Airborne bacteria and fungi associated with waste-handling work Donguk Park1, Seunghun Ryu1, Shinbum Kim2, Hyaejeong Byun3, Chungsik Yoon3, Kyeongmin Lee4 1
Department of Environmental Health, Korea National Open University, Korea, 2Wonjin Institute for Occupational and Environmental Health, Korea, 3Dept. of Environmental Health, Graduate School of Public Health, Seoul National University, Korea, 4Occupational Lung Diseases Institute, Korea
Background: Municipal workers handling household waste are potentially exposed to a variety of toxic and pathogenic substances, in particular airborne bacteria, gram-negative bacteria (GNB), and fungi. However, relatively little is known about the conditions under which exposure is facilitated. Methods: This study assessed levels of airborne bacteria, GNB, and fungi, and examined these in relation to the type of waste-handling activity (collection, transfer, transport, and sorting at the waste preprocessing plant), as well as a variety of other environmental and occupational factors. Airborne microorganisms were sampled using an Andersen single-stage sampler equipped with agar plates containing the appropriate nutritional medium and then cultured to determine airborne levels. Samples were taken during collection, transfer, transport, and sorting of household waste. Multiple regression analysis was used to identify environmental and occupational factors that significantly affect airborne microorganism levels during waste-handling activities. Results: The ‘‘type of waste-handling activity’’ was the only factor that significantly affected airborne levels of bacteria and GNB, accounting for 38% (P50.029) and 50% (P50.0002) of the variation observed in bacteria and GNB levels, respectively. In terms of fungi, the type of waste-handling activity (R250.76) and whether collection had also occurred on the day prior to sampling (P,0.0001, R250.78) explained most of the observed variation. Given that the type of waste-handling activity was significantly correlated with levels of bacteria, GNB, and fungi, we suggest that various engineering, administrative, and regulatory measures should be considered to reduce the occupational exposure to airborne microorganisms in the wastehandling industry. Keywords: Household waste, Microorganism, Bioaerosol
Introduction Household waste refers to mixed waste streams derived from domestic activity that typically require any form of pre-processing or sorting before they can be properly disposed. For example, biodegradable food and kitchen wastes are generally separated from total household waste, as are recyclable materials such as metal, wood, paper, glass, aluminum cans, and plastic. Although some wastes may be sorted at the source (e.g. home or office), most wastehandling activities are carried out by municipal workers. Although they may wear protective equipments, these workers are in some degree of contact with household waste from the time of collection through to final disposal in a landfill or incinerator. This is a concern because when biodegradable waste Correspondence to: Donguk Park, Department of Environmental Health, Korea National Open University, 169 Dongsung-dong, Jongroku, Seoul, Korea. Email: [email protected]
ß W. S. Maney & Son Ltd 2013 DOI 10.1179/2049396713Y.0000000036
is handled, organic particles (including microorganisms) can be aerosolized, and waste handlers may consequently be exposed to multiple pathogenic agents, including bacteria, endotoxins, mold spores, glucans, volatile organic compounds, and even infectious materials.1 Such exposure may underlie reports of respiratory complaints, gastrointestinal problems, eye and skin irritation, and symptoms of toxic organic dust syndrome among workers collecting the organic fraction of household waste.2,3 Waste collectors around the world are at risk for workrelated disorders and injuries. There is increasing evidence that the incidence of work-related pulmonary illness is high among waste collectors.1,2,4 Despite these reports, relatively little is known regarding the environmental and occupational factors that contribute to exposure to aerosolized microorganisms during waste handling. Specific wastehandling activities, such as collection, sorting, and
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disposal, may differentially affect levels of microorganisms and their toxins in organic dusts. Additionally, other environmental and occupational factors in waste handling may be associated with the generation of potentially harmful bioaerosols. To date, numerous factors have been reported to influence working conditions and hence the level of potential exposure among waste collectors. Such factors include the type of company (private or governmental), organization of work, type of equipment, type of district, type of waste, frequency of collection, and seasonal variation.2,4,5 To our knowledge, no study has previously examined how the type of waste-handling activity affects airborne levels of microorganism. Accordingly, we identified the factors responsible for worker exposure to airborne bacteria and fungi in typical exposure scenarios and examined levels of exposure with respect to several environmental and occupational characteristics.
Methods Brief description of household waste handling activities in Korea Throughout the entire process of waste collection and disposal, waste handlers may participate in a variety of activities that may differentially influence exposure to hazardous agents. Accordingly, we defined four activity groups based on the routing of wastes, different types of wastes, working conditions, and common practices, in such a way that potential differences in bioaerosol exposure within the same activity group were minimized, and contrast among groups was maximized. Waste handling involves a number of different waste streams, including source-separated biodegradable waste (i.e., food waste from homes, and restaurants), source-separated non-biodegradable waste (recyclable and reusable materials), and non-separated wastes. Waste handling also involves a number of process steps. First, all wastes are collected from fixed sites and loaded into small vehicles or motorcycles equipped with small containers. Second, the waste from several districts is transferred from smaller collection vehicles to larger transport equipment. The transferring and agitation of waste may expose waste collectors riding at the back end of the truck to bioaerosols. Larger transport trucks make frequent stops to pick up municipal waste. Thus, waste collectors usually stand outside and at the rear end of the truck to facilitate getting on and off the truck during these frequent stops. Third, the waste is transported, usually over long distances, to a material processing plant. During this time, personnel riding in the vehicle cab may be exposed to bioaerosols from contaminated hands or clothing. Finally, having reached the material processing plant, waste is sorted to remove valuable recyclables or reusable materials.
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Biodegradable or food waste is sent for further processing into organic fertilizer or animal food, whereas non-separated waste (e.g., leaves, vegetables, dead animals, feces, and other non-usable wastes) is transported directly to a landfill or incinerator. This study focused on the generation of airborne microorganisms during waste collection, transfer, transport, and sorting at the material processing plant; potential exposure at disposal sites (incinerator or landfill) was excluded.
Sampling of airborne microorganisms Levels of airborne bacteria, gram-negative bacteria (GNB), and fungi were analyzed according to wastehandling activity (collection, transfer, transport, and sorting). Air samples were collected using an Andersen one-stage cascade sampler either fixed in place or moved around between the heights of 1.2 and 1.5 m to simulate the inhalation and exposure of waste handlers. Air was drawn through the sampler at a flow rate of 28.3 l/minute for less than 5 minutes; a short sampling period was selected to avoid overloading the plates such that distinct colonies could not be enumerated. The time-weighted average (TWA) was calculated over the 5-minute sampling interval during each waste-handling activity. Airborne microorganisms were sampled using a 20 ml nutrient plate (tryptic soy agar for bacteria, MacConkey agar for GNB, and sabouraud dextrose agar with chloramphenicol for fungi) coupled inside the stage sampler. When changing the collection plates, the stage hole was sterilized with a 70% ethanol solution to prevent cross-contamination. An IAQ-Calc Indoor Air Quality Meter (Model 8762; TSI, Inc., Shoreview, Minnesota, USA) was used to simultaneously monitor air temperature and humidity during each sampling interval. Data were logged every 30 seconds, and a TWA was used in the data analysis. Bioaerosol and air quality data were collected during the day from 06:00 to 18:00 and at night from 18:00 to 06:00. After sample collection, the agar plates were transported to the laboratory and incubated at 37¡1uC for 2 days for bacteria and GNB or at 25¡1uC for 4 days for fungi.6 Specific statistical corrections were made using correction factors obtained for each growing medium from the Conversion Tables provided with the Anderson one-stage sampler operating manual.7 The microbial counts were expressed in terms of colony forming units (CFU) per unit volume of air (m3). Total culturable bacterial and fungal counts were compared to ambient environmental (background) levels to determine the exposure to microorganisms generated during household waste handling. Our microbial sampling strategy was designed to best represent the
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level of microorganisms generated during typical household waste handling.
