Position statement - Pesticides and cancer

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Key messages

  • The term 'pesticides' describes hundreds of synthetic and naturally occurring chemicals (i.e. those produced by plants) designed or naturally produced to deter insects and other agricultural pests. The wide-ranging variety of synthetic and naturally occurring chemical pesticides makes it difficult to accurately assess their potential to cause cancer in humans.
  • Studies examining cancer risk from exposure to specific pesticides have been limited by the small numbers of study subjects; conclusive evidence of risk has to date been impossible to establish.
  • The wide range of chemicals used in pesticides, and exposure to other possible carcinogens in workers who may also use pesticides, make it impossible to currently establish direct links between pesticides used in Australia and cancer.
  • Two chemicals used as pesticides – arsenic and ethylene oxide – are among agents rated as Group 1 carcinogens, or conclusive causes of cancer, by the International Agency for Research on Cancer (IARC), as is the chemical 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), which may occur as a contaminant in certain pesticides.
  • Arsenic and arsenic compounds are no longer used in pesticides in Australia; ethylene oxide is used in three pesticides licensed for use in Australia until July 2012. Many other pesticides have been reviewed by IARC but there is insufficient evidence to establish them as conclusive or probable causes of cancer in humans.
  • Studies have shown a possible association between cancer and occupational exposure to four pesticide chemicals: metolachlor, pendimethalin, permethrin and trifluralin. Further research is recommended.
  • The use of household pesticides, such as insecticides, can expose people to pesticide residues in the home. However, there is no clear evidence linking household pesticide use in Australia with cancer.
  • Meta-analyses (i.e. analyses of multiple international studies) have shown an association between women exposed to insecticides in pregnancy and an increased risk of leukaemia in their children. These studies were limited; causation could not be confirmed. More and better quality research is required into a possible link between antenatal exposure to insecticides and childhood leukaemia.
  • There is no evidence that pesticide residues on food consumed in Australia cause cancer. (Coincidentally, consumption of foods most commonly associated with pesticide use – fresh vegetables and fruit – can help to prevent cancer.)
  • The level of pesticide residue on foods sold in Australia is regularly monitored by government agencies to help ensure levels stay well within agreed safety limits.
  • Overall, there is no conclusive evidence linking cancer incidence or mortality with pesticides currently used in Australia. However, the evidence is limited due to the reasons outlined above, so it is impossible to also conclude there is no link between pesticide exposure and cancer.

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Overview

Pesticides are widely used in agriculture, other workplaces and households. Some chemicals used in pesticides have been linked to cancer through laboratory and epidemiological research. However, there is no conclusive evidence linking pesticide use in general with cancer.

The wide range of chemicals used in pesticides, and possible co-factors leading to cancer in people exposed to pesticides, make it impossible to establish direct links between pesticides used in Australia and cancer. However, there is also insufficient evidence to conclusively show there is no link between pesticide exposure, either through direct chemical or residual contact, and cancer.

This position statement provides an overview of the evidence on the carcinogenic potential of occupational, dietary and residual/environmental exposure to pesticides.

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Specific pesticide components

The term “pesticides” includes hundreds of individual chemicals; exposure therefore describes contact with a wide range of products.

Determining which particular pesticide chemicals account for a specific health effect is difficult. Cell and rodent experiments can provide some indication of potential hazards in humans, but their results are not always applicable. For example, the IARC originally classified the herbicide atrazine as a possible human carcinogen (Group 2B) on the basis of rat experiments. However, the mechanisms turned out to be irrelevant to humans, the chemical was downgraded to Group 3 (unclassifiable)[1] and later epidemiological studies showed no link between atrazine and cancer[2][3]. This highlights the need for epidemiological evidence in humans in addition to cell and animal experiments.

Arsenic compounds are a known cause of lung cancer and have been classed as Group 1 carcinogens[4], meaning that they have conclusively been shown to cause cancer in humans, by the IARC (see Appendix 1). Classification was based on studies involving workers in sectors other than agriculture who were exposed to arsenic-contaminated water.

Ethylene oxide is classed within Group 1[4] and is licensed as an ingredient in five fumigant products, at least until July 2013[5]. Aside from these clear exceptions, no specific pesticide has been conclusively linked to a specific cancer, and suggested links do not group by class or type of pesticide.

