Grass Sickness and Botulism

Keith Miller MRCVS, Biotrix, Peebles

Sporadic cases of equine grass sickness (EGS) were first suspected in Angus towards the end of the 19th Century. Subsequently the disease occurred in local epidemics initially affecting army horses at Barry Camp, Montrose in the spring of 1905. Thereafter, the disease spread rapidly and extensively inland along the fertile straths of Angus and Perthshire (Strathmore 1916); concurrently EGS extended northwards along the coast through Kincardineshire and Aberdeenshire to affect areas of Banff (Spey Valley, 1920) and Moray. In these early years cases were invariably associated with fertilised improved grazing and the disease decimated the large population of young Clydesdale horses in affected areas. Throughout subsequent decades a pattern developed and recurrent outbreaks tended to occur on previously affected premises, disease becoming particularly persistent in and around estates regularly involved in the intensive rearing of game birds.

Coincidentally, during the same period (1880-1920) medical and scientific interest had been focused on a dramatic and fatal human poisoning known as botulism. The disease results from ingestion of a potent bacterial toxin, botulin (or botulinum toxin) produced in imperfectly preserved food. Botulinum toxins were demonstrated to attack the nervous system causing a range of symptoms culminating in respiratory paralysis and death.

In 1918 an Aberdeen-based research team was established by the Highland and Agricultural Society to investigate the cause of EGS which was now regarded as a dire threat to the future of the working horse population in Scotland: the results of a survey in the Morayshire area (1919-1922) revealed a mortality rate of 14.4% in a total population of 888 horses on farms which had had one or more cases of EGS. However, by this time it was evident that some older horses did not succumb to acute and rapidly fatal EGS. Individual animals survived for weeks, or months, with a characteristic sequence of disease signs dominated by profound weight loss with a ‘tucked-up’ abdomen. The overall recovery rate at this time was around 4%.

The EGS research team included medical and agricultural microbiologists and their broad scientific interest led to speculation – could EGS be associated with botulinum toxins? Certainly the neurological signs of chronic EGS were strikingly similar to those of human botulism. The administration of minute doses of botulinum toxins to experimental horses induced dramatic weight loss without affecting appetite or causing any other ill-effect. However, larger doses of botulin, given by mouth, were lethal but failed to reproduce any of the signs of acute EGS.

Unfortunately methodical scientific investigation and consideration of a link between botulism and EGS was upstaged by a dramatic incident of human botulism. The Loch Maree tragedy claimed the lives of eight hotel guests in the western Scottish Highlands. The unfortunate victims had all consumed wild duck paté at lunchtime on Monday 14 August 1922 and all died within the following week: ‘rarely has an almost unknown scientific subject gripped the attention of the multitude as this (incident) did in August and September, 1922.’ The resultant alarmist publicity in Britain and America further confused the equine botulism/EGS issue and led to premature public debate which, in turn, antagonised veterinary opinion against the developing hypothesis.

The inconclusive results of the Highland and Agricultural Society’s research programme, including those of a vaccine trial involving 1316 horses, were presented to a meeting of the Scottish Branch of the National Veterinary Medical Association held at the Station Hotel, Perth on 15 December 1922. These data were discussed at length and unceremoniously discounted at a subsequent acrimonious gathering of veterinary practitioners in Perth on 26 January 1923.

Nevertheless in the period 1920-24 there were reports of devastating animal disease associated with different types of botulinum toxins affecting cattle, horses and poultry in Australia, S. Africa and elsewhere. The equine disease subsequently designated as Forage Poisoning was associated with the presence of preformed botulin present in silage or other feeds contaminated with soil or small animal/bird carcasses. These reports continued to highlight the differences between Forage Poisoning and EGS and effectively put an end to the notion that botulinum toxins are involved in grass sickness. A leading article in the Lancet (19 November, 1927) concluded that veterinary opinion was justified in dismissing any association between ‘grass disease’ and botulism. However, contemporary issues of the Veterinary Record still carried advertisements for botulinum antiserum which practitioners were urged to consider for the treatment and prevention of grass disease and Forage Poisoning.

The present hypothesis was developed in 1995 in an attempt to link the foregoing historical evidence with up to date knowledge of the range of activities of individual botulinum toxins.

