Occupational health and safety in agriculture. A systematic review

Introduction: The prevalence of occupational diseases in the agricultural sector is higher than in other industries, since agricultural workers are at higher risk of exposure to different chemicals and pesticides, and are more prone to occupational accidents. Objective: To conduct a review of recent literature on occupational health and risk in agriculture. Materials and methods: A literature search was conducted in PubMed, SciencieDirect and Scopus using the following search strategy: type of articles: original research papers; publication language: English; publication period: 2006-2016; search terms: “agricultural health”, “agrarian health”, “risk factors”, “epidemiology”, “causality” and “occupational”, used in different combinations (“AND” and “OR”). Results: The search yielded 350 articles, of which 102 met the inclusion criteria. Moreover, 5 articles were found in grey literature sources and included in the final analysis. Most research on this topic has been conducted in the United States, which produced 91% (97/107) of the articles included in the review. Conclusions: Most studies on agricultural health focused primarily on the harmful effects of occupational exposure to agrochemicals and pesticides, and the consequences of occupational accidents. However, since more than 90% of these studies come from USA, a more comprehensive approach to agricultural health is required, since what is reported here may be far from the reality of other regions, especially Latin America.


Introduction
It is widely believed that many important human diseases originated with the advent of agriculture. 1 Nowadays, there are legislative instruments to regulate health in the agricultural sector, as well as established concepts explaining what both human and animal health entail for such sector. For example, when addressing safety and health in agriculture, the International Labor Organization (ILO) defines agricultural health as the promotion of a safe and healthy environment for human beings that take part in farming activities; 2 in addition, according to the Food and Agriculture Organization of the United Nations (FAO), agricultural health is the primary health of animals, plants, products and by-products obtained from both sources, soil, water, air, and people, and the close relationship between them, which incorporates agro-ecological science principles to promote food security and sovereignty, and popular participation through the formulation, implementation and monitoring of policies, plans and programs for the prevention, control, and eradication of pests and diseases. 3 Likewise, the National Cancer Institute, the National Institute of Environmental Health Sciences and the Environmental Protection Agency (EPA) of the United States, within the framework of the Agricultural Health Study, 4 have conducted several studies where the main objective was to evaluate agricultural health, understood as the interaction between agricultural exposures and the development of cancer and other diseases in agricultural workers. 4 In comparison with other industries, agriculture provides a significant amount of jobs worldwide. Nearly 40% (450 million) of workers are in the farming sector and represent more than 40% of total agricultural labor force. 5 In 2016, 40% of the total population of developing countries worked in the agricultural sector or in agriculture-related activities, while in developed and industrialized countries, only 3% of their population did it. 6 However, even in industrialized countries, this sector constitutes a significant portion of the total workforce.
It has been estimated that by 2013 there were about 12 million farms in the 27 European Union member countries, with an average extension of 14.2 hectares, of which, 95% were family farms. 7,8 In the case of Central and North America, in 2010, there were around 4 million farms in Mexico occupying 932 149 million hectares of land, while in USA, there were 2.32 million farms using about 56 667 million hectares; 9 likewise, in Canada, around 64 232 million hectares were used as agricultural land by 205 000 farms in 2011. 10 Regarding Oceania, in 2014 there were 135 000 farms in Australia using around 394 million hectares of land, 11 while in New Zealand, nearly 78 549 farms were found in approximately 555 000 hectares by 2012. 12 Finally, in countries such as Brazil, about 33.81% of the land was used for agricultural purposes, and approximately 21 203 million hectares of land were used for cereal production, according to data reported for 2015. 6 Similarly, according to the ILO, about 317 million people worldwide suffer from occupational accidents, and 2.34 million die due to occupational accidents and diseases. 2 In Latin America, about 11.1 fatal accidents take place for every 100 000 workers in the industrial sector, while in the agriculture industry and the agricultural services provision services sector, there are about 10.7 and 6.9 fatal accidents for ev-ery 100 000 workers. 13 In addition, in some countries, several important economic sectors such as mining, construction, agriculture, and fishery have the highest incidence of occupational accidents. In this regard, according to the Bureau of Labor Statistics, in 2013 the injury rate of agricultural workers exceeded the 40%, being the highest among all industries; also injury rates in crop production and animal production workers were 5.5 and 6.7 for every 100 workers, respectively. In contrast, injury rate in workers from all industries was 3.8/100. 14 In 2013, 479 occupational deaths were reported within the agricultural industry in USA, that is, a fatality ratio of 22.2/100 000, which is significantly higher than the 3.2/100 000 ratio reported for all occupations in the same country. 15 Somehow, occupational deaths in the agricultural sector in other countries are significantly lower. For example, in Canada and Finland death ratios for 2013 were 11.6/100 000 and 6.5/10 000, respectively. 16,17 Regarding, non-fatal injuries and diseases, monitoring them is a more challenging task, given the scarcity of data and population based studies. In USA, the non-fatal injury rate in agricultural workers ranged from 5/100 000 to 170/100 000 between 2002 and 2017. 15,18,19 When it comes to occupational diseases in the agricultural sector, these are even more difficult to quantify since they are rarely associated with situations happening at the workplace, and in fact, there is not any reporting mechanism in USA.
According to surveys conducted by the Bureau of Labor Statistics in 2014, occupational disease rate in agricultural workers from USA was 3.1/1 000. 15 However, sensitivity and specificity of these data need to be considered when taking into account such reports, since they greatly depend on the information provided by employers. In said country, most occupational diseases are skin problems (56%), chronic traumas (14%) and respiratory problems (13%). On the other hand, in Finland, an occupational diseases ratio of 6.4/1 000 in this sector has been reported, out of which 40% represent respiratory disorders, 21%, skin problems, and 31%, joint disorders. 20,21 However, most studies on occupational health and safety in agriculture carried out in recent years have focused on workers inhabiting industrialized countries going through rapid socioeconomic and political changes. 22 In developing countries, the rapid emergence of industries such as chemical production, car manufacturing, and agriculture has resulted in fewer safety regulations compared to developed countries, which in turn has worsened their existing environmental and occupational problems. 23 In this sense, there is strong evidence that there is a correlation between health condition and socioeconomic status, and that, in general, people's health in low-income countries is affected by several factors, including environmental, cultural, and socioeconomic conditions . 23,24 Other public health problems affecting these countries include outbreaks of zoonotic diseases and of infections caused, on the one hand, by enteric pathogens due to the consumption of contaminated food, and, on the other, by antimicrobial-resistant organisms acquired in animal production activities. 25 Therefore, in these countries, many of environmental, occupational, and public health problems are affected by the global economy and are too complex to understand, thus their mitigation requires jointly actions by both, actors from several disciplines, and representatives of the different industries.
Since most studies on agricultural health conducted in developing countries focus on small rural communities, further research on this topic in these countries with a broader scope is urgently required. Taking the above into account, the aim of this paper was to conduct a review of recent literature on occupational health and risk in agriculture.

