Animal poisoning in Europe. Part 1: Farm livestock and poultry

6
Review Animal poisoning in Europe. Part 1: Farm livestock and poultry Raimon Guitart a , Siska Croubels b , Francesca Caloni c, * , Magda Sachana d , Franca Davanzo e , Virginie Vandenbroucke b , Philippe Berny f a Unit of Toxicology, Faculty of Veterinary Science, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain b Department of Pharmacology, Toxicology and Biochemistry, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium c Department of Veterinary Sciences and Technologies for Food Safety, Faculty of Veterinary Medicine, University of Milan, Via Celoria 10, 20133 Milan, Italy d Laboratory of Biochemistry and Toxicology, School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece e Centro Antiveleni di Milano, Ospedale Niguarda Cà Granda, Piazza Ospedale Maggiore 3, 20162 Milan, Italy f Pharmacie-Toxicologie, Ecole Nationale Vétérinaire de Lyon, 1 av. Bourgelat, 69280 Marcy l’Étoile, France article info Article history: Accepted 4 March 2009 Available online xxxx Keywords: Toxicoepidemiology Food animals Natural Toxins Heavy metals Dioxins abstract The lack of a reference Veterinary Poison Control Centre for the European Union (EU) means that clini- cians find it difficult to obtain information on poisoning episodes. This three-part review collates pub- lished and unpublished data obtained from Belgium, France, Greece, Italy and Spain over the last decade in order to provide a broader toxicoepidemiological perspective. The first article critically evalu- ates the national situation in the five European countries and concludes that information for livestock and poultry is limited and fragmentary compared to other animal groups. The analysis has revealed that clin- ical cases of poisoning are only occasionally studied in depth and that cattle are the species most fre- quently reported. Several plants and mycotoxins, a few pesticides and metals, together with contaminants of industrial origin, such as dioxins, are responsible for most of the recorded cases. Ó 2009 Elsevier Ltd. All rights reserved. Introduction Poisoning appears to be an uncommon cause of illness in ani- mals compared to other clinical problems such as infectious dis- eases, trauma or neoplasia. One reason for this may be a lack of information on the most common toxicants affecting the veteri- nary species so consequently there is little information available to guide and facilitate diagnosis. The European Union (EU) has no Veterinary Poison Control Centre to centralise and publish infor- mation on poisoning, and even in individual nations the data are often managed by several different institutions, mainly Faculties of Veterinary Medicine or Science, and frequently only with a re- stricted area of coverage. This leads to poor and limited dissemina- tion of toxicoepidemiological data, with little or no availability to veterinarians in other regions or countries. In an endeavour to provide relevant facts and figures, scientists from five European countries (Belgium, France, Greece, Italy and Spain) have participated in this review. It covers (but is not re- stricted to) the period 1998–2007, which we considered would be long enough to obtain data useful for veterinary clinicians work- ing in these (and other) European countries. We made an effort to include not only information published in peer-reviewed journals, but also that from other sources, such as more restricted national or local journals, generally unavailable reports and unpublished data from laboratories, institutions or universities. Raw data were not available, except partially for France, so statistical analysis could not be performed. It should be noted that most published cases of poisoning refer to special and/or unusual cases, since com- mon causes of poisoning are rarely published and reliable and complete toxicoepidemiologic data are not easy to obtain. A further difficulty with investigating causes of animal poison- ing is that neither the veterinarian nor the animal owner are ob- liged to report the case nor to send samples for chemical analysis. Even when this does occur, the results are usually not published (even in annual reports) and there are really only spo- radic peer-reviewed papers dealing with regional incidences of animal poisoning. This limited reporting obscures the incidence of accidental or malicious poisoning, particularly when only a lim- ited number of samples from the total number of animals involved, or only the baits used in poisoning attempts, are sent for analysis and the results recorded. Furthermore, only a few possible toxi- cants can be investigated in the designated laboratories, so that new chemicals are often not detected and, consequently, the real number of positive cases may be underestimated. This review consists of three separate articles, each dealing with a different animal group. In this first section, poisoning in livestock and poultry are reported. The other articles cover companion ani- mals and horses (Berny et al., 2009) and wildlife (Guitart et al., 2009). 1090-0233/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tvjl.2009.03.002 * Corresponding author. Tel./fax: +39 02 50317884. E-mail address: [email protected] (F. Caloni). The Veterinary Journal xxx (2009) xxx–xxx Contents lists available at ScienceDirect The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl ARTICLE IN PRESS Please cite this article in press as: Guitart, R., et al. Animal poisoning in Europe. Part 1: Farm livestock and poultry. The Veterinary Journal (2009), doi:10.1016/j.tvjl.2009.03.002