Data analysis Descriptive statistics, correlation analysis, t-tests, and univariate and multiple regression analyses were conducted using Stata Version 11.0 (Stata Corp. LP, College Station, Texas, USA). Initially, the distributions of bacteria, GNB, and fungi were skewed; to improve our statistical models, all microorganism data were log-transformed.
Airborne bacteria and fungi in waste-handling
In addition to the microorganism data (dependent variable), we reviewed the literature to identify a number of environmental and occupational factors (independent variables) that are likely to influence airborne levels of bacteria, GNB, and fungi during waste handling (Table 1). We also included variables related to the four specific waste-handling works or activities (collection, transfer, transport, and sorting) that were intended to isolate and maximize differences in exposure conditions. Simple linear regression was performed to examine their relationship with the
Table 1 Description of occupational and environmental variables related to waste collection Independent variable
Number of samples
Description (number of samples)
City Seoul Local
11 22
One district in Seoul Three cities within Gyeonggi Province: Guri (n53); Uijeongbu (n53); Pyungtaek (n516)
Weather on day prior to sampling Sunny Other
10 23
Sunny Rainy (n511); cloudy (n53); humid (n59)
Weather during sample collection Sunny Cloudy
30 3
Sunny Overcast and humid
Season Summer Fall
27 6
Samples collected during August (n527) Samples collected during September (n53) and October (n53)
Collection day Week day
22
Weekend
11
Samples collected on Monday (n59), Tuesday (n53), and Wednesday (n510) Samples collected on Sunday
Waste collection on day prior to sampling Yes
11
No
22
Type of company Government Private Type of waste Street
5 28 5
Household Food garbage Reusable
9 11 8
Type of wastehandling activity Sorting Collection Transfer
7 12 11
Transport Waste-handling location Indoor Outdoor Collection time Day Night Total
If waste was not collected on the day before sampling, waste accumulation was likely to have occurred.
Local government tends to contract out waste collection work. Workers employed at private company may have much waste Waste collected from either stationary containers or various types of waste discarded on the street Non-separated waste from households or restaurants Separated food waste from household or restaurants Reusable wastes (separated), such as paper, wood, metal, glass, etc.
3
To select reusable waste from non-separated waste To collect waste at fixed sites and load into vehicle To transfer from smaller collection vehicles to larger transport equipment Inside vehicle
8 25
Sorting work occurred indoors Collection and transport activities occurred outdoors
22 11 33
Waste collected between 06:00 and 18:00 Waste collected between 18:00 and 06:00
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observed quantitative variables (air temperature, humidity, and airborne microorganism levels). Analysis of variance (ANOVA) was used to compare mean microorganism levels among categories of qualitative variables. Only variables with P-values ,0.25 were introduced to our multiple regression analysis.8 Finally, stepwise analysis was used to identify factors that significantly affected airborne levels of bacteria, GNB, and fungi. Categories serving as a reference group for comparing with other groups were given a value of zero.
microorganism levels were regressed against quantitative environmental factors such as air temperature and humidity and compared among qualitative environmental and occupational categories (Table 2). Simple linear regression showed that air humidity accounted for 12.3% of the variation observed in airborne fungi generated during waste handling (P50.0258), while airborne bacteria and GNB levels were not associated with changes in temperature at P,0.05(results are not shown). Occupational and environmental factors affecting airborne bacteria included ‘‘season’’ (P50.157), ‘‘type of waste’’ (P50.0517), and ‘‘type of waste-handling activity’’ (P50.0029). In addition to these factors, ‘‘type of waste collection company’’ (P50.1805) was also significantly associated with airborne GNB levels at P,0.25. Regarding fungi, all
Results The mean levels of airborne microorganisms were 1.66104 CFU/m3 for bacteria, 1.46104 CFU/m3 for GNB, and 1.86104 CFU/m3 for fungi. Airborne Table 2 Levels of airborne environmental variables
bacteria,
gram-negative
bacteria
Bacteria, CFU/m3 Independent variable City Seoul Local cities Weather on day prior to sampling Sunny Other Weather on day of sampling Sunny Other Season Summer Fall Collection day Week day Weekend Waste collection on day prior to sampling On Off Type of organization Government Private Type of waste handled Street Household Food garbage Reusable Type of wastehandling work Sorting Collection Transfer Transport (inside car) Location where waste is handled Indoor Outdoor Waste collection time Day (06:00218:00) Night (18:00206:00) Total
No. of sample
Mean
SE
(GNB),
and
fungi
according
GNB, CFU/m3
P-value
Mean
SE
to
occupational
and
Fungi, CFU/m3 P-value
Mean
SE
P-value
11 22
1.76104 8.06103 NS 1.66104 3.46103
2.26104 9.56103 NS 1.76104 4.46103
4.36104 1.26104 ,0.0001 5.46103 1.16103
10 23
2.26104 6.26103 NS 1.46104 4.16103
2.36104 6.76103 NS 1.66104 5.46103
7.36103 1.96103 0.1396 2.36104 7.16103
30 3
1.76104 3.76103 NS 1.56104 5.66103
2.06104 4.66103 NS 7.76103 6.06103
1.96104 5.66103 NS 6.26103 1.76103
27 6
1.86104 4.06103 0.1570 8.26103 4.06103
2.26104 4.96103 0.0252 4.26103 3.26103
2.16104 6.16103 0.1464 3.36103 1.56103
22 11
1.66104 3.46103 NS 1.76104 8.06103
1.76104 4.46103 NS 2.26104 9.56103
5.46103 1.16103 ,0.0001 4.36104 1.26104
11 22
2.06104 5.66103 NS 1.46104 4.26103
2.16104 6.46103 NS 1.76104 5.46103
6.76103 1.86103 0.0697 2.46104 7.46103
5 28
8.86103 4.26103 NS 1.86104 3.96103
5.46103 3.76103 0.1805 2.16104 4.86103
2.36103 8.06102 0.0519 2.16104 5.96103
5 9 11 8
8.86103 2.36104 6.86103 2.76104
4.26103 0.0517 9.46103 2.06103 6.46103
5.46103 3.06104 8.66103 2.86104
3.76103 0.0594 1.16104 5.36103 6.66103
2.36103 3.26104 2.06104 9.16103
8.06102 0.1672 1.46104 9.46103 2.06103
7 12 11 3
3.16104 1.16104 1.76104 1.56103
5.86103 0.0029 2.86103 8.06103 6.06102
3.26104 1.26104 2.26104 1.36102
5.96103 0.0002 5.66103 9.56103 4.3610
4.36104 3.76103 1.06104 4.76102
1.26104 ,0.0001 9.76102 1.86103 1.96102
8 25
1.66104 5.86103 NS 1.76104 4.26103
1.76104 6.16103 NS 1.96104 5.36103
5.26103 1.66103 0.0647 2.26104 6.56103
22 11 33
1.66104 3.46103 NS 1.76104 8.06103 1.66104 1.96104
1.76104 4.46103 NS 2.26104 9.56103 1.46104 2.46104
5.46103 1.16103 ,0.0001 4.36104 1.26104 1.86104 2.76104
P-values derived from analysis of variance (ANOVA); NS5Not statistically significant; CFU5colony forming unit; SE5standard error; Dependent variables5log-transformed values
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Table 3 Correlation matrix analysis based on the logtransformed values for culturable bacteria, gram-negative bacteria (GNB), and fungi (CFU/m3)
Bacteria GNB Fungi
Bacteria
GNB
Fungi
1 0.84 (P,0.0001) 0.51 (P50.0022)
1 0.54 (P50.0014)
1
CFU5colony forming unit.