Materials and methods
In April 2016, a systematic review was carried out in the ScienceDirect, Scopus and PubMed databases based on the PRISMA guidelines for conducting systematic reviews, 26 and the methodology proposed by Cardona. 27 Exhaustivity was guaranteed by using non-DeCS (Descriptors of Health Sciences) descriptors as search terms. Also, sensitivity was ensured using descriptors registered in the DeCS or the Medical Subject Headings (MeSH) thesauruses as search terms. The combination of Boolean operators, based on the research question, provided specificity. The "agricultural health "OR" agrarian health" general search path was used alone or combined with the terms "risk factors" OR "epidemiology" OR "causality" OR "Occupational" through the following operators "AND ALL" or "AND". In addition, "2006 to present", "Published 2006 to present" and "published in the last 10 years" publication time filters were used in the searches conducted in ScienceDirect, Scopus, and PubMed, respectively, thus the search included scientific literature published between April 2006 and April 2016.
The specific search combinations used in each database are shown below: ScienceDirect: TITLE-ABSTR-KEY ("agricultural health" OR "agrarian health") and ALL ("risk factors" OR "epidemiology" OR "causality" OR "Occupational").
Finally, the citations of the studies retrieved in the searchers, together with their respective abstracts, were imported into the Thomson Reuters EndNote® software manager, 2011 Version, in order to remove duplicate references.