Transcript of Animal poisoning in Europe. Part 1: Farm livestock and poultry

The Veterinary Journal xxx (2009) xxx–xxx

ARTICLE IN PRESS

Contents lists available at ScienceDirect

The Veterinary Journal

journal homepage: www.elsevier .com/ locate/ tv j l

Review

Animal poisoning in Europe. Part 1: Farm livestock and poultry

Raimon Guitart a, Siska Croubels b, Francesca Caloni c,*, Magda Sachana d, Franca Davanzo e,Virginie Vandenbroucke b, Philippe Berny f

a Unit of Toxicology, Faculty of Veterinary Science, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spainb Department of Pharmacology, Toxicology and Biochemistry, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgiumc Department of Veterinary Sciences and Technologies for Food Safety, Faculty of Veterinary Medicine, University of Milan, Via Celoria 10, 20133 Milan, Italyd Laboratory of Biochemistry and Toxicology, School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greecee Centro Antiveleni di Milano, Ospedale Niguarda Cà Granda, Piazza Ospedale Maggiore 3, 20162 Milan, Italyf Pharmacie-Toxicologie, Ecole Nationale Vétérinaire de Lyon, 1 av. Bourgelat, 69280 Marcy l’Étoile, France

a r t i c l e i n f o

Article history:Accepted 4 March 2009Available online xxxx

Keywords:ToxicoepidemiologyFood animalsNatural ToxinsHeavy metalsDioxins

1090-0233/$ - see front matter � 2009 Elsevier Ltd. Adoi:10.1016/j.tvjl.2009.03.002

* Corresponding author. Tel./fax: +39 02 50317884E-mail address: [email protected] (F. Calon

Please cite this article in press as: Guitart, R.,doi:10.1016/j.tvjl.2009.03.002

a b s t r a c t

The lack of a reference Veterinary Poison Control Centre for the European Union (EU) means that clini-cians find it difficult to obtain information on poisoning episodes. This three-part review collates pub-lished and unpublished data obtained from Belgium, France, Greece, Italy and Spain over the lastdecade in order to provide a broader toxicoepidemiological perspective. The first article critically evalu-ates the national situation in the five European countries and concludes that information for livestock andpoultry is limited and fragmentary compared to other animal groups. The analysis has revealed that clin-ical cases of poisoning are only occasionally studied in depth and that cattle are the species most fre-quently reported. Several plants and mycotoxins, a few pesticides and metals, together withcontaminants of industrial origin, such as dioxins, are responsible for most of the recorded cases.

� 2009 Elsevier Ltd. All rights reserved.

Introduction

Poisoning appears to be an uncommon cause of illness in ani-mals compared to other clinical problems such as infectious dis-eases, trauma or neoplasia. One reason for this may be a lack ofinformation on the most common toxicants affecting the veteri-nary species so consequently there is little information availableto guide and facilitate diagnosis. The European Union (EU) has noVeterinary Poison Control Centre to centralise and publish infor-mation on poisoning, and even in individual nations the data areoften managed by several different institutions, mainly Facultiesof Veterinary Medicine or Science, and frequently only with a re-stricted area of coverage. This leads to poor and limited dissemina-tion of toxicoepidemiological data, with little or no availability toveterinarians in other regions or countries.

In an endeavour to provide relevant facts and figures, scientistsfrom five European countries (Belgium, France, Greece, Italy andSpain) have participated in this review. It covers (but is not re-stricted to) the period 1998–2007, which we considered wouldbe long enough to obtain data useful for veterinary clinicians work-ing in these (and other) European countries. We made an effort toinclude not only information published in peer-reviewed journals,but also that from other sources, such as more restricted national

ll rights reserved.