qualitative variables except for ‘‘weather on day of sampling’’ were significant at P,0.25. Notably however, only ‘‘type of waste-handling activity’’ was significantly associated with all three types of airborne microorganisms (P#0.0001). Among these activities, sorting was associated with markedly higher levels of exposure to bacteria, GNB, and fungi than collection, transfer, or transport. Although transport (i.e., levels inside the cab of the vehicle) was associated with the lowest levels of airborne microorganisms, these levels remained above 100 CFU/m3. Correlation matrix analysis revealed that airborne levels of bacteria, GNB, and fungi were significantly correlated with one another (Table 3). All significant (P,0.25) occupational and environmental variables identified in the univariate analysis were entered into a multiple regression analysis. As
Airborne bacteria and fungi in waste-handling
shown in Table 4, ‘‘type of waste-handling activity’’ was the only factor that appeared to significantly affect airborne levels of bacteria and GNB, accounting for 38% (P50.0029) and 50% (P50.0002) of the observed variation, respectively. In terms of fungi, ‘‘type of waste-handling activity’’ explained most of the observed variation in airborne fungi (P,0.0001, R250.78), whereas ‘‘waste collection on day prior to sampling’’ had a small effect on airborne fungi (adjusted R250.2)(Table 5).
Discussion Several studies have indicated that refuse collectors are at an increased risk of respiratory and influenzalike symptoms,2,9,10 due to high exposure to bioaerosols and organic dusts, including microorganisms and their toxins. These studies have reinforced the hypothesis that exposure to airborne microorganisms and their toxic products causes a multitude of health problems among workers at waste sorting and recycling plants. Our results confirm the high levels of airborne bacteria and fungi present during waste handling, independently of other occupational and environmental conditions. The mean levels observed in this study (bacteria: 1.66104 CFU/m3; fungi: 1.86104 CFU/m3) were higher than those previously
Table 4 Multiple regression models to predict the log-transformed values of bacteria and gram-negative bacteria (GNB) levels during household-waste collection Bacteria, CFU/m3 Independent variable
Coefficient
Type of waste-handling activity Sorting Collection Transfer Transport (inside vehicle) Constant Model p Adjusted R2
Reference 21.54 21.18 23.10 10.24 0.0029 0.38
GNB, CFU/m3
Standard Error
P
Coefficient
0.53 0.54 0.78 0.42
0.007 0.038 ,0.0001 ,0.0001
Reference 21.99 21.71 25.58 10.29 0.0002 0.50
Standard Error
P
0.73 0.76 1.06 0.58
0.011 0.032 ,0.0001 ,0.0001
Table 5 Multiple regression model to predict the level of fungi during household-waste collection Fungi, CFU/m3 Independent Variable Coefficient Type of waste-handling activity Sorting Collection Transfer Transport (inside vehicle)
Reference 22.54 20.26 23.65
Collection on day prior to sampling On Off Constant Model P Adjusted R2
Reference 1.42 9.14 , 0.0001 0.78
Standard Error
P-value
0.60 0.68 0.60
0.015 , 0.001 0.707
0.54 0.31
0.015 , 0.001
Dependent variables (fungi level)5log-transformed value. CFU5colony forming unit.
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measured for workers sorting household garbage11 and are consistent with those cited in studies reviewed by Kuijer and Frings-Dresen.12 Although the airborne microorganism levels reported here should not be directly interpreted as inhalation exposure because they were obtained from area samplers operating for only a short period, these results are useful to compare airborne microorganism levels generated under various waste collection circumstances with the existing recommended levels. In this study, the mean level of airborne bacteria exceeded the occupational exposure limit (OEL) of 104 CFU/m3 proposed by Malmros et al.11 Additionally, the mean levels of airborne GNB (1.86104 CFU/m3) and fungi (1.86 104 CFU/m3) were similar to or nearing the respective OELs recommended by Go´rny and Dutkiewicz (26104 CFU/m3 for GNB and 56104 CFU/m3 for fungi).13 Similar exposures to culturable bacteria and fungi have been reported for European waste handlers, who showed adverse health effects such as nausea, diarrhea, upper respiratory tract irritation, and allergies. Lavoie et al.14 reported the highest personal exposures to bacteria observed for urban compostable waste collectors, a median of 5.06104 CFU/m3, in North America. Fungal counts collected were highest among a group of rural compostable waste collectors, with median of 16105 CFU/m3, measured biweekly.14 To minimize bioaerosol exposure, it is crucial to characterize the occupational and environmental determinants affecting the level of microorganisms generated during waste handling. However, it is difficult to generalize which factors influence the exposure of waste handlers to hazardous agents, including microorganisms, because characteristics of waste collection or waste-management systems (the type of waste handled, the type of vehicle, the frequency of waste handling, the shift worked, service time, the size of the area serviced, the type of employment, etc.) vary greatly among regions and countries. In addition, constantly shifting weather conditions (e.g., temperature and humidity) are also likely to influence exposure to hazardous agents such as bioaerosols during waste collection. To probe this complexity, we selected various occupational and environmental factors that may influence levels of airborne microorganisms generated during waste-handling work (Table 1). Of these, only the type of waste-handling activity was significantly associated with airborne levels of bacteria, GNB, and fungi in two consecutive statistical analyses. Sorting waste was associated with significantly higher levels of bacteria (3.16104 CFU/m3), GNB (3.26 104 CFU/m3), and fungi (4.36104 CFU/m3) compared with the other types of waste-handling activities (Table 2). This is likely due to both the type of waste received in the sorting workplace and
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the working conditions. Material processing plants receive both source-separated and non-separated household wastes. Handling recyclable materials, for example, may pose a health risk in that small amounts of contaminated water, food, or milk left in containers could provide a growth medium for microbes during waste transportation or storage. Manual sorting of unseparated domestic waste may be associated with exposure to large quantities of airborne microorganisms. Furthermore, lack of exposure-control measures and other unique work characteristics related to waste sorting may exacerbate the level of bioaerosols generated during sorting.13 In 2008, 65.6% of all waste handlers in Korea (n5105,858) were employed in small workplaces of less than 50 employees.15 In general, these small facilities may not have the means or capacity to invest in engineering controls and administrative measures to control exposure to hazardous agents such as bioaerosols. Workers sorting source-separated waste materials (plastics, ferric, and non-ferric metals) may be exposed to airborne biological agents, especially fungi and GNB.16 In a plant sorting source-separated household waste, the predominant airborne microorganisms were fungi, with counts greater than 12 000 CFU/m3, which is similar to the results of this study. At such plants bioaerosol exposure levels are generally low, but during some activities (e.g., manual sorting and work near balers) exposure may occasionally reach harmful levels.17 Concentrations of airborne bacteria measured at the sorting operations of municipal solid waste recycling and composting plants in Canada were.105 CFU/ m3,18 higher than those found in our study. In contrast to sorting work, collection and transfer activity occurs outdoors under distinct conditions. We examined two specific outdoor activities: the collection of waste at several fixed points and the transfer of waste from smaller collection vehicles to larger transport equipment. We observed no significant difference in airborne microorganisms between these two activities (Table 2). Therefore, in future studies, workers who collect and transport household waste in the open air should be classified into the same exposure group. However, despite these results and those of previous studies showing high exposure risks and associated respiratory disease risk among waste handlers, it is difficult to propose effective control measures for these individuals due to the nature of the job, which involves the constant handling of waste, and physical labor, over a concentrated period of time. Strenuous activity in particular, may make it difficult for workers to tolerate the use of respirators. In addition, we found that the air inside vehicle cabs was contaminated with microorganisms, with