The IARC has also classified the “spraying and application of non-arsenical insecticides” as a probable cause of cancer[6]. However, only two specific pesticides – captafol and ethylene dibromide– are classed within this category. Neither of these are used in Australia. Several pesticides have been classed as possible causes of cancer (Group 2B). Phenoxy herbicides, chlorothalonil, dichlorvos, and sodium ortho-phenylphenate are licensed for agricultural use, although some are under review. Para-dichlorobenzene is not used as an agricultural pesticide, but is used in mothballs and urinal cakes. Other pesticides in this category are banned in Australia (see Appendix 1).

The US Agricultural Health Study is the largest prospective study to assess the link between pesticide exposure and cancer. It recruited more than 57,000 pesticide applicators (mostly male) and 32,000 spouses of applicators (mostly female). In 2010, a review of the study’s 28 publications found that 19 out of 32 pesticides were associated with at least one type of cancer, including lung, pancreatic, bowel (colon and rectal), prostate, brain and bladder cancer, melanoma, leukaemia, non-Hodgkin lymphoma and multiple myeloma[7]. However, for most of these pesticides the “highest exposure” categories included fewer than 12 cases, meaning little could be concluded regarding the causal nature of these associations on the available evidence[7]. Further research is required.

Of the 19 pesticides associated with cancer, six were singled out for future investigation based on corresponding animal toxicity data. Of these six, alachlor is not permitted for use in Australia; carbaryl is under review, and metolachlor, pendimethalin, permethrin and trifluralin are in use. The IARC has classified permethrin and trifluralin as Group 3 (inadequate evidence)[6], but has not evaluated metolachlor and pendimethalin. The US Environmental Protection Agency describes permethrin as a “likely” carcinogen and the other five as “possible” carcinogens[8].

Outside the Agricultural Health Study, a small number of studies have assessed cancer risk according to exposure of individual pesticides. Some results are reviewed in Weichenthal et al[7], however a full systematic analysis is beyond the scope of this position statement. Many of these studies suffer from similar weaknesses[9] – exposure to pesticides is generally measured through self-reports, which makes studies vulnerable to recall bias. Validation analyses show that self-reporting provides a reasonable measure of the highest and lowest exposure levels, but is less effective at quantifying moderate exposures. Furthermore, pesticide exposure varies significantly between occupations. It can also be intense during certain tasks but cumulatively low, since those tasks are performed only on a few days a year and often vary over the years as pesticide types and application methods change. Farmers and family members may have additional exposure from inadvertent contact, but such “bystander exposure” is difficult to measure.

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Occupational pesticide exposure

A number of international studies have found higher incidence and mortality rates from specific cancers among people occupationally exposed to pesticides, including farmers and pesticide applicators[7], pesticide manufacturing workers[10][11], golf course superintendents[12] and market gardeners or orchardists[13]. There is, however, no increase in the incidence or mortality of these cancers among pest control workers (e.g. exterminators)[14].

Meta-analyses (compilations of multiple studies) have reported higher than average levels of various cancers among farmers and pesticide applicators (see Blair and Freeman for a review[9]). These include non-Hodgkin lymphoma[15][16][17][18], leukaemia[10][11][19], multiple myeloma[20], brain cancer[21], prostate cancer[22][23][24], lip cancer[9] and skin cancer[9]. However, most of the associations were relatively weak, with occupational exposures attributable for a 10-40% increase in risk, depending on cancer type. Exceptions include: two meta-analyses which found a two-fold higher risk of lip cancer among farmers[9]; and a meta-analysis that found a two-fold higher risk of leukaemia among pesticide applicators (employees applying pesticides) and a six-fold higher risk among pesticide manufacturing workers[16].

It is not clear if pesticides are attributable for these elevated incidence rates, because workers in these sectors are also exposed to a range of other potential carcinogens. For example, agricultural workers are regularly exposed to diesel exhaust, solvents, metals, grain dusts, zoonotic (transmissible from animals to humans) viruses and ultraviolet radiation, all of which could confound the relationship between pesticides and cancer[25].

In addition, a study in Western Australia found that 78% of farm jobs have “no likelihood of pesticide exposure”[26]. The study noted “classification of all farm jobs as pesticide-exposed is likely to substantially over-estimate the number of individuals exposed”[26].

The time lag between environmental exposures and the development of some cancers may make it difficult to draw conclusions about current workplace exposures. This time lag also means it is difficult to study new pesticides, as associated cancers may occur many years after their introduction. For example, agricultural workers could develop cancers through exposure to arsenic and arsenic compounds used in pesticides many years ago but no longer permitted in Australia.

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Exposure to pesticides in the home

Exposure to pesticides in the home includes professional applications (e.g. professional fumigation and other pest control services), the use of household sprays and other retail pesticides, and chemicals brought into the home from workplaces[27].