Inclusion and exclusion criteria
Only research articles written in English and published between April 2006 and April 2016 were considered for inclusion. Studies that were finally included for full analysis were required to follow a methodology that allowed the extraction of elements useful in the definition of the concept of agricultural health. Other articles that provided empirical evidence, based on retrospective and prospective findings, regarding agricultural health were also considered. On the other hand, studies in which the units of analysis were in vitro models, cells or those that were conducted only in laboratories were excluded. In order to ensure the reproducibility of the review, two researchers independently conducted the searches and selected the articles to be included for full analysis. Disagreements were solved through consensus.
The following data were extracted from all studies included in the review, and then entered into an information collection form for their analysis: general information (title, name of the journal in which the article was published, year of publication, and country in which the study was conducted); agricultural health topics addressed in the paper (occupational exposure to pesticides or to chemical products, agricultural health and safety, medical training and agricultural health); study type (retrospective, prospective, cohort, qualitative, exploratory, cross-sectional, case-control study), and the organizations involved in the making of each study (academic institutions, public institutions and government agencies).

Results
A total of 350 studies were retrieved after the initial search was carried out (ScienceDirect 23, Scopus 160, and PubMed 167). Once duplicates (n=180) were removed, 43 publications were excluded for full-text reading since, based on the reading of titles and abstracts, it was decided they did not meet the established inclusion criteria and did not provide useful information for the objective of the review. Out of the 127 studies selected for full-text reading, 25 were excluded based on the established exclusion criteria. Finally, 102 articles were included for full analysis. In addition, 5 studies that were published in journals that were not indexed in the databases but met the inclusion criteria were also included. It should be noted that these 5 gray literature studies were retrieved from Google Scholar. The studies screening and selection process is shown in Figure 1. Despite the 107 studies were conducted in 11 countries, most of them (n=97) were carried out in USA, while the remaining 10 were conducted in the other 10 countries, including France and Canada. Furthermore, in the USA, studies were mainly carried out in the following States: California, Colorado, Iowa, North Carolina, Kentucky, Minnesota, Nebraska, New York, Texas, Washington, and Wisconsin. Table 1 shows the journals, in a descending order, in which the studies were published; data regarding impact factor, publishing house, year, country and frequency of publication, and field of study of each journal are also shown. The journals in which most studies included were published were the Journal of Agromedicine, Environmental Health Perspective (n=22), and Environmental Health Perspective (n=19).
USA was the most frequent country of publication, followed by the United Kingdom and the Netherlands. Environmental Health Perspective had the highest impact factor for 2015 (8.44), followed by Journal of Cancer (5.531) ( Table 1).

Agricultural health topics addressed in the studies
Agricultural health concepts addressed in the 107 studies, and inferred by us based on their full analysis, are shown in Table 2. Concepts were classified into seven categories. Table 2. Main concepts of agricultural health inferred from the analysis of the studies included in the systematic review.

Concepts Institution that mainly addresses the concept References
Assessment of cancer and other diseases among farmers and their family members in relation to their occupational exposure in agriculture and their lifestyle.
To reduce the risk of death from livestock-handling-related injuries and to ensure compliance with recommended practices regarding safe livestockhandling and proper facilities, especially when working with aggressive cattle.
Centers for Disease Control and Prevention (CDC) 30,31 Health and safety in farms.
To implement better farm machinery safety and hazards control measures such reducing exposure of children to this machinery and making mandatory to wear helmets when riding quad bikes, motorbikes, and horses.
Australian Centre for Agricultural Health and Safety and School of Public Health, University of Sydney