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mean levels of 1.56103 CFU/m3 for bacteria, 1.36102 CFU/m3 for GNB, and 4.76102 for fungi. This is likely due to both the infiltration of contaminated air through open doors and windows and to the fact that drivers occasionally leave the cab of the vehicle to assist loaders, and then return bearing organic dusts on their clothes and hands. Therefore, personnel riding in the vehicle cab may be exposed to contaminated microorganisms within the vehicle. Thus, the exposure risk for drivers may be high, with higher short-term exposure during loading as well as sustained, low-level exposure while driving. To reduce airborne microorganism levels inside the vehicle, cabs should receive a steady supply of fresh air and vehicle interiors should be cleaned as frequently as possible. In addition to the type of waste-handling activity, we examined a number of other environmental and occupational factors that are thought to affect exposure to bioaerosols. As detailed in Poulsen et al.,2 the type of waste-management company, organization of work, type of equipment, the district, type of waste, frequency of collection, and seasonal variations are important determinants of exposure. Heldal et al. (2003) reported that for household-waste collectors, the degree of bioaerosol exposure depends likely on the type of container, the truck, and the manner in which the work is carried out.4 Breum et al. (1996) found that the level of bioaerosol exposure during household-waste collection was correlated with several variables: the type of waste, the household collection unit, type of collection vehicle, and the waste collector’s job description.5 In our univariate analysis, most of these occupational factors were found to be significant at a level of P,0.25 (Table 2). However, all factors except for ‘‘type of waste-handling work’’ were removed in the final multivariate regression analysis (Table 4 and Table 5). To our knowledge, this study is the first to dissect the job title of ‘‘waste collector’’ into several specific waste-handling activities. This approach has allowed us to detect stronger significant relationships between airborne microorganisms and these activities than with other occupational variables. A major limitation of this study was the small sample size (n533), which may not be representative of household-waste handling activities as a whole (sorting57, collection512, transfer511, transport53), given the various types of collection, containers, vehicles, and other factors. This study also provides results for airborne microorganism levels over a specific period of time during which waste-handling activities were performed. Further studies using samples from additional locations and sampling intervals are needed to identify other occupational and environmental factors influencing airborne microorganism levels. We also did not
Airborne bacteria and fungi in waste-handling
examine associations between microorganism exposure and additional occupational technical factors such as the design of the collection vehicle or equipment or the level of manual handling or automation. Nevertheless, our results are useful not only for characterizing the level of airborne bacteria, GNB, and fungi encountered during waste handling but also for identifying factors that may significantly influence airborne concentrations of these agents and the recommendation of mitigation measures. Our results support the enforcement of legally mandated occupational health measures including medical surveillance to prevent potentially adverse health effects in waste handlers. Waste collection is recognized as one of the most hazardous and poorly paying jobs in Korea. In 2008, waste collectors were reported to work a mean 41 hours per week, with a range from 33–66 hours.15 Thus, one way to limit exposure and mitigate risk among these workers may be to enforce a shorter work week. Finally, this sector may benefit from increased surveillance by government regulatory agencies, which currently do not pay any special attention to the fact that waste collectors are exposed to high levels of hazardous agents including microorganisms. Because waste collection workers belong to the service industry, the exact number of individuals working in this sector is unclear, and occupational illnesses are not officially reported. In conclusion, given that waste-handling activities were found to be significantly associated with high levels of bacteria, GNB, and fungi, various engineering, administrative, and regulatory measures should be considered to reduce exposure to airborne microorganisms during household-waste collection. Authorities responsible for the inspection of the work environment should engage with private and governmental waste-management companies to ensure the provision of necessary measures, such as automated waste collection, clean rest areas, personal protective equipment (gloves and respirators), meticulous personal hygiene, and medical surveillance for illnesses brought on by airborne microorganisms.
References 1 An H, Englehardt J, Fleming L, Bean J. Occupational health and safety amongst municipal solid waste workers in Florida. Waste Manag Res. 1999;17(5):369–77. 2 Poulsen OM, Breum NO, Ebbehoj N, Hansen AM, Ivens UI, Van LD, et al. Collection of domestic waste. Review of occupational health problems and their possible causes. Sci Total Environ. 1995;170(1–2):1–19. 3 Ivens UI, Breum NO, Ebbehoj N, Nielsen BH, Poulsen OM, Wurtz H. Exposure-response relationship between gastrointestinal problems among waste collectors and bioaerosol exposure. Scand J Work Environ Health. 1999;25(3):238–45. 4 Heldal KK, Halstensen AS, Thorn J, Djupesland P, Wouters I, Eduard W, Halstensen TS. Upper airway inflammation in waste handlers exposed to bioaerosols. Occup Environ Med. 2003;60(6):444–50.
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13 Gorny RL, Dutkiewicz J. Bacterial and fungal aerosols in indoor environment in central and eastern European countries. Ann Agric Environ Med. 2002;9(1):17–23. 14 Lavoie J, Dunkerley CJ, Kosatsky T, Dufresne A. Exposure to aerosolized bacteria and fungi among collectors of commercial, mixed residential, recyclable and compostable waste. Sci Total Environ. 2006;370:23–8. 15 Korea Occupational Safety Health Agency (KOSHA). Study on the validity of installation of washing facilities in the workplace (focus on sanitation work). Research No. 2010-84915. South-Korea, KOSHA, 2010(in Korean). 16 Solans X, Alonso RM, Constans A, Mansilla A. Occupational exposure to airborne fungi and bacteria in a household recycled container sorting plant. Rev Iberoam Micol. 2007;24(2):131– 5. 17 Poulsen OM, Breum NO, Ebbehøj N, Hansen AM, Ivens UI, Lelieveld DV, et al. Sorting and recycling of domestic waste. Review of occupational health problems and their possible causes. Sci Total Environ. 1995;168(1):33–56. 18 Marchand G, Lavoie J, Lazure L. Evaluation of bioaerosols in a municipal solid waste recycling and composting plant. J Air Waste Manag Assoc. 1995;45:778–81.
