NP 1796). [Standard]: Instituto Português de Qualidade, 2014 [Portuguese]. [Google Scholar]] We accordingly decided to use the value of 2 ppm as recommended exposure limit for further discussion.

Our results for waste anesthetic gas concentrations were similar to those by Canadian and Austrian studies.[12Friembichler, S., P. Coppens, H. Sare, and Y. Moens: A scavenging double mask to reduce workplace contamination during mask induction of inhalation anesthesia in dogs. Acta Vet. Scand. 53:17 (2011). [Crossref], [PubMed], [Web of Science ®][Google Scholar],39Korczynski, R.: Anesthetic gas exposure in veterinary clinics. Appl. Occup. Environ. Hyg. 14:384390 (1999). [Taylor & Francis Online][Google Scholar]] The Canadian study reported isoflurane exposures between 1.3 to 13 ppm with a mean of 5.3 ± 2.7 ppm collected from six small clinics.[39Korczynski, R.: Anesthetic gas exposure in veterinary clinics. Appl. Occup. Environ. Hyg. 14:384390 (1999). [Taylor & Francis Online][Google Scholar]] The Austrian study reported that the maximum isoflurane concentrations ranged from 0.7 to 2.8 ppm and from 8.3 to 43.7 ppm, in a group of six dogs when the scavenging function was performed or disabled, respectively.[12Friembichler, S., P. Coppens, H. Sare, and Y. Moens: A scavenging double mask to reduce workplace contamination during mask induction of inhalation anesthesia in dogs. Acta Vet. Scand. 53:17 (2011). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

Some studies[11Sakhvidi, M., A. Bahrami, A. Ghiasvand, H. Mahjub, and L. Tuduri: Determination of inhalational anesthetics in field and laboratory by SPME GC/MS. Anal. Lett. 45:375385 (2012). [Taylor & Francis Online], [Web of Science ®][Google Scholar],12Friembichler, S., P. Coppens, H. Sare, and Y. Moens: A scavenging double mask to reduce workplace contamination during mask induction of inhalation anesthesia in dogs. Acta Vet. Scand. 53:17 (2011). [Crossref], [PubMed], [Web of Science ®][Google Scholar],39Korczynski, R.: Anesthetic gas exposure in veterinary clinics. Appl. Occup. Environ. Hyg. 14:384390 (1999). [Taylor & Francis Online][Google Scholar],40Nesbitt, J., D. Krageschmidt, and M. Blanco: A novel approach to scavenging anesthetic gases in rodent surgery. J Occup Env. Hyg 10:D12531 (2013). [Taylor & Francis Online], [Web of Science ®][Google Scholar]] reported that an extractor gas system generated higher worker's exposures to isoflurane than a scavenging system, as also observed in this study. These findings indicate that it is likely that veterinary workers might be exposed to isoflurane levels higher than 2 ppm when the extractor system is employed. Thus, for those having the extractor system, additional control methods are required to minimize exposures to isoflurane or employers must consider changing their system to a scavenging waste anesthetic gas system. In addition, Portuguese veterinarians must be aware and educated to reduce unintended exposure, more likely through leakage of anesthetic gases from equipment and from around the animal face mask.

Sakhvidi et al.[11Sakhvidi, M., A. Bahrami, A. Ghiasvand, H. Mahjub, and L. Tuduri: Determination of inhalational anesthetics in field and laboratory by SPME GC/MS. Anal. Lett. 45:375385 (2012). [Taylor & Francis Online], [Web of Science ®][Google Scholar]] proved that humidity has a strong effect on sampling rate, but increasing humidity from 50% to 80% caused only ca. 10% change in the sampling rate. In the present study, an effect of humidity on isoflurane concentrations among clinics cannot be determined because humidity throughout the sampling period was similar.