.i).

et al. Animal poisoning in Eu

or local journals, generally unavailable reports and unpublisheddata from laboratories, institutions or universities. Raw data werenot available, except partially for France, so statistical analysiscould not be performed. It should be noted that most publishedcases of poisoning refer to special and/or unusual cases, since com-mon causes of poisoning are rarely published and reliable andcomplete toxicoepidemiologic data are not easy to obtain.

A further difficulty with investigating causes of animal poison-ing is that neither the veterinarian nor the animal owner are ob-liged to report the case nor to send samples for chemicalanalysis. Even when this does occur, the results are usually notpublished (even in annual reports) and there are really only spo-radic peer-reviewed papers dealing with regional incidences ofanimal poisoning. This limited reporting obscures the incidenceof accidental or malicious poisoning, particularly when only a lim-ited number of samples from the total number of animals involved,or only the baits used in poisoning attempts, are sent for analysisand the results recorded. Furthermore, only a few possible toxi-cants can be investigated in the designated laboratories, so thatnew chemicals are often not detected and, consequently, the realnumber of positive cases may be underestimated.

This review consists of three separate articles, each dealing witha different animal group. In this first section, poisoning in livestockand poultry are reported. The other articles cover companion ani-mals and horses (Berny et al., 2009) and wildlife (Guitart et al.,2009).

rope. Part 1: Farm livestock and poultry. The Veterinary Journal (2009),

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General overview

Table 1 summarises the most recent census available of farmlivestock and poultry in the five EU countries considered. As canbe seen, food-producing animals were well represented.

Poisoning is seldom recorded in food-producing animals inFrance or Belgium, probably as it is usually only suspected afterexclusion of common pathological disorders. Furthermore, poison-ing in livestock is often only addressed when the economic loss issufficient to justify immediate investigation. For instance, very fewcases are reported in goats and sheep, which are of low economicvalue. Also, many species (poultry, swine) are kept in a confinedenvironment, which precludes exposure to toxicants and, conse-quently, poisoning is unlikely to occur.

Sheep and goats are rarely housed in Greece during the springand summer months, and are therefore more vulnerable to acci-dental poisoning, especially by pesticides and metals. Housingand feeding with supplements are more frequent for bovines, pigsand poultry, although some small ruminants are housed, particu-larly in winter. Most studies related to food-animal poisonings fo-cus on small ruminants but the poultry industry is also affectedand cases involving the death of a significant number of birds havebeen reported in the last decade in Northern Greece.

In Italy, information on the poisoning of food-producing ani-mals is scarce. The Centro Antiveleni di Milano (CAV) reported alow percentage of poisoning in bovines (1.2%), compared to the to-tal number of animal poisoning episodes (Caloni et al., 2003); an-other investigation from the University of Pisa noted that only0.5% of bovine cases included a request for analysis (Giorgi et al.,2002). Even less information is available for other species, suchas pigs and poultry.

There are comparatively few poisoning records for livestock inSpain. For example, at the Servicio de Atención Toxicológica Vete-rinaria (SATVe) in Lugo, Galicia, a region mainly dedicated to farmactivities and with a population of over 1 million cows (MAPA,2006), cattle-related consultations represented only a minor frac-tion of the total incoming calls (Pérez-López et al., 2004). Theauthors ascribed this to the limited attention that veterinary prac-titioners and owners pay to large animal toxicology problems.

Species involved

At the Laboratory of Toxicology of the Ghent University (LTGU)in Belgium, cattle represent about 18% of the cases presentedannually, with sheep and goats 4% and 1%, respectively. In France,cattle are the most common species exposed to toxicants, account-ing for about 7% of the 70,000 calls received at the Centre Nationald’Informations Toxicologiques Vétérinaires (CNITV) from 1990 to1998 (Royer and Buronfosse, 1998). Sheep only represented 1.4%

Table 1Census of farm livestock and poultry in five EU countries. The values reported areexpressed in millions.