Pesticides can persist indoors from carpets, where they are protected from environmental degradation; such residues can be measured in samples of carpet dust[28][29]. Children may experience greater exposure and adverse reactions to such pesticide residues, because their concentration is higher closer to the floor[27] and a child’s metabolism builds up different levels of toxic metabolites to that of adults[30].

A number of studies have assessed the risk of various cancers among both adults and children following residential pesticide exposure. There have been positive results from isolated, small studies for prostate cancer[31], neuroblastoma[32] and childhood brain tumours[33]; inconsistent evidence for breast cancer[34][35][36][37] and non-Hodgkin lymphoma[38][39][40]; and no strong evidence for Wilms' tumour[41][42] or germ cell tumours[43].

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Exposure to pesticides through diet

Pesticides are sprayed on crops and thus may end up in the human body through diet. Food Standards Australia New Zealand and the Australian Pesticides and Veterinary Medicines Authority monitor levels of pesticide residue in Australian foods to ensure they remain within approved food safety levels. These agencies determine an Acceptable Daily Intake (ADI) for each chemical, which reflects the amount “that can be ingested daily over a lifetime without appreciable risk to health”.

The 20th Australian Total Diet Survey, conducted in 2003 (the most recent survey), screened 65 types of food for pesticide residues, including chlorinated organic pesticides, organophosphorus pesticides, synthetic pyrethroids, carbamates and fungicides. The survey report concluded that “the levels of pesticide residues... in our food are very low, and in all cases they are within acceptable safety limits”[44].

For most pesticides of concern, Australians are exposed to less than 0.2% of the ADI through their diet[44]. The report recommended that pesticide residue monitoring should be undertaken less frequently, although it should also be expanded to focus on chemicals beyond those registered for use in Australia (given the importation of certain foodstuffs)[44].

Analysis shows the effect of dietary synthetic pesticides on cancer would be minimal, given the tiny proportion of synthetic pesticides ingested compared with those naturally produced by plants to deter insects and other animals[45]. It is estimated that more than 99% of the pesticides we eat are naturally occurring, yet around 60% of both synthetic and natural pesticides have been shown to cause cancer in rodent tests[45].

There is also no evidence that eating foods most likely to contain pesticide residues[44] – i.e. fruit, vegetables and cereals – increases cancer risk. On the contrary, evidence shows that eating such foods can reduce cancer risk[45][46].

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Environmental pesticide exposure

People can be exposed to pesticides that seep into the water supply or food chain, persisting for a long time in the environment. The persistent, residual nature of such compounds enables them to be measured in the human body in blood and breast milk.

Some of these chemicals, such as organochlorine pesticides, have been shown to be endocrine disruptors with the ability to mimic or block natural hormones like oestrogen and testosterone. These properties have been hypothesised to increase the risk of hormonal cancers such as breast or prostate cancers, although there is not enough evidence to support a causal link[47][48].

As a case study, the organochlorine DDT has been extensively studied as a risk factor for breast cancer. It is now banned in Australia and other parts of the world, but in the 1940s and 1950, it was heavily used as an insecticide. The IARC classifies DDT in Group 2B (possible carcinogen) after three rounds of evaluation, in 1974, 1987 and 1991[6][49][50]. Most epidemiological studies[51], including the Long Island nested case-control study[52], do not support a conclusive link between DDT and cancer although there is some evidence that exposure in early life or adolescence could increase the longer-term risk of breast cancer[53]. Epidemiological studies have similarly not supported a link between organochlorine pesticides in general and breast cancer[54].

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Childhood cancer and parental exposure to pesticides

There is some evidence that parental exposure to pesticides could increase the risk of cancer in the next generation. A 2011 meta-analysis considered 40 studies and concluded that maternal occupational pesticide exposure before birth is associated with a 48% increased risk of childhood leukaemia and a 53% increased risk of lymphoma, while paternal exposure before or after birth was associated with a 49% higher risk of brain cancer[55].

Two other meta-analyses found that maternal occupational pesticide exposure before birth was associated with a 62% and 109% higher risk of childhood leukaemia risk respectively[56][57]. Neither study found an association between paternal exposure and childhood leukaemia[56][57].

One meta-analysis of 15 case-control studies concluded that residential exposure to pesticides during pregnancy increased the risk of childhood leukaemia by 54%[58]. The association was especially strong for insecticides – a doubling of risk – and it remained significant after stratifying for high-quality studies with the most accurate exposure measurements and adjustment to confounding factors. Another meta-analysis of 13 studies concluded that residential pesticide exposure was linked to a 74% higher risk of childhood leukaemia, with the strongest risk for exposure during pregnancy (2.2-fold) and insecticide exposure (73%)[57].