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Department of Environmental Health, Korea National Open University, Korea, 2Wonjin Institute for Occupational and Environmental Health, Korea, 3Dept. of Environmental Health, Graduate School of Public Health, Seoul National University, Korea, 4Occupational Lung Diseases Institute, Korea
Background: Municipal workers handling household waste are potentially exposed to a variety of toxic and pathogenic substances, in particular airborne bacteria, gram-negative bacteria (GNB), and fungi. However, relatively little is known about the conditions under which exposure is facilitated. Methods: This study assessed levels of airborne bacteria, GNB, and fungi, and examined these in relation to the type of waste-handling activity (collection, transfer, transport, and sorting at the waste preprocessing plant), as well as a variety of other environmental and occupational factors. Airborne microorganisms were sampled using an Andersen single-stage sampler equipped with agar plates containing the appropriate nutritional medium and then cultured to determine airborne levels. Samples were taken during collection, transfer, transport, and sorting of household waste. Multiple regression analysis was used to identify environmental and occupational factors that significantly affect airborne microorganism levels during waste-handling activities. Results: The ‘‘type of waste-handling activity’’ was the only factor that significantly affected airborne levels of bacteria and GNB, accounting for 38% (P50.029) and 50% (P50.0002) of the variation observed in bacteria and GNB levels, respectively. In terms of fungi, the type of waste-handling activity (R250.76) and whether collection had also occurred on the day prior to sampling (P,0.0001, R250.78) explained most of the observed variation. Given that the type of waste-handling activity was significantly correlated with levels of bacteria, GNB, and fungi, we suggest that various engineering, administrative, and regulatory measures should be considered to reduce the occupational exposure to airborne microorganisms in the wastehandling industry. Keywords: Household waste, Microorganism, Bioaerosol
Introduction Household waste refers to mixed waste streams derived from domestic activity that typically require any form of pre-processing or sorting before they can be properly disposed. For example, biodegradable food and kitchen wastes are generally separated from total household waste, as are recyclable materials such as metal, wood, paper, glass, aluminum cans, and plastic. Although some wastes may be sorted at the source (e.g. home or office), most wastehandling activities are carried out by municipal workers. Although they may wear protective equipments, these workers are in some degree of contact with household waste from the time of collection through to final disposal in a landfill or incinerator. This is a concern because when biodegradable waste Correspondence to: Donguk Park, Department of Environmental Health, Korea National Open University, 169 Dongsung-dong, Jongroku, Seoul, Korea. Email: [email protected]
ß W. S. Maney & Son Ltd 2013 DOI 10.1179/2049396713Y.0000000036
is handled, organic particles (including microorganisms) can be aerosolized, and waste handlers may consequently be exposed to multiple pathogenic agents, including bacteria, endotoxins, mold spores, glucans, volatile organic compounds, and even infectious materials.1 Such exposure may underlie reports of respiratory complaints, gastrointestinal problems, eye and skin irritation, and symptoms of toxic organic dust syndrome among workers collecting the organic fraction of household waste.2,3 Waste collectors around the world are at risk for workrelated disorders and injuries. There is increasing evidence that the incidence of work-related pulmonary illness is high among waste collectors.1,2,4 Despite these reports, relatively little is known regarding the environmental and occupational factors that contribute to exposure to aerosolized microorganisms during waste handling. Specific wastehandling activities, such as collection, sorting, and
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disposal, may differentially affect levels of microorganisms and their toxins in organic dusts. Additionally, other environmental and occupational factors in waste handling may be associated with the generation of potentially harmful bioaerosols. To date, numerous factors have been reported to influence working conditions and hence the level of potential exposure among waste collectors. Such factors include the type of company (private or governmental), organization of work, type of equipment, type of district, type of waste, frequency of collection, and seasonal variation.2,4,5 To our knowledge, no study has previously examined how the type of waste-handling activity affects airborne levels of microorganism. Accordingly, we identified the factors responsible for worker exposure to airborne bacteria and fungi in typical exposure scenarios and examined levels of exposure with respect to several environmental and occupational characteristics.
Methods Brief description of household waste handling activities in Korea Throughout the entire process of waste collection and disposal, waste handlers may participate in a variety of activities that may differentially influence exposure to hazardous agents. Accordingly, we defined four activity groups based on the routing of wastes, different types of wastes, working conditions, and common practices, in such a way that potential differences in bioaerosol exposure within the same activity group were minimized, and contrast among groups was maximized. Waste handling involves a number of different waste streams, including source-separated biodegradable waste (i.e., food waste from homes, and restaurants), source-separated non-biodegradable waste (recyclable and reusable materials), and non-separated wastes. Waste handling also involves a number of process steps. First, all wastes are collected from fixed sites and loaded into small vehicles or motorcycles equipped with small containers. Second, the waste from several districts is transferred from smaller collection vehicles to larger transport equipment. The transferring and agitation of waste may expose waste collectors riding at the back end of the truck to bioaerosols. Larger transport trucks make frequent stops to pick up municipal waste. Thus, waste collectors usually stand outside and at the rear end of the truck to facilitate getting on and off the truck during these frequent stops. Third, the waste is transported, usually over long distances, to a material processing plant. During this time, personnel riding in the vehicle cab may be exposed to bioaerosols from contaminated hands or clothing. Finally, having reached the material processing plant, waste is sorted to remove valuable recyclables or reusable materials.
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Biodegradable or food waste is sent for further processing into organic fertilizer or animal food, whereas non-separated waste (e.g., leaves, vegetables, dead animals, feces, and other non-usable wastes) is transported directly to a landfill or incinerator. This study focused on the generation of airborne microorganisms during waste collection, transfer, transport, and sorting at the material processing plant; potential exposure at disposal sites (incinerator or landfill) was excluded.
Sampling of airborne microorganisms Levels of airborne bacteria, gram-negative bacteria (GNB), and fungi were analyzed according to wastehandling activity (collection, transfer, transport, and sorting). Air samples were collected using an Andersen one-stage cascade sampler either fixed in place or moved around between the heights of 1.2 and 1.5 m to simulate the inhalation and exposure of waste handlers. Air was drawn through the sampler at a flow rate of 28.3 l/minute for less than 5 minutes; a short sampling period was selected to avoid overloading the plates such that distinct colonies could not be enumerated. The time-weighted average (TWA) was calculated over the 5-minute sampling interval during each waste-handling activity. Airborne microorganisms were sampled using a 20 ml nutrient plate (tryptic soy agar for bacteria, MacConkey agar for GNB, and sabouraud dextrose agar with chloramphenicol for fungi) coupled inside the stage sampler. When changing the collection plates, the stage hole was sterilized with a 70% ethanol solution to prevent cross-contamination. An IAQ-Calc Indoor Air Quality Meter (Model 8762; TSI, Inc., Shoreview, Minnesota, USA) was used to simultaneously monitor air temperature and humidity during each sampling interval. Data were logged every 30 seconds, and a TWA was used in the data analysis. Bioaerosol and air quality data were collected during the day from 06:00 to 18:00 and at night from 18:00 to 06:00. After sample collection, the agar plates were transported to the laboratory and incubated at 37¡1uC for 2 days for bacteria and GNB or at 25¡1uC for 4 days for fungi.6 Specific statistical corrections were made using correction factors obtained for each growing medium from the Conversion Tables provided with the Anderson one-stage sampler operating manual.7 The microbial counts were expressed in terms of colony forming units (CFU) per unit volume of air (m3). Total culturable bacterial and fungal counts were compared to ambient environmental (background) levels to determine the exposure to microorganisms generated during household waste handling. Our microbial sampling strategy was designed to best represent the
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level of microorganisms generated during typical household waste handling.