Belgiuma Franceb Greecec Italyd Spaine

Cattle 2 18 0.88 6 6.46Sheep 0.15 8 8.83 6.8 22.9Goats 0.03 1 5.57 0.92 2.84Buffaloes – – 0.0015 0.18 –Pigs 6 14 1.99 8.6 24.9Poultry 32 200 65.10 171 180

a FPS Economy, SMEs, Self-Employed and Energy, Statistics Belgium Division(2006).

b Agreste-Ministère de l’Agriculture et de la Pêche (2007).c Agriculture-Livestock Census 2007 (C. Mprozos, personal communication).d ISTAT (2000).e MAPA (2006).

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and goats <1% of all the calls. All other domestic farm species wererarely involved in the cases recorded by the animal poison controlcentre. In recent years, the total number of calls received for cattledecreased to 5.4% (Barbier, 2005). At the toxicology laboratory, cat-tle represented 5.5% of the cases received, sheep 2.0%, poultry 1.6%and all other food-producing animals accounted for <0.5% each(Berny, 2003).

Most poisoning episodes in Greece are related to small rumi-nants and poultry. Sheep have a higher exposure to toxic sub-stances (32.7%) than goats (23.0%) (Antoniou et al., 2005),possibly related to differences in feeding habits as sheep grazeand are therefore more likely to consume soil contaminated withhigh levels of toxins than are goats that mainly eat leaves takenfrom trees or bushes.

In a previous Italian study (Caloni et al., 2003), the sub-class‘other species’ (1.4%) included horses, pigs, avians, rabbits, ovinesand caprines, showing the scarce information recovered by theCAV on animals other than pets. From 2003 to 2005, out of 323calls, 83.6% related to dogs, 14% to cats, 0.9% to horses and the restcomprised a variety of species, such as goats, ferrets, exotics andporcupines. Bovines were not mentioned. In a study by the Univer-sity of Pisa, it was stated that bovine and equine poisonings wererare (Giorgi et al., 2002).

Data on poisoning episodes in Catalonia may offer a picture ofthe general situation in Spain: after dogs and cats, the greatestnumber of incidents affected birds of prey (9.1%), horses (6.8%),sheep (4.1%), pigeons (4.1%), cattle (2.7%), pigs (2.3%), game birds(quails and partridges; 2.3%), Passeriformes (1.8%), hens (1.4%),freshwater fish (1.4%), and ravens (1.4%), with rabbits, goats, pea-cocks, bees, farm ducks, foxes and other species all <1% (Guitartet al., 1999). Detailed data are however scarce and mostly reflect-ing acute episodes of poisoning in cattle, sheep and poultry.

Most common toxic agents

In Belgium, toxic plants, heavy metals and pesticides are themost common toxicants suspected of being involved in food-ani-mal poisoning. In France and Greece, pesticides are, by far, themost common class of toxicants (Royer and Buronfosse, 1998;Antoniou et al., 2005); in France, mainly insecticides and seed-coatproducts are involved, followed by drugs, plants and nutritionaldisorders (e.g., urea poisoning, grain overload). In Italy, mycotoxinsand toxic plants dominate in cattle and chronic mycotoxicoses area real problem with birds and pigs also affected.

In ruminants in Spain, the most common toxicoses are thoseproduced by plants, fungi and metals. For example, from the dataon cattle obtained from an insurance company covering the wholeSpanish territory from 1996 to 2001, the total number of deathsdue to poisoning was 418, with 275 cases related to outdoor prac-tices (usually linked to meat production) and 143 to indoor sys-tems (for milk) (García-Arroyo et al., 2005). The authors foundthat 12 different plants and fungi were responsible for 90.79%and 72.45% of the cattle deaths in outdoor and indoor systems,respectively, with fern, oak and beet being the most common tox-icants for cattle (Table 2).

Pesticides

At the LTGU, many calls dealt with the possible effects of di-verse pesticides on the health status and performance of animals,mainly cows and horses, particularly when herbicide sprays haddrifted onto neighbouring pastures where cattle grazed. However,toxicological analyses on pesticide poisoning are rarely under-taken, mainly due to the lack of scientific data about toxic levels,metabolism and analytical methods required in the examination

rope. Part 1: Farm livestock and poultry. The Veterinary Journal (2009),

Table 2Toxic plants involved in poisoning episodes in farm livestock and poultry in Europe (see text).

