Title

Mental Health and Fatigue of Sheep Farmers Exposed to Organophosphate Pesticides

Author Details

C.A. Jackson PhD, A. Spurgeon PhD, and K. Gardiner PhD

Correct Reference
C.A. Jackson PhD, A. Spurgeon PhD, and K. Gardiner PhD, Mental Health and Fatigue of Sheep Farmers Exposed to Organophosphate Pesticides, International Journal of Rural Psychology, Vol. 4, No. 13, URL http://www.ruralpsych.com/Members/RefereedReports/Jackson Spurgeon Gardiner/RR-Jackson-spurgeon-Gardiner.html

Affiliation & Contact Details

Institute of Occupational Health

University of Birmingham

Edgbaston B152TT

United Kingdom

Corresponding Author

Dr Craig Jackson

School of Health and Policy Studies,

Faculty of Health and Community Care

University of Central England.

Birmingham,

United Kingdom, B42 2SU

Craig.Jackson@uce.ac.uk

Abstract

To investigate the role of low level pesticide exposure and psychosocial factors in the health of English sheep farmers, mental health and fatigue were assessed in 259 farmers exposed to organophosphate pesticides (OPs) while dipping sheep, at least 28 days after exposure. Of exposed farmers, 38% showed mental health problems and 44% displayed severe fatigue. Of farmers reporting no exposure, incidence was 27% and 40% respectively. Risk of developing case-qualifying mental health and severe fatigue scores (as measured by the GHQ and CFS respectively) were slightly raised in the exposed farmers (odds ratios 1.67 and 1.19 respectively) when compared with non-exposed farmers. However, the number of mental health and severe fatigue cases across the exposed and no exposure groups were not significant (p = 0.43 and p = 0.89 respectively). Case-qualifying scores were considered to represent probable cases of psychological distress and severe fatigue. Relationships between long term OP exposure, mental health and fatigue were non significant (p = 0.55 and p = 0.95 respectively). Regression models showed three variables (stressful life events, agricultural satisfaction and handling sheep within 48 hours of dipping) were significant in prediction of mental health; exposure to spray from the dip bath while dipping and mental health were significant factors in prediction of fatigue. Farmers who reported excessive spray rising from the dip bath were three times as likely to rated themselves ill. Results support a biopsychosocial model of response to hazard exposure, as illness appeared to be explained by the interplay of physical and psychosocial factors rather than any single neurotoxicological, physiological or psychological cause.

Sheep dipping to control various parasitic infections has been carried out voluntarily in the UK for many years by sheep farmers. However, from 1976 until 1988, (apart from a brief period between 1983-1984), compulsory dipping was introduced by the UK government in an attempt to control the re-emergence of an epidemic of sheep scab. From 1984, as a result of a ban on organochlorine compounds, products containing organophosphate-based pesticides (OPs) became the approved dip of choice for sheep farmers. Following their introduction however some farmers began to complain of symptoms of poor health which they attributed to exposure during dipping. Regular dipping with these products remains widespread today.

The acute neurotoxic effects of short-term high exposures to OPs in humans have been well documented (Marrs 1993). However, unlike short-term effects, farmers' symptoms appeared to be chronic, persisting long after exposure had ceased and were often associated with relatively low exposures, as indicated by little or no changes in blood cholinesterase levels, (Rees 1993 & 1996). Symptoms also tended to be diverse in nature (National Farmers Union 1992, Sims 1994,) and not always consistent with the expected pattern of an acute cholinergic response to OP exposure, (Jackson & Spurgeon 2001). In particular they tended to focus on aspects of mood and mental health rather than muscarinic or nicotinic effects.