Recent studies have suggested that parental exposure to pesticides may also be associated with brain cancer. In 2013, a meta-analysis of 20 studies from 1974 to 2010 supported an association between parental occupational exposure to pesticides and brain tumours in children and young adults[59].

A 2011 meta-analysis has suggested that paternal exposure to pesticides either before or after birth increases the risk of brain cancer in children by 50-65%[55]. The study found no evidence to suggest that maternal exposure to pesticides before or after birth was associated with an increased risk of brain cancer[55].

An Australian case-control study also published in 2013 suggested that preconception pesticide exposure, and possibly exposure during pregnancy, is associated with an increased risk of childhood brain tumour[60].

All studies analysed to 2010 were susceptible to various forms of reporting bias[61]. For example, the studies were case-control – i.e. based on data on exposure levels provided by individuals with a specific cancer compared to individuals without that cancer. Self-reported data on previous exposures is often unreliable, particularly when derived from people with a cancer that they think may be linked to a possible cause (this is known as “recall bias”).

Most studies used small sample sizes and were unable to single out any specific pesticide of concern. Van Maele-Fabry et al. concluded that “data were too scarce” to assert a causal link between residential pesticide exposure and leukaemia[57]. They called for more studies on interactions between genetic predisposition in individuals and environmental exposures, while suggesting “it may be opportune to consider preventive actions including educational measures to increase the awareness of the public and particularly of pregnant women about the potential adverse influence of pesticides on children’s health”[57].

Moreover, variations in the size, quality and consistency (e.g. of data sets) of studies made it difficult to draw conclusions. However, while the limitations and flaws of these studies weakened the overall evidence, there was still an association between residential pesticides and leukaemia[57][58].

It should be noted that association indicates a possible link and is not conclusive evidence of causation.

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Appendix 1. Overview of pesticide carcinogenicity classifications

The IARC has classified various pesticides according to their carcinogenic potential (see Siemiatycki et al.[62] for a full list). The full list of agents classified by the IARC Monographs is available on the IARC website.


Table 1. Pesticide carcinogenicity classifications and licensing in Australia

IARC group Pesticide Human evidence Animal evidence Use in Australia
Group 1 (carcinogenic in humans) Arsenic and arsenic compounds Sufficient (lung, skin, liver) - No longer used as crop insecticide. Use of arsenic trioxide as a wood preservative is allowed if treated wood is covered after application; use of copper chrome arsenic for the same purpose has been heavily restricted since 2005
Ethylene oxide Limited (leukaemia) Sufficient Licensed as an ingredient in five fumigant products, until July 2013
TCDD Limited (cancer overall) Sufficient Not specifically used as a pesticide, but sometimes found as a contaminant in chlorophenoxy herbicides
Group 2A (probably carcinogenic in humans) Spraying and application of nonarsenical insecticides Limited (strongest evidence for lung cancer; weaker for brain, leukaemia, non-Hodgkin lymphoma, multiple myeloma) Not available -
Ethylene dibromide Inadequate Sufficient Not permitted for use as a pesticide in Australia since 1998
Captafol Not available Sufficient No countries allow use of captafol
Group 2B (possibly carcinogenic in humans) Aramite
Chlordane
Chlordecone
Chlorophenoxy herbicdes
Chlorothalonil
DDT

1,2-Dibromo-3-chloropropane (DBCP)
para-Dichlorobenzene
Dichlorvos
Hexachlorobenzene
Hexachlorocyclohexanes (including Lindane)
Mirex
Nitrofen
Sodium ortho-phenylphenate
Toxaphene (polychlorinated camphenes)

Limited for chlorophenoxy herbicides; inadequate or unavailable for all others Inadequate for chlorophenoxy herbicides; sufficient for all others Chlordane, chlordecone, DDT, hexachlorobenzene, hexachlorocyclohexanes, mirex, nitrofen, toxaphene, are all banned. Aramite and DCBP are not used in Australia.

Phenoxy herbicides are licensed for use, although some specific chemicals such as 2,4-D are under review.

Chlorothalonil and dichlorvos (recently reviewed) are licensed.

Sodium ortho-phenylphenate is used to disinfect citrus fruits.

Para-dichlorobenzene is not used as an agricultural pesticide but in mothballs and urinal cakes.


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References

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