Data analysis Descriptive statistics, correlation analysis, t-tests, and univariate and multiple regression analyses were conducted using Stata Version 11.0 (Stata Corp. LP, College Station, Texas, USA). Initially, the distributions of bacteria, GNB, and fungi were skewed; to improve our statistical models, all microorganism data were log-transformed.
Airborne bacteria and fungi in waste-handling
In addition to the microorganism data (dependent variable), we reviewed the literature to identify a number of environmental and occupational factors (independent variables) that are likely to influence airborne levels of bacteria, GNB, and fungi during waste handling (Table 1). We also included variables related to the four specific waste-handling works or activities (collection, transfer, transport, and sorting) that were intended to isolate and maximize differences in exposure conditions. Simple linear regression was performed to examine their relationship with the
Table 1 Description of occupational and environmental variables related to waste collection Independent variable
Number of samples
Description (number of samples)
City Seoul Local
11 22
One district in Seoul Three cities within Gyeonggi Province: Guri (n53); Uijeongbu (n53); Pyungtaek (n516)
Weather on day prior to sampling Sunny Other
10 23
Sunny Rainy (n511); cloudy (n53); humid (n59)
Weather during sample collection Sunny Cloudy
30 3
Sunny Overcast and humid
Season Summer Fall
27 6
Samples collected during August (n527) Samples collected during September (n53) and October (n53)
Collection day Week day
22
Weekend
11
Samples collected on Monday (n59), Tuesday (n53), and Wednesday (n510) Samples collected on Sunday
Waste collection on day prior to sampling Yes
11
No
22
Type of company Government Private Type of waste Street
5 28 5
Household Food garbage Reusable
9 11 8
Type of wastehandling activity Sorting Collection Transfer
7 12 11
Transport Waste-handling location Indoor Outdoor Collection time Day Night Total
If waste was not collected on the day before sampling, waste accumulation was likely to have occurred.
Local government tends to contract out waste collection work. Workers employed at private company may have much waste Waste collected from either stationary containers or various types of waste discarded on the street Non-separated waste from households or restaurants Separated food waste from household or restaurants Reusable wastes (separated), such as paper, wood, metal, glass, etc.
3
To select reusable waste from non-separated waste To collect waste at fixed sites and load into vehicle To transfer from smaller collection vehicles to larger transport equipment Inside vehicle
8 25
Sorting work occurred indoors Collection and transport activities occurred outdoors
22 11 33
Waste collected between 06:00 and 18:00 Waste collected between 18:00 and 06:00
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observed quantitative variables (air temperature, humidity, and airborne microorganism levels). Analysis of variance (ANOVA) was used to compare mean microorganism levels among categories of qualitative variables. Only variables with P-values ,0.25 were introduced to our multiple regression analysis.8 Finally, stepwise analysis was used to identify factors that significantly affected airborne levels of bacteria, GNB, and fungi. Categories serving as a reference group for comparing with other groups were given a value of zero.
microorganism levels were regressed against quantitative environmental factors such as air temperature and humidity and compared among qualitative environmental and occupational categories (Table 2). Simple linear regression showed that air humidity accounted for 12.3% of the variation observed in airborne fungi generated during waste handling (P50.0258), while airborne bacteria and GNB levels were not associated with changes in temperature at P,0.05(results are not shown). Occupational and environmental factors affecting airborne bacteria included ‘‘season’’ (P50.157), ‘‘type of waste’’ (P50.0517), and ‘‘type of waste-handling activity’’ (P50.0029). In addition to these factors, ‘‘type of waste collection company’’ (P50.1805) was also significantly associated with airborne GNB levels at P,0.25. Regarding fungi, all
Results The mean levels of airborne microorganisms were 1.66104 CFU/m3 for bacteria, 1.46104 CFU/m3 for GNB, and 1.86104 CFU/m3 for fungi. Airborne Table 2 Levels of airborne environmental variables
bacteria,
gram-negative
bacteria
Bacteria, CFU/m3 Independent variable City Seoul Local cities Weather on day prior to sampling Sunny Other Weather on day of sampling Sunny Other Season Summer Fall Collection day Week day Weekend Waste collection on day prior to sampling On Off Type of organization Government Private Type of waste handled Street Household Food garbage Reusable Type of wastehandling work Sorting Collection Transfer Transport (inside car) Location where waste is handled Indoor Outdoor Waste collection time Day (06:00218:00) Night (18:00206:00) Total
No. of sample
Mean
SE
(GNB),
and
fungi
according
GNB, CFU/m3
P-value
Mean
SE
to
occupational
and
Fungi, CFU/m3 P-value
Mean
SE
P-value
11 22
1.76104 8.06103 NS 1.66104 3.46103
2.26104 9.56103 NS 1.76104 4.46103
4.36104 1.26104 ,0.0001 5.46103 1.16103
10 23
2.26104 6.26103 NS 1.46104 4.16103
2.36104 6.76103 NS 1.66104 5.46103
7.36103 1.96103 0.1396 2.36104 7.16103
30 3
1.76104 3.76103 NS 1.56104 5.66103
2.06104 4.66103 NS 7.76103 6.06103
1.96104 5.66103 NS 6.26103 1.76103
27 6
1.86104 4.06103 0.1570 8.26103 4.06103
2.26104 4.96103 0.0252 4.26103 3.26103
2.16104 6.16103 0.1464 3.36103 1.56103
22 11
1.66104 3.46103 NS 1.76104 8.06103
1.76104 4.46103 NS 2.26104 9.56103
5.46103 1.16103 ,0.0001 4.36104 1.26104
11 22
2.06104 5.66103 NS 1.46104 4.26103
2.16104 6.46103 NS 1.76104 5.46103
6.76103 1.86103 0.0697 2.46104 7.46103
5 28
8.86103 4.26103 NS 1.86104 3.96103
5.46103 3.76103 0.1805 2.16104 4.86103
2.36103 8.06102 0.0519 2.16104 5.96103
5 9 11 8
8.86103 2.36104 6.86103 2.76104
4.26103 0.0517 9.46103 2.06103 6.46103
5.46103 3.06104 8.66103 2.86104
3.76103 0.0594 1.16104 5.36103 6.66103
2.36103 3.26104 2.06104 9.16103
8.06102 0.1672 1.46104 9.46103 2.06103
7 12 11 3
3.16104 1.16104 1.76104 1.56103
5.86103 0.0029 2.86103 8.06103 6.06102
3.26104 1.26104 2.26104 1.36102
5.96103 0.0002 5.66103 9.56103 4.3610
4.36104 3.76103 1.06104 4.76102
1.26104 ,0.0001 9.76102 1.86103 1.96102
8 25
1.66104 5.86103 NS 1.76104 4.26103
1.76104 6.16103 NS 1.96104 5.36103
5.26103 1.66103 0.0647 2.26104 6.56103
22 11 33
1.66104 3.46103 NS 1.76104 8.06103 1.66104 1.96104
1.76104 4.46103 NS 2.26104 9.56103 1.46104 2.46104
5.46103 1.16103 ,0.0001 4.36104 1.26104 1.86104 2.76104
P-values derived from analysis of variance (ANOVA); NS5Not statistically significant; CFU5colony forming unit; SE5standard error; Dependent variables5log-transformed values
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Table 3 Correlation matrix analysis based on the logtransformed values for culturable bacteria, gram-negative bacteria (GNB), and fungi (CFU/m3)
Bacteria GNB Fungi
Bacteria
GNB
Fungi
1 0.84 (P,0.0001) 0.51 (P50.0022)
1 0.54 (P50.0014)
1
CFU5colony forming unit.