The possibility that OP exposure can result in long term effects on the nervous system which are different both in manifestation and causal mechanism from an acute response is controversial but has received increasing attention in recent years. Jamal (1997) describes two possible syndromes of Chronic Organophosphate Induced Neuropsychiatric Disorder (COPIND), with Type 1 resulting from a single intoxication incident and Type 2 resulting from low-level long-term exposure. Both syndromes are argued to involve effects on cognitive functioning and mental health. Current epidemiological evidence however is limited and contradictory. Some environmental studies have shown evidence of increased suicide rates in areas with greater OP use in the USA (Gershon & Shaw, 1961), and in Spain, (Parron et al 1996). However, exposure to OPs has not been identified as a major factor in the excess of mortality from suicide found among British farmers (HMSO 1993; Kelly et al. 1995; Malmberg et al. 1997).

Some studies of health effects in long-term OP-exposed workers have indicated effects on mood states as well as on neuropsychological performance (Daniell et al.1992; Dudek & Bazylewcz-Walczak 1993; Fiedler et al. 1997; Korsak & Sato 1977; Stephens et al. 1995). In particular the study by Stephens et al. identified an increased risk of mental health problems in British sheep farmers involved in dipping. However, the design of the study did not allow the role of OP exposure relative to that of other potential effect modifiers to be determined. An additional complication faced by studies which use retrospective exposure models is the level of reliability of farmers' recall of pesticides used by them throughout their working life time. Such accounts could at best only partially describe the true picture - which is often exposure to a wide range of OP compounds of varying neurotoxic potential. Other studies of mental health have considered the role of psychosocial factors such as loneliness (DeBerard et al. 1995), isolation (Booth et al. 2000) or deliberate avoidance of assistance (Gerrard 1998). Recent work focusing on stress among farmers in the UK (Simkin et al. 1998) has demonstrated that a significant proportion suffer as a result of enforced paper-work, regulations, and financial worries.

The relative importance of neurotoxicant exposure as a cause of poor mental health therefore remains unclear. The continuing debate on this subject has tended towards an assumption that the source of peoples' symptoms must be either their chemical exposure or their psychosocial situation. In other words the problem must be either physiological or psychological. Recent discussion of the response to hazard exposure however has included the possibility of a third multifactorial explanation (Spurgeon et al. 1996). Essentially this invokes a biopsychosocial model which proposes a continuous interplay between physical and psychosocial factors and thus accepts that the illness response can represent the product of both types of influence. The distinction between physical and psychological complaints is therefore regarded as an artificial and unhelpful one. This may offer a useful way forward in situations where individuals strongly attribute their symptoms to low level hazard exposure in the absence of any plausible toxicological explanation.

The aim of the current study therefore was to investigate further the current prevalence of mental health problems in English sheep farmers and to determine the possible role of OP exposure in the context of other simultaneously occurring psychosocial factors. The specific objectives were (i) to determine whether there was any association between exposure to OPs as a result of sheep dipping, and the reporting of mental health symptoms (ii) to determine the role of other factors, notably individual differences, life stress and life satisfaction in reporting of mental health symptoms, and thus to develop multivariate models to predict mental health in farmers exposed to OPs.

Method

The sample of sheep farmers was obtained from those registered with the British Wool Marketing Board (the criteria being those keeping 5 or more sheep). All those living in one county in the north of England (Lancashire) were invited to participate in the study and to complete a screening questionnaire (n = 2040, Phase I) in order to determine their suitability for the study. All farmers between the ages of 18 and 80 were initially included. However, farmers were subsequently excluded if their first language was not English; if they had a learning or reading disability (because of the requirement for questionnaire completion); if they were suffering from a pre-existing disease likely to affect the nervous system; had a previous head injury resulting in loss of consciousness; a history of substance abuse or had experienced an OP poisoning episode resulting in hospital treatment. The exclusion criteria concerning any previous acute exposures related specifically to any incidences of hospitalisation due to exposure, and it is accepted that some farmers who may have experienced high-level acute exposures in the past may not have sought hospital treatment (Woods, 1999) thereby remaining in the study albeit after experiencing previous acute exposures. Those remaining in the study after Phase I were sent a postal questionnaire pack (Phase II). This was dispatched at a time when dipping was unlikely to have taken place within the previous 28 days. Those who reported dipping within that period were also excluded from the study in order to negate inadvertent reporting of any possible intermediate or delayed effects occurring as a result of possible sub-acute exposure within that time, which can occur within 28 days of exposure, as noted by Jamal (1997). In addition to a questionnaire concerned with demographic details the questionnaire pack also comprised the following:

1. General Health Questionnaire GHQ (Golberg 1985)
2. Chronic Fatigue Scale CFS (Chalder et al. 1993)
3. Impulsiveness Questionnaire IVE (Eysenck & Eysenck, 1991)
4. Life Events Inventory Scale LEI (Spurgeon et al. 2001)
5. Satisfaction with Agricultural Life Scale SAL

The GHQ is a well-established psychiatric screening questionnaire developed for use with community samples. The CFS is a recently developed scale, based on the response and scoring system of the GHQ, but focussing specifically on the reporting of severe chronic fatigue. Current thinking tends to the view that chronic fatigue may be a biopsychosocial problem resulting from an interaction between the response to a physical hazard and various psychosocial modifiers. As such it constitutes a potential outcome of interest in relation to OP exposure which may be similar but not identical to the reporting of mental health problems. Both the GHQ and the CFS were scored using the binary method, with the two least symptomatic responses for each item scoring 0, and the two most symptomatic responses scoring 1. The GHQ provides both global scores and scores for four separate subscales: anxiety, depression, somatic symptoms and social dysfunction. The CFS provides both global scores and scores for two separate subscales: mental and physical fatigue, and has been found to be reliable and valid (Chalder et al. 1993). For both scales total scores equalling or exceeding a value of 4 were classed as "case qualifying". It should be noted however that the CFS does not measure Chronic Fatigue Syndrome when applied in a cross-sectional design such as this, since the diagnosis of CFS requires two instances of severe fatigue, measured six months apart. In this case therefore, the scale simply provided a measure of severe fatigue.

The IVE scale was included to assess aspects of risk taking behaviour which may have relevance in terms of attitudes to health and safety at work The scale measured three separate personality factors: impulsiveness, venturesomeness and empathy. The LEI consisted of a revised and updated version (Spurgeon et al. 2001) of the original scale, (Cochrane & Robertson, 1973) which was designed to assess levels of stress associated with specific life events occurring in the six months leading up to questionnaire completion. The SAL was a purpose-developed questionnaire designed to explore job/life satisfaction in relation to aspects of rural life.

Overall exposure to OP dips was estimated in units of individual dips, calculated using a simple formula: mean number of sheep kept in the years between 1990 and 1999, multiplied by the number of dipping sessions per year, multiplied by the number of years spent dipping with OP dips, expressed as:

(Sheep) X (Dips) X (Years).

Handling of OP concentrate was estimated in units of individual/dilution episodes. Buchanan et al. (2001) observed that in practice, farmers made dip replenishments approximately after every 100th sheep as a practical way of remembering when to replenish the dip bath. The formula used in the present study therefore was: estimated number of replenishments per session (1 per 100 sheep), multiplied by the number of dips per year, multiplied by years spent dipping with OPs, expressed as:

(Concentrate handling episodes) x (Dips) x (Years).

In addition to these overall measures a number of specific aspects of exposure were assessed by questionnaire, for example the design of the dip bath, dipping procedures, use of personal protective equipment and knowledge of the health and safety aspects of OP use. The study used a significance level of p = 0.05.