Group or common name Species References

Annual mercury Mercurialis annua Deprez et al. (1996)Beet Beta vulgaris García-Arroyo et al. (2005)Common sorrel Rumex acetosa García-Arroyo et al. (2005)European yew tree Taxus baccata Barbier (2005)Fern Pteridium aquilinum García-Arroyo et al. (2005)Goat’s rue Galega officinalis Bezard et al. (2002)Japanese pieris Pieris japonica Baert et al. (2005)Japanese spindle Euonymus japonicus Baert et al. (2005)Jimson weed Datura stramonium Bofill et al. (2007)Monk’s hood Aconitum napellus Present paper (Italy)Oak (English oak) Quercus spp. Quercus robur García-Arroyo et al. (2005), Barbier (2005), Deroo and de Kruif (2003)Oleander Nerium oleander Langford and Boor (1996)Ragworts and groundsels (Common groundsel) Senecio spp. Senecio vulgaris Vos et al. (2002), Moyano et al. (2006)Rhododendron Rhododendron ponticum This paperViper’s bugloss Echium vulgare Moyano et al. (2006)

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of livestock. In addition, there are no reliable data available for Italyon pesticides and toxicoses.

In 2003, pesticide poisoning represented 33% of the confirmedpoisoning cases in food-producing animals at the animal poisoncontrol centre and over 50% of the cases diagnosed at the toxicol-ogy laboratory in France (Berny, 2003; Barbier, 2005). Until 1998,lindane and endosulfan, two chlorinated hydrocarbons, were themost common causes of poisoning in cattle (especially as coated-seeds). Both products have now been banned or are in very limiteduse as wood preservatives. Snail and slug baits, such as metalde-hyde and methiocarb, represent a common and persistent sourceof poisoning in cattle and sheep (Royer and Buronfosse, 1998).Many suspected cases of herbicide poisoning are received (therewere 82 calls in 2003), but very few are confirmed (only 4 in2003) (Barbier, 2005). Amongst herbicides, only chlorate is regu-larly reported (Sachot and Pouliquen, 1998). Fungicide poisoningis rarely suspected (less than 20 cases in 2003). Ruminants havebeen poisoned by anticoagulant rodenticides, although this is rare(Berny et al., 2006).

A study involving 175 samples analysed between 1998 and2004 in Northern Greece revealed that carbamate insecticides(methomyl, carbofuran, carbaryl, aldicarb and mecarbam) wereresponsible for 46.9% of positive cases in sheep and 66.7% in goats(Antoniou et al., 2005). Organophosphates (methamidophos,terbufos, phorate, parathion-methyl and malathion) accountedfor 15.6% of sheep and 16.7% of goat positive samples. A less com-mon cause (7%) of small ruminant toxicosis involved herbicidessuch as paraquat and atrazin (Antoniou et al., 2005). Two episodeswith high mortality were reported in the poultry industry in thesurrounding area of Thessaloniki (Antoniou et al., 1998); in bothcases, carbamates were found to be the cause of death of 5000 tur-keys and 1500 broilers due to contamination of animal feed andspraying of the barn, respectively.

One of the largest poisoning episodes occurred in Spain when abatch of fungicide-treated feed was given to poultry (Guitart et al.,1996, 1999). Thiram (tetramethylthiuram disulphide) was the fun-gicide involved and approximately 1 million chickens were af-fected: the main findings were soft-shelled eggs, growthdepression and leg abnormalities. Another episode caused thedeath of 3000 young peacocks on a large farm in Catalonia dueto the misuse of pentachlorophenol-treated sawdust (Guitartet al., 1999).

Plants

Livestock can be poisoned by many different plant species (Ta-ble 2) but an analytically confirmed diagnosis is not always easy,

Please cite this article in press as: Guitart, R., et al. Animal poisoning in Eudoi:10.1016/j.tvjl.2009.03.002

and most cases are only suspected following necropsy and identi-fication of leaves, stems or pods in the rumen. For example, thehigh number of negative cases (72.5%) reported in a study of lethalpoisoning in small ruminants in Northern Greece, revealed thatplant toxins probably remained undetected (Antoniou et al., 2005).