qualitative variables except for ‘‘weather on day of sampling’’ were significant at P,0.25. Notably however, only ‘‘type of waste-handling activity’’ was significantly associated with all three types of airborne microorganisms (P#0.0001). Among these activities, sorting was associated with markedly higher levels of exposure to bacteria, GNB, and fungi than collection, transfer, or transport. Although transport (i.e., levels inside the cab of the vehicle) was associated with the lowest levels of airborne microorganisms, these levels remained above 100 CFU/m3. Correlation matrix analysis revealed that airborne levels of bacteria, GNB, and fungi were significantly correlated with one another (Table 3). All significant (P,0.25) occupational and environmental variables identified in the univariate analysis were entered into a multiple regression analysis. As
Airborne bacteria and fungi in waste-handling
shown in Table 4, ‘‘type of waste-handling activity’’ was the only factor that appeared to significantly affect airborne levels of bacteria and GNB, accounting for 38% (P50.0029) and 50% (P50.0002) of the observed variation, respectively. In terms of fungi, ‘‘type of waste-handling activity’’ explained most of the observed variation in airborne fungi (P,0.0001, R250.78), whereas ‘‘waste collection on day prior to sampling’’ had a small effect on airborne fungi (adjusted R250.2)(Table 5).
Discussion Several studies have indicated that refuse collectors are at an increased risk of respiratory and influenzalike symptoms,2,9,10 due to high exposure to bioaerosols and organic dusts, including microorganisms and their toxins. These studies have reinforced the hypothesis that exposure to airborne microorganisms and their toxic products causes a multitude of health problems among workers at waste sorting and recycling plants. Our results confirm the high levels of airborne bacteria and fungi present during waste handling, independently of other occupational and environmental conditions. The mean levels observed in this study (bacteria: 1.66104 CFU/m3; fungi: 1.86104 CFU/m3) were higher than those previously
Table 4 Multiple regression models to predict the log-transformed values of bacteria and gram-negative bacteria (GNB) levels during household-waste collection Bacteria, CFU/m3 Independent variable
Coefficient
Type of waste-handling activity Sorting Collection Transfer Transport (inside vehicle) Constant Model p Adjusted R2
Reference 21.54 21.18 23.10 10.24 0.0029 0.38
GNB, CFU/m3
Standard Error
P
Coefficient
0.53 0.54 0.78 0.42
0.007 0.038 ,0.0001 ,0.0001
Reference 21.99 21.71 25.58 10.29 0.0002 0.50
Standard Error
P
0.73 0.76 1.06 0.58
0.011 0.032 ,0.0001 ,0.0001
Table 5 Multiple regression model to predict the level of fungi during household-waste collection Fungi, CFU/m3 Independent Variable Coefficient Type of waste-handling activity Sorting Collection Transfer Transport (inside vehicle)
Reference 22.54 20.26 23.65
Collection on day prior to sampling On Off Constant Model P Adjusted R2
Reference 1.42 9.14 , 0.0001 0.78
Standard Error
P-value
0.60 0.68 0.60
0.015 , 0.001 0.707
0.54 0.31
0.015 , 0.001
Dependent variables (fungi level)5log-transformed value. CFU5colony forming unit.
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measured for workers sorting household garbage11 and are consistent with those cited in studies reviewed by Kuijer and Frings-Dresen.12 Although the airborne microorganism levels reported here should not be directly interpreted as inhalation exposure because they were obtained from area samplers operating for only a short period, these results are useful to compare airborne microorganism levels generated under various waste collection circumstances with the existing recommended levels. In this study, the mean level of airborne bacteria exceeded the occupational exposure limit (OEL) of 104 CFU/m3 proposed by Malmros et al.11 Additionally, the mean levels of airborne GNB (1.86104 CFU/m3) and fungi (1.86 104 CFU/m3) were similar to or nearing the respective OELs recommended by Go´rny and Dutkiewicz (26104 CFU/m3 for GNB and 56104 CFU/m3 for fungi).13 Similar exposures to culturable bacteria and fungi have been reported for European waste handlers, who showed adverse health effects such as nausea, diarrhea, upper respiratory tract irritation, and allergies. Lavoie et al.14 reported the highest personal exposures to bacteria observed for urban compostable waste collectors, a median of 5.06104 CFU/m3, in North America. Fungal counts collected were highest among a group of rural compostable waste collectors, with median of 16105 CFU/m3, measured biweekly.14 To minimize bioaerosol exposure, it is crucial to characterize the occupational and environmental determinants affecting the level of microorganisms generated during waste handling. However, it is difficult to generalize which factors influence the exposure of waste handlers to hazardous agents, including microorganisms, because characteristics of waste collection or waste-management systems (the type of waste handled, the type of vehicle, the frequency of waste handling, the shift worked, service time, the size of the area serviced, the type of employment, etc.) vary greatly among regions and countries. In addition, constantly shifting weather conditions (e.g., temperature and humidity) are also likely to influence exposure to hazardous agents such as bioaerosols during waste collection. To probe this complexity, we selected various occupational and environmental factors that may influence levels of airborne microorganisms generated during waste-handling work (Table 1). Of these, only the type of waste-handling activity was significantly associated with airborne levels of bacteria, GNB, and fungi in two consecutive statistical analyses. Sorting waste was associated with significantly higher levels of bacteria (3.16104 CFU/m3), GNB (3.26 104 CFU/m3), and fungi (4.36104 CFU/m3) compared with the other types of waste-handling activities (Table 2). This is likely due to both the type of waste received in the sorting workplace and
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the working conditions. Material processing plants receive both source-separated and non-separated household wastes. Handling recyclable materials, for example, may pose a health risk in that small amounts of contaminated water, food, or milk left in containers could provide a growth medium for microbes during waste transportation or storage. Manual sorting of unseparated domestic waste may be associated with exposure to large quantities of airborne microorganisms. Furthermore, lack of exposure-control measures and other unique work characteristics related to waste sorting may exacerbate the level of bioaerosols generated during sorting.13 In 2008, 65.6% of all waste handlers in Korea (n5105,858) were employed in small workplaces of less than 50 employees.15 In general, these small facilities may not have the means or capacity to invest in engineering controls and administrative measures to control exposure to hazardous agents such as bioaerosols. Workers sorting source-separated waste materials (plastics, ferric, and non-ferric metals) may be exposed to airborne biological agents, especially fungi and GNB.16 In a plant sorting source-separated household waste, the predominant airborne microorganisms were fungi, with counts greater than 12 000 CFU/m3, which is similar to the results of this study. At such plants bioaerosol exposure levels are generally low, but during some activities (e.g., manual sorting and work near balers) exposure may occasionally reach harmful levels.17 Concentrations of airborne bacteria measured at the sorting operations of municipal solid waste recycling and composting plants in Canada were.105 CFU/ m3,18 higher than those found in our study. In contrast to sorting work, collection and transfer activity occurs outdoors under distinct conditions. We examined two specific outdoor activities: the collection of waste at several fixed points and the transfer of waste from smaller collection vehicles to larger transport equipment. We observed no significant difference in airborne microorganisms between these two activities (Table 2). Therefore, in future studies, workers who collect and transport household waste in the open air should be classified into the same exposure group. However, despite these results and those of previous studies showing high exposure risks and associated respiratory disease risk among waste handlers, it is difficult to propose effective control measures for these individuals due to the nature of the job, which involves the constant handling of waste, and physical labor, over a concentrated period of time. Strenuous activity in particular, may make it difficult for workers to tolerate the use of respirators. In addition, we found that the air inside vehicle cabs was contaminated with microorganisms, with