In Phase I, responses were received from 478 individuals, with 70 exclusions made, reducing the number of participants suitable for Phase II to 408. Of the 408 questionnaire packs dispatched, 270 were completed correctly and returned before the deadline. Eleven further dippers were excluded from Phase II on suspicion of recent dipping with OPs, giving a final useable response total of 259. The mean age of the final sample group was 50 years ± 11 (min. 23, max. 79, 95% C.I. = 49-52). Males accounted for 85.1% (mean age 50 years ± 11, min. 23, max. 79, 95% C.I. = 49-52) and females for 13% (mean age 50 years ± 10, min. 33, max. 77, 95% C.I. = 47-55). Sex was unknown for 1.9%. There was no significant difference in age between the sexes, (F = 0.08, p = 0.76). Internal consistency of the psychometric measures used was good: General Health Questionnaire = 0.83, Chronic Fatigue Scale = 0.87, and Satisfaction with Agricultural Life = 0.72.

Objective 1

Of the farmers with OP exposure (n = 209), 38% qualified for psychiatric caseness as measured by the GHQ and 44% for severe fatigue as measured by the CFS. Twenty-two farmers reported no OP exposure. Of those, 27% qualified for psychiatric caseness and 40% for severe fatigue. Initial comparison of the two groups indicated no significant difference in the percentage from each group qualifying for psychiatric caseness or severe fatigue (Chi-square = 0.61, p = 0.43 and Chi-square = 0.02, p = 0.89 respectively). However the odds ratio for psychiatric caseness in OP exposed dippers was 1.67 and for severe fatigue caseness was 1.19, indicating a slightly increased risk in the exposed group. Correlation (Pearson's r) between the two measures of long term OP exposure and GHQ and CFS scores were generally low.

Phase I respondents were asked to state if they believed they were suffering any form of ill health that they attributed to their dipping work, and these were categorized into groups who had previously dipped with OPs and those who had not, and the distribution is shown in Table 1. Chi square analysis (with Yates' correction for small samples) revealed a significant difference in perceived ill-health between OP users and non-users (Chi-square = 5.2, p = 0.02).

In order to investigate further the relationship between increased OP exposure and mental health or severe fatigue problems, farmers were classified into four exposure groups on the basis of the dip exposure formula described above. Exposure groups were (i) no exposure (ii) 1-25,000 units (iii) 25,001-50,000 units (iv) 50,001-75,000 units. There were no significant differences in mean global GHQ or CFS scores (F = 0.69, p = 0.55 and F = 0.11, p = 0.95 respectively) or in any test sub-scale score between the four exposure groups, after adjustment for covariates of stressful life events and age. There was also no significant difference in the percentage of respondents from each exposure group who qualified for psychiatric caseness or severe fatigue (Chi-square = 6.02, p = 0.11 and Chi-square = 0.41, p = 0.93 respectively). However, mean global GHQ and CFS scores were above the caseness thresholds (a score severe enough to warrant clinical intervention if presented to a General Practitioner) for all exposure groups except the no exposure group, and this may be perceived as a positive exposure-response effect, all be it at a gross level. However, as shown in Table 2, chi-square analysis showed no association between psychiatric caseness on the GHQ and those who ever/never used OP dips (p = 0.43) or severe fatigue on the CFS scale and those who ever/never used OP dips (p = 0.89).

Because exposure estimates were based on flock sizes and the frequency of dipping sessions per year, it must be remembered that a range of effects could be expected to be produced by OP dips with different mechanisms of action and toxic potencies. Results suggested that farmers were often not aware of which OP dips they recently used or had used in the past. The OPs recently used by respondents to Phase II were as follows: Diazinon (40.2%), Propetamphos (36.1%), Chlorfenvinphos (1.6%), with 22.1% unsure of their most recently used product.

Objective 2

In order to determine the important contributors to mental health and fatigue symptoms in the farmers a number of factors were assessed. These could be broadly categorised as demographic factors, individual differences in personality (risk taking) and health (medication use), stressful life events, life satisfaction and specific aspects of exposure relating to the way the dipping process was carried out. These were used as independent predictor variables in stepwise regressions to predict mental health and fatigue states, with global GHQ and CFS scores as the to-be-predicted variables. Potential predictors were classified as features related to (i) dipping work, (ii) PPE use, (iii) dip bath details, or (iv) individual psychosocial differences; and a full list of the 38 factors investigated is presented in Table 3, along with respective correlations with GHQ and CFS scores.