It is generally known that fresh and dried brash of the Europeanyew tree (Taxus baccata) contain the cardiotoxic agent taxin, whichoften causes sudden death, especially in horses and cows. On ayearly basis, the Belgian LTGU diagnoses yew tree poisoning in0.31% of all confirmed poisoning cases, and it also appears to bea common cause of plant poisoning in France (Barbier, 2005).

Two cases of annual mercury (Mercurialis annua) poisoning incattle were described in Belgium (Deprez et al., 1996). More re-cently, two cases of intoxication in small ruminants with toxic gar-den plants were also reported (Baert et al., 2005); the first involvedthe death of three goats that ate some garden plants, including Jap-anese pieris (Pieris japonica). In two different, unrelated places inItaly, goats also ingested P. japonica, but they survived. The secondcase in Belgium occurred in a flock of sheep suddenly showing sal-ivation. Five animals died and post-mortem examination revealednumerous leaves of the Japanese spindle (Euonymus japonicus) inthe ruminal content as well as oedematous lungs, haemorrhagicfluid in the trachea, and pleural and peritoneal cavities. The poi-sonous substances of E. japonicus are alkaloids and some are car-diac glycosides or cardenolides.

In 2003, acorn poisoning (Quercus robur) was described in Bel-gium in a 4-month old suckling calf (Deroo and de Kruif, 2003).The toxic syndrome was a gastro-intestinal and renal dysfunctioncaused by gallotannins, polyhydroxyphenolic compounds, or theirmetabolites. Recently, more attention has been paid to the dangersof Senecio spp. in pastures and hay (Vos et al., 2002).

Plant poisoning is commonly reported in cattle and sheep inFrance (Barbier, 2005), with oak trees (Quercus spp.) and Europeanyew being two common poisoning sources. Goat’s rue (Galega offi-cinalis) is regularly reported as a forage contaminant causing sud-den death in sheep and sometimes cattle (Bezard et al., 2002).

CAV (Caloni et al., 2003) collected information related to poi-soning with oleander (Nerium oleander), a highly toxic plant inwhich the cardioactive glycoside (oleandrin, neriin) also persistsafter dissecation (Langford and Boor, 1996). The first case was re-ported in 1990 and involved 50 dairy cows, of which 7 died. Duringthe period 1994–2000, CAV collected one case report of sheep poi-soned in Cortina (North-east Italy) by monk’s hood (Aconitumnapellus), a plant of the Ranunculacae family.

In Spain, there are only two reports of plant poisonings with athorough work-up and analysis. The first one involved a herd of700 Spanish fighting bulls, in which 10 animals died (Moyano

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et al., 2006). The problem was due to the ingestion of the pyrrolizi-dine alkaloid-containing plants Echium vulgare and Senecio vulgarisfrom pastures on the farm in Andalusia. The second reported twoconsecutive poisoning episodes caused by Jimson weed (Daturastramonium) consumption in two different dairy cattle farms (Bofillet al., 2007). In both cases the plant was mistakenly gathered to-gether with corn intended for animal feed.

Mycotoxins

Mycotoxins contaminate cereal grains and other vegetablesworldwide, and their presence in animal feed poses a potentialhealth threat to farm animals (and human consumers). A severeneurotoxicosis, comprising tremors, ataxia, paresis, recumbencyand death, occurred simultaneously amongst several herds of beefcattle in Flanders, Belgium. Aspergillus clavatus was found to be thedominant fungal species in a sample of compacted fodder contain-ing malting residues that was consumed by all affected herds. Mea-surable amounts of verrucologen and patulin could also beidentified in the feed samples involved (Sabater-Vilar et al., 2004).

Although mycotoxicoses are commonly suspected, publishedreports of poisoning are scarce in France. For instance, patulinneurotoxicity is described in some papers, but never confirmedin clinical cases. Despite a very high prevalence of Claviceps spp.fungi in perennial ryegrass, tremorgenic mycotoxins are only re-ported and confirmed in about 10 cases per year in cattle (Gran-cher and Bony, 2003). Other case reports includestachybotriotoxicosis with gastro-enteritis in stables (Guerre,1998), but there are no data with respect to frequency ofoccurrence.