Veterinary workers' opinions regarding OSH issues

A higher percentage of female than male in this type of profession is consistent with results reported in other countries, such as the United Kingdom, the United States, Canada and Australia.[6Jeyaretnam, J., and H. Jones: Physical, chemical and biological hazards in veterinary practice. Aust. Vet. J. 78:751758 (2000). [Crossref], [PubMed], [Web of Science ®][Google Scholar],13Epp, T.: Occupational health hazards in veterinary medicine: physical, psychological and chemical hazards. Can. Vet. J. 53:151157 (2012). [PubMed], [Web of Science ®][Google Scholar],17Dowd, K., M. Taylor, J. Toribio, C. Hooker, and N. Dhand: Zoonotic disease risk perceptions and infection control practices of Australian veterinarians: Call for change in work culture. Prev. Vet. Med. 111:1724 (2013). [Crossref], [PubMed], [Web of Science ®][Google Scholar],40Nesbitt, J., D. Krageschmidt, and M. Blanco: A novel approach to scavenging anesthetic gases in rodent surgery. J Occup Env. Hyg 10:D12531 (2013). [Taylor & Francis Online], [Web of Science ®][Google Scholar],41Allweiler, S., and L. Kogan: Inhalation anesthetics and the reproductive risk associated with occupational exposure among women working in veterinary anesthesia. Vet. Anaesth. Analg. 40:285289 (2013). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] Workers' ages and years of experience can be explained by the recent demand for small animal treatments (such as dental examination and neutering surgery), as well as for beauty care (bathing and brushing), which consequently increased the number of veterinary clinics operating in Portugal. Additionally, this profession requires physical effort and adaptation to work shift schedules, more likely to be accepted by young people.

Considering the lack of information and training in OSH among veterinary workers, we recommend that Portuguese veterinary schools incorporate preventive measures in their syllabi to make new graduates aware of OSH-related hazards. This suggestion was already proposed in two studies originating in Germany[15Kozak, A., G. Schedlbauer, C. Peters, and A. Nienhaus: Self-reported musculoskeletal disorders of the distal upper extremities and the neck in German veterinarians: A cross-sectional study. PLoS One 9:e89362 (2014). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] and the United States.[27Berry, S., P. Susitaival, A. Ahmadi, and M. Schenker: Cumulative trauma disorders among California veterinarians. Am. J. Ind. Med. 55:855861 (2012). [Crossref], [PubMed], [Web of Science ®][Google Scholar]]

Although an Australian study showed that 24% (n = 87) of workers believed that exposure to X-rays was a major occupational health and safety issue,[42Phillips, M., J. Jeyaretnam, and H. Jones: Disease and injury among veterinarians. Aust. Vet. J. 78:625629 (2000). [Crossref], [PubMed], [Web of Science ®][Google Scholar]] Portuguese workers did not express a concern therewith. Portuguese veterinary workers from all 15 clinics did not report symptoms of stress and emotional fatigue, although these were considered as an emerging risk in veterinary practices.[4Bonini, S., A. Buonacucina, L. Selis, A. Peli, A. Mutti, and M. Corradi: Occupational hazards in veterinarians: An updating. J. Vet. Sci. Technol. 7:317 (2016). [Google Scholar]] However, physical fatigue was an important health issue reported by nurses from three clinics that handled more animals per day. They reported a demanding work load considering the long duration and rotating shift work schedules. Furthermore, they are required to perform activities that do not need specific knowledge of veterinary medicine, such as cleaning of animal areas, beauty treatments, animal feeding, reception, telephone calls, and storage of materials and animals' food.

Conclusions

Our study reports risk assessment (identifying occupational hazards, determining risk levels, and suggesting preventive/protective measures) covering the main activities incurred in small animal practice and clinical areas. As of now, this comprehensive approach has not been applied to veterinary activities. As far as our knowledge goes, this is the second study that quantifies the IAQ in veterinary clinics. Some IAQ parameters did not adhere to the regulatory limits; attention to temperature and concentrations of TVOC and PM10 is required.

Overall, veterinary workers were aware of physical, ergonomic, chemical, and biological hazards, but they did not react proactively to change their attitudes. Although the ultimate responsibility lies with the employer to enforce all OSH standards and provide a safe and healthy work environment, it is also crucial that veterinary workers themselves participate in the planning of preventive measures. Thus, it is strongly recommended that employers place additional control methods, along with the provisions of OSH information and training. In addition, provision of OSH education and training at Portuguese veterinary schools should help students' awareness regarding OSH issues.

Acknowledgments

The authors would like to thank all clinic workers for their collaboration and availability.

Additional information

Funding

The authors would like to thank MAIEUTICA – Cooperativa do Ensino Superior, C.R.L. for financial support.

References

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