* levels of ordinal variables arranged in increasing (anecdotal / traditional) association with ill-effects.

The stepwise regressions showed three variables to be significant in the prediction of GHQ likert scores, (life events score, agricultural satisfaction, and handling sheep within 48 hours of dipping) and 2 variables in the prediction of CFS scores, (presence of dip spray and GHQ score). These are shown in Tables 4a and 4b respectively. These variables were then entered into separate multiple regression models to predict the two outcome variables.

The model predicting likert GHQ scores had the following properties: R = 0.64, R2 = 0.41, Adjusted R2 = 0.41, F = 69.3, p = 0.00, N = 250, and Intercept = 11.81, which was expressed thus:
GHQ = 11.81 + ( .45xLEI ) + ( - .33xSAL ) + ( .13xH )
Where:
LEI denotes LEI severity score (ordinal value).
SAL denotes satisfaction with agricultural lifestyle score (ordinal value).
H denotes handling sheep within 48 hours of dipping (1 = Yes, 0 = No).

The model predicting likert CFS scores had the following properties: R = 0.67, R2 = 0.45, Adjusted R2 = 0.45, F = 121.3, p = 0.00, N = 250, and Intercept = 10.57, which was expressed thus:
CFS = 10.57 + ( .16xDS ) + ( .61xGHQ )
Where:
DS denotes dip spray rising from the surface (1 = Yes, 0 = No).
GHQ denotes likert GHQ score (ordinal value).

Discussion

All the farmers in this sample reported high levels of mental distress and severe fatigue. This is in keeping with other data indicating that farmers in general, at least in the UK, are at high risk of mental health problems. In addition it should be noted that the study was carried out during a period of agricultural recession, economic hardship and general dissent amongst the rural community in Britain. The Spring of 1998, when the data were collected, was marked by large protest marches over issues as diverse as the lack of facilities in rural villages, the banning of field sports and the burden of increasingly complex financial regulations. In terms of this investigation the influence of these factors was possibly twofold. First they may have produced a reluctance to participate because of a preoccupation with other matters and an unwillingness to become involved in more paperwork. Secondly, the sources of mental distress other than neurotoxic exposure (OPs) were likely to be considerably magnified relative to a few years earlier.

The low overall response rate of just over 23% in Phase I reduced to 13% in Phase II is an obvious cause for concern and reduces the generalisability of the results. Self-selection into the study may result in the over-estimation of some effects, either because the self-selected group represented a subset of individuals suffering from extreme health effects, or because the group had (psychosocial) reasons for symptom exaggeration. Both may have occurred in the current study.

There was some evidence that farmers with exposure to OP dips had poorer mental health and more severe fatigue than those without such exposure. These effects were not very marked and only weakly related to degree of exposure. However, a trend concerning increased exposure and symptomology was suggested by the data, in that the lowest symptom scores for both mental health and fatigue were observed in the non-exposed farmers, and the most symptomatic scores were observed in those farmers with the greatest estimated exposure. In addition, all exposure groups except the no-exposure group had mental health and fatigue scores above clinical caseness thresholds, although definitive association between some exposure / no exposure and clinical caseness of mental health or fatigue status was present.

Self-rated ill health was significantly associated with past exposure, although caution must be used in the interpretation of such findings on two levels. First, self-rating of health was a subjective rating, and second, there is a possibility that some farmers may have been mistaken in their ratings of whether they had ever dipped with OPs before. This seems more likely, in that 20% of phase II respondents did not know if their most recent dip of choice was OP based or not. Logistic regression to predict self-rated ill health revealed the importance of spray from the dip on a windy day, with results suggesting farmers reporting such spray were almost three-times more likely to described themselves as being ill. Odds ratios for the other factors in the regression were unchanged. This poses a difficulty in the interpretation of this finding - was dip spray a genuine increased exposure which may account for increased self-ratings of ill health, or was there a perceptual attribution process where excess spray convinced dippers they may have had some excessive exposure. The data suggest therefore that while OP exposure may have had a role to play in mental health and fatigue problems reported by farmers, other factors were likely to be of equal importance. A biopsychosocial model is able to explain why the UK dippers showed such symptomology.