In Italy, mycotoxicoses have been reported in different speciesafter chronic and sub-chronic exposure to mycotoxins like aflatox-ins, fusariotoxins (fumonisins, trichothecenes, zearalenone) andochratoxins. Zearalenone mycotoxicoses occur frequently in swineand bovine breeding (Haouet and Altissimi, 2003; Nebbia and Calo-ni, 2009) and effects of dietary ochratoxin on growing and finishingpigs are reported (Smith et al., 2005). In animal feed, a concentra-tion of fumonisin 1 (FB1) and 2 (FB2) 1.5 times higher than thelethal dose (Iulini et al., 2005) was also found in Italy. In otherareas of that country, FB1 was responsible for porcine pulmonaryoedema in various swine-breeding units (Miraglia et al., 1998). Inthe summer of 2003, the weather led to a critical situation causinghigh levels of mycotoxins in cereals for human and animal con-sumption. The emergency was related to the high level of aflatoxinM1 in cow’s milk, above the established European maximum level(50 ng/kg) (Nebbia and Caloni, 2009). Some acute cases of aflatox-icosis have been reported in bovines. Mycotoxicoses by aflatoxins,ochratoxins and trichothecenes, are also common in poultry (Neb-bia and Caloni, 2009).

Although there are reports of aflatoxin detection in raw andmarket milk in Greece (Roussi et al., 2001), the occurrence of deathsecondary to mycotoxicosis in food animals appears to be rare orunreported. Data from Spain are also scarce and commonly involveaflatoxins (Pérez-López et al., 2004). Some cases are frequently re-directed to private laboratories: in Catalonia, veterinarians in-formed the Faculty of Veterinary Medicine of two confirmed casesof aflatoxicosis in 200 pigs in 2004 and 2006, but the laboratoriescould not provide more information.

Metals

In Northern Greece, heavy metals were found to be the secondmost significant mortality factor in accidental poisoning, corre-sponding to 34.4% of total positive cases, with copper (Cu) toxico-ses being the most prevalent. Toxic Cu levels in the liver weredetected in sheep grazing in pasture previously sprayed with a

Please cite this article in press as: Guitart, R., et al. Animal poisoning in Eudoi:10.1016/j.tvjl.2009.03.002

Cu-containing preparation (Antoniou et al., 2005). The presenceof excessive Cu in commercially prepared milk replacers causedchronic Cu toxicity in veal calves on two different Belgian farms(Croubels et al., 2001a,b).

In France, chronic Cu poisoning is commonly described in sheep(Pouliquen and Douart, 1998). Chronic Cu exposure has been re-ported in the past in Italy (Zanetti et al., 1988) and still representsa problem in those regions where sheep breeding units are found.In Spain, three cases have been described in the last 10 years. Thefirst, in which 24 sheep died, was due to grazing on contaminatedpasture near an old electric wire manufacturing plant (Guitartet al., 1999). A second report, in which 31 lambs died, followedfeeding with sunflowers grown in high Cu-fertilised soils leadingto sunflower meal with elevated metal levels (García-Fernándezet al., 1999). The third event, with 6/7 deaths, occurred in a zoolog-ical park for domestic animals where wood fences treated with aCu-based preservative were found to have been the cause of theproblem (Guitart et al., 1999).

Historically, lead (Pb) poisoning occurred frequently in largeanimals, particularly in cattle. In Belgium, causes have been tracedto the intake of Pb-containing paint used in stables and the lickingof car batteries dumped in meadows (De Corte-Baeten andDebackere, 1973; Debackere and De Corte-Baeten, 1974). InFrance, Pb remains the most frequent cause of metal poisoning in-volved in cases of sudden death. Recently, 9/12 cows died within3 days of ingesting fragments of a battery found in hay. The onlysigns were diarrhoea, sedation, hypermetria and blindness (Gran-cher et al., 2007). In Spain, a case of Pb poisoning in cattle was re-ported by Miranda et al. (2006); here the source was also adiscarded battery found in the pasture, and 6/10 yearling heifersdied. Of the four survivors, three presented symptoms, withdetectable Pb levels in blood for more than 6 months after expo-sure. The long half-life of Pb in these cattle posed a risk for humanconsumers even after such a long period of withdrawal from thetoxic source.