Initially the current investigation was based on the premise that EGS is similar to human infant botulism – a cause of sudden death which is known to result from the proliferation of toxin-producing bacteria within the intestine. This phenomenon, known as toxicoinfection, leads to the continuous or intermittent local production of botulinum toxins which may then be absorbed from the bowel. Furthermore, from the outset, it was necessary to demonstrate the involvement (in EGS) of a particular strain of botulinum-toxin producing organism which is commonly carried by birds. The unique combination of botulin types produced by the avian organism is believed (but not yet proved) to be capable of causing the whole spectrum of acute and chronic symptoms and disease signs collectively associated with the EGS ‘disease process’.

Preliminary results are encouraging and clearly demonstrate the presence of avian-type botulinum neurotoxin in the bowel of EGS-affected horses at all stages of the disease. However, it is also evident that many Scottish horses carry the toxin-producing infective organism without ill-effect. These data support the long-suspected belief that horses may develop immunity to EGS and that lactating mares produce milk antibodies to protect suckling foals which rarely suffer from EGS. The concept of immunity would also explain the characteristic age-related susceptibility to grass sickness which is uncommon in older horses.

Current research programmes based in the University of Edinburgh and the University of Liverpool are directed towards elucidation of the role of these specific botulinum toxins and of the mechanisms of immunity. Associated investigations focus on the trigger factor(s), believed to be of dietary origin and/or stress related, which induce a ubiquitous and generally harmless microorganism to produce lethal toxins.

The origin of the avian infection, which has now been re-implicated in a century of incalculable equine suffering and human distress, is and will remain a matter for conjecture. In the early years of research the ‘finger of blame’ was pointed at various imported agents including clover or grass seeds, fertiliser products or even ‘infected’ carrier horses. However, for the most likely explanation to ‘fit the facts’ it may be necessary to put the clock back further to the period from 1860-1880. These years were witness to an agricultural revolution in Scotland (and the eastern counties of England) when millions of tons of imported fertiliser of avian origin were applied to improve arable pastures and rotational crops. The practice was particularly prevalent on premises within easy reach of Dundee, Montrose and Norwich which were the main ports for the trade: the farms in these areas were also home to vast populations of working horses.

Peruvian guano was a potent nitrogenous fertiliser and likely to be an abundant source of toxin-producing bacteria. The material was derived from primordial accumulations of excreta, eggs and the carcasses of countless generations of seabirds and marine mammals (the renowned agronomical qualities of Peruvian guano were primarily due to negligible rainfall on the offshore islands which minimised any leaching of soluble nutrients).

The micro-organisms responsible for producing botulinum toxins are primitive bacteria which can survive as spores in soil or other suitable material. The process of sporulation would thus ensure safe and viable transport of the infective agent from the islands of Peru to the fertile fields of Angus and subsequently throughout the UK and parts of mainland Europe. Intriguingly guano was applied to improve the fertility of farm land on the slopes of the Andes since pre-Christian times – a possible source of infection for horses with mal seco, a disease almost indistinguishable from EGS, affected horses in Patagonia?

The majority of devastating outbreaks of EGS occurred in groups of young army horses. Initially epidemics occurred at TA camps in Scotland (1905-1907) and later on Salisbury Plain (annually from 1922-1936). The concentration of infection resulting from particularly severe outbreaks in 1934 may have contributed to avian-assisted spread of the disease throughout the UK to the Low Countries and Scandinavia.

The Scottish army horses were imported from Ireland in the spring of each year and their apparent susceptibility to EGS could be attributed to lack of any previous exposure to the infective agent. After use in the summer camps the best animals were retained for longer-term duties but the majority were mustered for private sale in the autumn. These annual auctions provided a mechanism for extensive re-distribution of disease-carrying horses: the last end of season dispersal sale of 1000+ ‘ex-army’ horses was held at Perth in 1926. Finally it is interesting to speculate that the routine practice of tethering army horses in picket lines led to a massive accumulation of toxin-producing bacteria (spores) in these areas. Undoubtedly the contaminated soil would provide a risky environment for susceptible ‘new recruits’ in future years.

Copyright © J.K. Miller – March 1999

Footnote:
The author would be pleased to hear from any readers who have factual information relating to the early history of Grass Sickness.
Keith Miller Tel: 01721 723372 or Fax: 01721 723388