32-35
Occupational health and risks in agriculture.
To identify factors associated with work-related injuries in farmers.
To provide better information about agricultural health policies and guidelines on good working practices to older farmers, such as policies governing the maximum work hours and the minimum rest hours per week, as well as guidelines about the proper distribution of farming tasks, and information on ergonomic advances and new farm equipment and technology. Source: Own elaboration.
Some of the agricultural health topics addressed in the studies reviewed include several occupational factors associated with the development of physical diseases such as age, workforce management, ethnicity, types of products used by workers in farms, work practices, agricultural machinery engineering controls, and the use of personal protection equipment, among others. 28,30,32,39,42,44 It should be noted that workforce varies significantly from one region to another. Also, the number of permanent employees working outside the farms has increased, which means a greater exposure to occupational risks. 45 Furthermore, in USA, according to the 2014 Census of Agriculture, conducted by the United States Department of Agriculture, the average age of farm workers was 54.3 years, which may increase their susceptibility to the adverse effects of occupational exposure, for example, an increased risk of developing chronic diseases affecting the respiratory and the locomotor systems. 46

Discussion
Agriculture is one of the most dangerous industries for workers in both, developing and developed countries. 1 In comparison with other industries, occupational accidents, chemical exposure, and fatality rates are higher in farm workers, and resources available for their compensation are scarce. 7,20,24,45 One of the main challenges of occupational health and safety in agriculture is that a wide variety of working activities are carried out in this sector, which, unlike in other industries, makes it necessary to develop and implement interventions aimed at these many activities. In addition, the monitoring of farm workers' health condition and the reporting systems of work-related injuries are inadequate and non-standardized. For example, according to the ILO, official data on the incidence of occupational accidents and work-related diseases in agricultural workers are inaccurate, notoriously underestimated and insufficient as indicators to measure the effect of occupational health and safety interventions. 2,13 In recent decades, the interest in agricultural health has increased worldwide, particularly in the field of occupational safety and health. This has led to positive changes in national policies on working practices in the agricultural sector, and the involvement and jointly effort of public agencies, social organizations, occupational health experts, the academy, agriculture companies, unions, and public and private insurance companies. 6,14 Also, both research and prevention actions regarding occupational health and safety in agriculture have increased significantly in the last decade, since more support has been given to this field of study by different academic institutions, private organizations, and government agencies that has resulted in the creation of academic programs aimed at improving agricultural safety and health (ASH), as well as the foundation or involvement of existing institutions in the research of ASH (Tables 3 and 4). However, these initiatives have only been considered in recent years, and so far, most of them have been implemented in developed countries such as USA, Canada, and France. Table 3. Academic institutions working in agricultural safety and health programs as of 2016.

Institutions
Agricultural safety and health program Location Type of Institution

Vermont Farm Health Task Force
To ensure a healthy and safe workforce in Vermont by working with farmers, medical practitioners, agricultural professionals, public and behavioral health providers and staff from key state and community agencies. To improve human health and safety associated with rural and agricultural work, life and environments by conducting high quality research, developing and delivering health and safety information, and exploring innovative service models.

Private National Rural Health Association
To provide leadership on rural health issues through advocacy, communications, education, and research.

European Union Governmental
AgHealth Australia (Australian Center for Agricultural Health and Safety) To research on non-intentional fatal and non-fatal incidents occurring on farms across Australia.
To provide on-farm health and safety auditing services, since audits start the process of identifying gaps and assist in working towards meeting health and safety requirements.

Australia
Governmental National Rural Health Alliance Inc.
To improve the health and well-being of the more than 6.7 million people in rural and remote Australia Governmental Somehow, the situation in Latin-America is different. According to the ILO, while 59% of the total population in this region are engaged in farming activities, per year there are around 250 million accidents affecting both permanent and temporary workers. National regulations in Latin-American countries concerning safety at work are often too general and vague. In addition, in some of these countries, this situation is worsened due to the exclusion of the agricultural sector and farm workers from workers' compensation insurance systems. Generally, agriculture is classified by these systems in their global statistical estimates as part of other industries such as forestry and fishing, which translates into the underreport of occupational accidents in this sector. 2,13 Health problems associated with the exposure to agrochemicals