Farmers were exposed to chemicals they knew to be hazardous and associated with dreaded consequences. However, there remained much uncertainty about the effects of dipping with OPs in the scientific community, with many farmers tending to err on the side of caution. The relative isolation of farmers in both their working and social lives may have led to increases in their internal focus, with reduced opportunities to compare their concerns with other farmers. The on-going agricultural recession and mistrust of Government would have done nothing to reduce levels of anxiety or depression within farming communities. In addition, the popular consumer backlash against chemicals and intensive farming methods, and the general environmental concern of the public may have caused farmers to feel vilified, or express conflict between their personal economic and social concerns. Essentially, the legal requirement of compulsory dipping mean that an involuntary risk was present, along with the opportunity to attribute blame elsewhere.

Mental health amongst those exposed to OPs was best predicted by a model accounting for 41% of the variance in mental health scores, including the factors of personality type, recent stressful life events, satisfaction with the agricultural life and handling sheep within 48 hours of dipping. Fatigue was best predicted with a model accounting for only 45% of the variance in fatigue scores, which was comprised of two factors: dip spray rising from the bath, and mental health (GHQ score). Both predictive models therefore used a combination of individual factors and work-processes to predict the separate outcome measures of mental health and fatigue. Both models were seemingly intuitive, in that they predicted poorer mental health and fatigue when the values of individual variables used in the models mimicked those traditionally associated with poorer outcomes: such as increased severity of stressful events or lifestyle dissatisfaction.

The mental health model in particular provides support for a biopsychosocial approach to the explanation of the mental health problems in these farmers. As a group they are not only exposed to a potentially hazardous neurotoxicant but are also experiencing a range of psychosocial influences likely to modify their response to this exposure. The explanation of their symptoms does not necessarily therefore require a decision about whether this is a "physical" or a "psychological" problem but can encompass the contribution of both elements. The fatigue model is perhaps less clear and contains only two significant predictor variables (an exposure variable - dip spray, and an individual variable - mental health). The inclusion of severe fatigue as an outcome measure is perhaps itself questionable since its status as a psychologically or physically based illness remains controversial.

Despite the relatively low numbers of participants in this study the results provide some support for the biopsychosocial approach as a means of understanding the problems of those who attribute their ill-health to occupational or environmental hazard exposure. Sheep farmers provide an example of a group of workers who encounter exposure to a known neurotoxicant (but often at a level where toxicological effects would not be expected to occur) who are also exposed to a number of lifestyle features (psychosocial hazards) such as isolation, financial pressures, and uncertainty, which may account for increased levels of psychological problems. Groups such as these may often report symptoms which are not readily explicable in terms of organic factors and cannot be linked to any discernible toxicological mechanism. In terms of the understanding and management of these problems both at an individual level and in terms of occupational health policy it would seem more productive to adopt a biopsychosocial position than to continue what is often a sterile debate about whether their illness is physically or psychologically based. The implication of this approach however is that management of the problem is likely to be multifaceted, requiring that both exposure factors (in this case aspects of the dipping process) and psychosocial and attitudinal factors be addressed. Research has suggested that agricultural workers do want occupational health provision (Booth et al. 2000 and Gerrard 1998), and would be willing to use such services (Clerk & Lester, 1989). In the UK and elsewhere, rural and agricultural community health teams, often with a specific focus and remit to work with isolated members of farming communities, would appear to be well-placed to tackle these problems and to adopt a broader perspective than one which attempts to identify a single cause.

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