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mean levels of 1.56103 CFU/m3 for bacteria, 1.36102 CFU/m3 for GNB, and 4.76102 for fungi. This is likely due to both the infiltration of contaminated air through open doors and windows and to the fact that drivers occasionally leave the cab of the vehicle to assist loaders, and then return bearing organic dusts on their clothes and hands. Therefore, personnel riding in the vehicle cab may be exposed to contaminated microorganisms within the vehicle. Thus, the exposure risk for drivers may be high, with higher short-term exposure during loading as well as sustained, low-level exposure while driving. To reduce airborne microorganism levels inside the vehicle, cabs should receive a steady supply of fresh air and vehicle interiors should be cleaned as frequently as possible. In addition to the type of waste-handling activity, we examined a number of other environmental and occupational factors that are thought to affect exposure to bioaerosols. As detailed in Poulsen et al.,2 the type of waste-management company, organization of work, type of equipment, the district, type of waste, frequency of collection, and seasonal variations are important determinants of exposure. Heldal et al. (2003) reported that for household-waste collectors, the degree of bioaerosol exposure depends likely on the type of container, the truck, and the manner in which the work is carried out.4 Breum et al. (1996) found that the level of bioaerosol exposure during household-waste collection was correlated with several variables: the type of waste, the household collection unit, type of collection vehicle, and the waste collector’s job description.5 In our univariate analysis, most of these occupational factors were found to be significant at a level of P,0.25 (Table 2). However, all factors except for ‘‘type of waste-handling work’’ were removed in the final multivariate regression analysis (Table 4 and Table 5). To our knowledge, this study is the first to dissect the job title of ‘‘waste collector’’ into several specific waste-handling activities. This approach has allowed us to detect stronger significant relationships between airborne microorganisms and these activities than with other occupational variables. A major limitation of this study was the small sample size (n533), which may not be representative of household-waste handling activities as a whole (sorting57, collection512, transfer511, transport53), given the various types of collection, containers, vehicles, and other factors. This study also provides results for airborne microorganism levels over a specific period of time during which waste-handling activities were performed. Further studies using samples from additional locations and sampling intervals are needed to identify other occupational and environmental factors influencing airborne microorganism levels. We also did not
Airborne bacteria and fungi in waste-handling
examine associations between microorganism exposure and additional occupational technical factors such as the design of the collection vehicle or equipment or the level of manual handling or automation. Nevertheless, our results are useful not only for characterizing the level of airborne bacteria, GNB, and fungi encountered during waste handling but also for identifying factors that may significantly influence airborne concentrations of these agents and the recommendation of mitigation measures. Our results support the enforcement of legally mandated occupational health measures including medical surveillance to prevent potentially adverse health effects in waste handlers. Waste collection is recognized as one of the most hazardous and poorly paying jobs in Korea. In 2008, waste collectors were reported to work a mean 41 hours per week, with a range from 33–66 hours.15 Thus, one way to limit exposure and mitigate risk among these workers may be to enforce a shorter work week. Finally, this sector may benefit from increased surveillance by government regulatory agencies, which currently do not pay any special attention to the fact that waste collectors are exposed to high levels of hazardous agents including microorganisms. Because waste collection workers belong to the service industry, the exact number of individuals working in this sector is unclear, and occupational illnesses are not officially reported. In conclusion, given that waste-handling activities were found to be significantly associated with high levels of bacteria, GNB, and fungi, various engineering, administrative, and regulatory measures should be considered to reduce exposure to airborne microorganisms during household-waste collection. Authorities responsible for the inspection of the work environment should engage with private and governmental waste-management companies to ensure the provision of necessary measures, such as automated waste collection, clean rest areas, personal protective equipment (gloves and respirators), meticulous personal hygiene, and medical surveillance for illnesses brought on by airborne microorganisms.
References 1 An H, Englehardt J, Fleming L, Bean J. Occupational health and safety amongst municipal solid waste workers in Florida. Waste Manag Res. 1999;17(5):369–77. 2 Poulsen OM, Breum NO, Ebbehoj N, Hansen AM, Ivens UI, Van LD, et al. Collection of domestic waste. Review of occupational health problems and their possible causes. Sci Total Environ. 1995;170(1–2):1–19. 3 Ivens UI, Breum NO, Ebbehoj N, Nielsen BH, Poulsen OM, Wurtz H. Exposure-response relationship between gastrointestinal problems among waste collectors and bioaerosol exposure. Scand J Work Environ Health. 1999;25(3):238–45. 4 Heldal KK, Halstensen AS, Thorn J, Djupesland P, Wouters I, Eduard W, Halstensen TS. Upper airway inflammation in waste handlers exposed to bioaerosols. Occup Environ Med. 2003;60(6):444–50.
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13 Gorny RL, Dutkiewicz J. Bacterial and fungal aerosols in indoor environment in central and eastern European countries. Ann Agric Environ Med. 2002;9(1):17–23. 14 Lavoie J, Dunkerley CJ, Kosatsky T, Dufresne A. Exposure to aerosolized bacteria and fungi among collectors of commercial, mixed residential, recyclable and compostable waste. Sci Total Environ. 2006;370:23–8. 15 Korea Occupational Safety Health Agency (KOSHA). Study on the validity of installation of washing facilities in the workplace (focus on sanitation work). Research No. 2010-84915. South-Korea, KOSHA, 2010(in Korean). 16 Solans X, Alonso RM, Constans A, Mansilla A. Occupational exposure to airborne fungi and bacteria in a household recycled container sorting plant. Rev Iberoam Micol. 2007;24(2):131– 5. 17 Poulsen OM, Breum NO, Ebbehøj N, Hansen AM, Ivens UI, Lelieveld DV, et al. Sorting and recycling of domestic waste. Review of occupational health problems and their possible causes. Sci Total Environ. 1995;168(1):33–56. 18 Marchand G, Lavoie J, Lazure L. Evaluation of bioaerosols in a municipal solid waste recycling and composting plant. J Air Waste Manag Assoc. 1995;45:778–81.
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