Systemic diseases
Between 29% and 44% of agricultural workers experience skin or respiratory diseases associated with exposure to agrochemicals 47-54 and scarce use of personal protective equipment while handling chemicals. 5,55 Generally, skin is the organ most affected in workers exposed to these substances. 56 Headaches (90%), skin rashes (85%), eye irritation (43%) and fatigue (23%) have also been reported as symptoms related to the exposure to agrochemicals. 57 Likewise, more than half of workers report experiencing any of these or similar symptoms after prolonged exposure to agrochemicals, and out of these, only half affirm they receive any form of assistance for medical treatment. 29,47,58,59 In addition, respiratory and flu-like symptoms have been associated with the exposure to agrochemicals among agricultural workers from Iowa after the application of insecticides on cattle, as well as skin reactions, mostly over hands and arms. 31,33,37,60-62

Effects on pregnancy, fertility and fetal development
Based on the studies reviewed, there is an association between the use of thiocarbamates, carbaryl, and pesticides and a higher risk of spontaneous abortion; also preterm birth has been associated with the use of herbicide mixtures or sequential applications. 17,63,64 On the other hand, there was not a consistent or strong pattern of association between being exposed to pesticides and altered pregnancy time. [65][66][67] However, it has been described that women and men working in agricultural industries and women living in farms have a higher risk of infertility. 68,69 Other birth defects related to the use of agrochemicals include oral and facial clefts 70,71 and congenital anomalies. 65

Organophosphate poisoning effects on farm workers' health
The serious outcomes regarding organophosphate poisoning in these workers have been well described, including organophosphate induced polyneuropathy (OPIDP), permanent neurological deficits, neuropsychiatric disorders, peripheral neuropathy, poor neuropsychiatric test results, and multiple chemical sensitivity. [72][73][74]

Mortality rates
Mortality rates due to exposure to agrochemicals in USA have declined markedly each year; 17,38,75-78 hospitalizations and acute intoxications have also decreased since workers have been provided with better training, better technological devices, non-toxic mixtures formulations, and greater regulation and control policies which include the registration of the most toxic agents 34,35,43,79 (Table 5).

Cancer and exposure to agrochemicals
Regarding associations between developing cancer and performing any type of agricultural activity, it has been reported that lip cancer occurs in 29% of agricultural workers. 75,80,81 Also, it has been described that up to 19% farm workers, regardless of their sex, have been diagnosed with multiple myeloma, and that said condition has been associated with their occupational exposure. [82][83][84][85][86] Other types of cancer observed in this population and that have been related to working in agriculture include non-Hodgkin's lymphoma (14%), prostate (14%), skin (7%), melanoma (6%), brain cancer (4%), and soft tissue sarcoma (3%). [87][88][89][90][91][92][93] Additionally, some types of cancer have been associated with specific agricultural exposures, and evidence shows that their occurrence may be higher in certain subgroups of agricultural workers. 94 For example, a greater association between exposure to herbicides such as a phenoxyacetic acid (e.g. 2,4 D) and having non-Hodkin's lymphoma has been described. 82,95 Yet, regarding exposure to Atrazine , the most widely used herbicide in USA, there is no evidence of an increased risk of colon cancer, soft tissue sarcoma, Hodgkin's disease, multiple myeloma, or leukemia 63,[95][96][97] (Tables 5 and 6).
Finally, many types of cancer have been associated with agricultural exposures in both epidemiological and cohort studies, but results by some of these studies have been inconsistent and, thus, there is no consensus on their causality. Source: own elaboration. Source: own elaboration.
Farmers and agricultural workers are subject to multiple hazardous exposures to pesticides, fertilizers, paint fumes, solvents, welding fumes, dust, pathogens, and endotoxins. 63,69,98,99 In general, most agricultural health studies have been conducted on permanent workers and, to a much lesser extent, on their partners. However, little research has been done regarding temporary agricultural workers, who may be subject to prolonged occupational exposures. Furthermore, these studies have generally focused on crop production workers, who are exposed to different pesticides (depending on the crops) only a few times per year. 98 Somehow, it should be noted that the results obtained in this review may greatly depend on the heterogeneity of the studies, the type of study, the geographical area and the period in which they were conducted, and the limitations of each study regarding the assessment of agricultural exposures.