Non-metals and metalloids

In the past, fluorosis in cattle has been ascribed to fluoride pol-lution caused by a brickworks and enamel factory in the Flemishcountryside of Belgium (Debackere and Delbeke, 1978, 1981). Insome regions, the intake of borehole water can lead to fluorosis,due to high levels of fluoride in deep-lying clay layers. This typeof fluoride poisoning has been described, for example, in turkeys,of which mainly fast-growing male animals were affected.

In 2000, a special case of high fluoride intake by calcium sul-phate (CaSO4) was reported at the LTGU. CaSO4 or plaster is formedas a residual product from the production of the fertiliser super-phosphate and can be used as binding agent in the making of beetpulp. The use of CaSO4 can result in raised levels of fluoride in thebeet pulp leading to chronic fluoride intoxication in cattle.

Industrial chemicals

In 1999, Belgium suffered an unprecedented food crisis causedby the contamination of animal feeds with polychlorinated biphe-nyls (PCBs), dioxins and dibenzofurans. The first signs of contami-nation were seen on several poultry farms with a sudden drop inegg production as the initial symptom, followed by a markedreduction in egg hatchability, reduced weight gain and an in-creased mortality of chicks. Histological examination revealeddegenerative changes of the skeletal and cardiac muscles resem-bling the classical manifestations of ‘chicken-oedema disease’ de-scribed in the 1950s to the 1970s in outbreaks of poultrypoisoning by polyhalogenated hydrocarbons (Gilbertson et al.,1991; Bernard et al., 1999; Vanhoutte and Paque, 2000).

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Other toxicants

Nitrite intoxication is known in several species as a cause ofmethaemoglobinaemia. Three cases of acute mortality in pigs,raised in different commercial farms in Belgium have been de-scribed and bacterial contamination of drinking water with subse-quent nitrite formation could be identified as the cause. Stagnantdrinking water within the water system of modern pig farms con-stitutes a risk for nitrite intoxication (Vyt et al., 2005).

Gas intoxication by hydrogen sulphide (H2S) and ammonia(NH3) is well known in the pig industry and can result in suddendeath, especially when the animals are kept in stables with opengrids or when the ventilation systems are working inefficiently.One case of NH3 intoxication was reported in Belgium in bovinesafter the consumption of large amounts of soybean meal withsymptoms such as head pressing, aggression and agitation. Soy-bean meal overconsumption by ruminants can cause acute carbo-hydrate fermentation and excessive ammonia release leading toammonia toxicosis and lactic acidosis (Osweiler, 1996).

Apart from overdose of antiparasitic drugs, very few cases ofdrug poisoning are reported in food-producing animals in France.In Belgium, a case of acute doxycycline intoxication in veal calveswas described during treatment of enzootic pneumonia. The ani-mals accidentally received 5–6 times more than the recommendeddose of doxycycline (Chiers et al., 2004). In 2001, acute tiamulin-salinomycin intoxication in pigs was described following theadministration of salinomycin in the feed and the presence oftraces of tiamulin in the drinking water, resulting from the admin-istration of tiamulin to fattening pigs housed in the stable4 months previously (Croubels et al., 2001a,b).

In the Italian CAV data for 1994–2000, a case of poisoning inMerino sheep was reported, following the application of 1-2dichloropropane liquid to eliminate tar from the fleece. The ani-mals subsequently displayed respiratory distress and difficultystanding, with some succumbing despite veterinary attention.

Conclusions

The first part of this three-part review on animal poisoning inEurope evaluates poisonings in farm livestock and poultry. Althoughfood-producing animals are well represented in all participatingEuropean countries, poisoning is seldom recorded. In Belgium andFrance, most poisoning accidents in food-producing animals occurin cattle, followed by sheep and goats. In Greece, small ruminantsand poultry appear to be more involved, but in Italy and Spainfood-producing animals only account for a minor part comparedto companion animals and horses. Toxic plants and mycotoxins,heavy metals and pesticides are most often suspected as the toxicagents in the five countries. Limited attention is paid to large animaltoxicology problems except when the economic loss is high.

Conflict of interest statement

None of the authors of this paper has a financial or personalrelationship with other people or organisations that could inappro-priately influence or bias the content of the paper.

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