Other conditions associated with agricultural exposures
Different physiological conditions, injuries or mechanical traumas, and infections caused by microorganisms have been associated to some extent with agricultural work. For example, it has been reported that more than 50% of agricultural workers experience hearing loss. 100 Also, the adoption of forced postures, the performance of repetitive movements and the manual handling of heavy loads have been associated with musculoskeletal disorders such as chronic back pain and low back pain, being more frequent in older men than in women (50% and 10%, respectively), and even with spontaneous miscarriages. 101 Furthermore, agricultural equipment operators are exposed to whole-body and hand-arm vibrations that cause them several health problems and health conditions, including tendinitis, tenosynovitis, carpal tunnel syndrome, degenerative changes of the spine, low back pain, herniated discs, and peripheral, vascular, gastrointestinal and vestibular nerves injuries. Likewise, excessive physical effort and fatigue as a result of using traditional farming tools and methods may increase the risk of occupational accidents. 101 On the other hand, agricultural work-related respiratory disorders include occupational asthma, allergic rhinitis, chronic bronchitis, extrinsic allergic alveolitis (or hypersensitivity pneumonitis), which are mainly associated with working in closed areas such as nurseries and silos where workers are exposed to high concentrations of allergen dust, fumes, pollen, dust mites, and grain dust. 40,102 According to some studies, chronic bronchitis is more prevalent in farmers compared to the general population. In this regard, it has been reported that most farmers with this disease have a history of exposure to grain dust or work in confined pig farms. Chronic bronchitis has also been described in farmers who grow cereals, especially during harvest time. 40,103,104 Among infections caused by microorganisms as a result of working in agricultural activities, it has been described that both latent tuberculosis infection and tuberculosis disease (caused by the Mycobacterium tuberculosis bacterium) cases are increasing in the migrant workforce, mainly in Mexico and Central America, and that most of cases occur in the Mexico-United States border area. 105,106 In addition, prevalence rates are significantly higher in communities living in said area. In that regard, Garfein et al. 107 report the need to improve the diagnosis and the monitoring of TB cases, as well as to promote the successful completion of TB treatments in order to reduce the occurrence of multidrug-resistant TB cases.
According to the evidence found here, studies on agricultural health and safety address topics such as cancer screening, autoimmune, respiratory, neurological and reproductive diseases, allergic disorders, work-related injuries, and overall mortality rates and their association with a wide range of agricultural exposures. Most of these studies have been conducted in northern and southern mid-latitudes, mainly in USA, possibly because this country is one of the largest consumers of insecticides and agrochemicals in the world. 6 In addition, 47% of the rural population in USA is engaged in some type of agricultural activity, and the US Government has acknowledged both, life and health sciences, as important factors for the Nation's economic growth, as well as the importance of increasing the quality of treatment provided to people who experience agricultural work-related injuries. 22

Limitations
Due to their design, in a systematic review fewer studies may be included compared to a narrative review. Also, systematic reviews are observational and retrospective studies that are susceptible to biases.

Conclusions
In agricultural workers, exposure to pesticides and other agrochemicals is one of the main occupational hazards, which can lead to intoxication and death, and, in some cases, to occupational cancers and reproductive disorders. Likewise, poor compliance with safety and health regulations in this sector worsens this situation.
The absence of registers regarding infections and infectious diseases affecting both humans and animals has been so far addressed independently by several disciplines, but not in a holistic way, which may be leading to the underreport of occupational diseases in agricultural workers.
The existing studies on agricultural health have been conducted mainly in developed countries, particularly in USA, and most of them focus on the harmful effects resulting from occupational exposure to the handling of farm machinery, and on work-related traumas. However, an adequate approach to agricultural health requires further discussion and a wider scope, since what is reported by said studies may be far from the reality of other regions, especially Latin America, where workers' agricultural health may be conditioned by several factors including weather, fauna, population density, living conditions, level of schooling, professional background, technological development, and health care services quality.
Even if systematics reviews have some limitations, results obtained here show that it is a useful tool for the identification of predominant research topics within a certain field of study. Further research should focus on studying agricultural health in other regions of the world and in the different production systems.
It is worth noting that in Latin America, most agricultural research is carried out by government and federal government agencies, which makes it difficult to access information regarding agricultural health in these countries.

Conflicts of interest
None stated by the authors.