Plants and mushrooms associated with animal poisoning incidents in South Africa.

BACKGROUND: There is extensive literature on animal poisoning from plants and mushrooms worldwide; however, there is limited account of poisoning from South Africa.
METHODS: This study sought to describe and provide an overview of animal poison exposures in South Africa. Poisoning episodes reported to the Poisons Information Helpline of the Western Cape, jointly run by the Poisons Information Centres at the Red Cross War Memorial Children's Hospital and Tygerberg Hospital over a period of approximately 2.5 years, from June 2015 to November 2017, were analysed to identify exposure patterns, severity and clinical outcomes.
RESULTS: Alien plant species accounted for most cases (n=10) of reported poison exposures. Among the 26 recorded animal poisoning episodes, the dog was the most commonly implicated species (n=24), whereas just two enquiries were related to other animals (one rabbit and one cow). There were 20 plant cases and 6 mushroom cases (all dogs). There was only one fatal case involving cycad in a dog.
CONCLUSION: Features of animal poisoning in South Africa were similar to those in other countries. The reported cases of animals exposed to poisonous plants and mushrooms could represent only a fraction of the actual exposures. Since most reported cases involved taxa that could not be identified to species level, more attention should be paid in case reporting and in animal poisoning prevention, engaging the public to enable people to recognise potentially hazardous plants and reduce the risk of poisoning in animals. © British Veterinary Association 2020. Re-use permitted under CC BY-NC. No commercial re-use. Published by BMJ.

Introduction

Invasive plants are plants diffusing into areas outside of their natural habitat where they may have a negative effect. The dissemination process can be very rapid and leads to negative consequences1 for the autochthonous species, affecting soil quality in terms of water and nutrients availability and also having a negative impact on the diversity of native species2–5 because of their influence on factors such as solar irradiation and temperature levels. For these reasons, invasive plants are generally undesired,6–11 even more so because of their impact on a large variety of animals quality and quantity of accessible food, refuge/nest sites, basking and perch spots.12–14

The most worrying issue is the emerging impact on human health,15–18 mainly through skin exposure or ingestion leading to poisoning. Indeed, poisoning is a global concern both in humans and animals.19–23 Animal poisoning occurs as a result of exposure to various toxic substances22 24–26 and episodes due to plant exposure are anything but rare.21–23 27–29 Long-term retrospective studies have shown that plants cause major animal poisoning: for example in Germany data of the Poison Centres (2012–2014) showed that plants and mushrooms accounted for 18.6 per cent of all the enquiries on animal (dogs, cats, horses, ruminants, rabbits/rodents and birds) poisoning and, as for calls involving a known toxicant (n=1752), plant and mushroom intoxications were responsible for the highest number of fatal cases (25.7 per cent), whereas in Italy plants accounted for 5.5 per cent of all the enquiries on animal (dogs, cats, horses, ruminants, rabbits, ferrets and exotics) poisoning received by the Poison Control Centre of Milan (2000–2010).22 30 Buttke and others27 indicated that between 2000 and 2010 in the USA, animal exposures resulted in 1 371 095 related cases; this represents 4.7 per cent of all the reported cases of poison exposures on humans and animals and, concerning the latter (dogs, cats, horses, ruminants, aquatics, birds and rodents), plants were responsible for 6.9 per cent of the cases.27 Moreover, according to this study, 15 animal poison exposures occur every hour in the USA, and globally, there are several notable cases of animal poisoning.21–23 25 27 28 31 32

In addition, individual case reports addressing single animal exposures are often reported.33–35 However, it is also worth noting that the underlying causes of animal poison exposures are difficult to ascertain due to various reasons, such as exposures occurring at night or going unobserved by the owners.25 36 Furthermore, in developing countries, there is the challenge of under-reporting of poison exposure cases, which could be attributable to the lack of knowledge and infrastructures.37

Previous studies conducted in South Africa focused on poisoning in humans,19 20 38–40 and only a few studies specifically focused on human poisonings due to plant exposures.19 38 Plant poisoning in South Africa has been described for horses and livestock,41 42 but no report describing poisoning exposures in all types of animals at a country scale has previously been published. Therefore, the aim of this study was to retrospectively collect, evaluate and analyse reports on plant and mushroom poisoning in animals in South Africa.

Materials and methods

A retrospective review of records from the Poisons Information Helpline of the Western Cape (PIH), jointly run by the Poisons Information Centres (PICs) at the Red Cross War Memorial Children’s Hospital and Tygerberg Hospital, was conducted over approximately 2.5 years, from June 1, 2015 to November 30, 2017. Standard PIC consultation forms include the date, origin of the call (province and district), circumstance of exposure, animal characteristics (species/sex/age), substances involved, clinical signs and route of exposure (eg, oral). All reported cases related to animal poisoning between June 1, 2015 and November 30, 2017 were reviewed to identify those caused by plants and mushrooms. The plants were identified by experts in the PIC in consultation with Universities and the South African National Biodiversity Institute. According to the data, the causative substances were classified into three main categories: alien, native and unknown taxa (unknown taxa refers to cases involving taxa that could only be identified to genus level), the origin of plants follows the classification by Richardson and others,1 alien plant species ‘Plant taxa in a given area whose presence there is due to intentional or accidental introduction as a result of human activity’. The Gwaltney-Brant method43 for classifying the severity of exposure was used postevent by the researchers, with the following categories: ‘no signs’, ‘mild’, ‘moderate’ or ‘severe’.

Results

The PIH handled 790 cases related to plants and mushrooms during the 2.5-year period and 26 recorded cases involving animals that were accidentally exposed to biological toxins (corresponding to 3.3 per cent of all animal-related exposures) (table 1). Of these enquiries, 24 cases involved dogs. Calls related to other species happened only two times, regarding one rabbit and one cow. In all reported cases, the route of exposure was ingestion.

Table 1

List of the poisoning cases due to plants reported to the Poisons Information Helpline of the Western Cape (PIH), jointly run by the Poisons Information Centres (PICs) at the Red Cross War Memorial Children’s Hospital and Tygerberg Hospital in South Africa from June 2015 to November 2017 with information on year of reporting, animal species involved, suspect plant species, active principles, origin of the plant species, severity of intoxication and clinical signs

Year	Animal poisoned	Suspected plant species		Toxic compounds	Origin of plant species (native/alien/unknown)	Severity of intoxication (no sign/mild/moderate/severe/death)*	Clinical signs
		Taxon	Common name
2017	Dog	Allium sativum	Garlic	Alliin (NPAA) cleaved to allicin and various allylsulphides†; disulfides and sulfoxides.‡	Alien	No signs	Asymptomatic.
2017	Dog	Brugmansia candida	Angel’s trumpet	Tropane alkaloids (eg, scopolamine, hyoscyamine and tigloidine).†	Alien	Severe	Vomiting and diarrhoea.
2016	Dog	Chlorophytum comosum	St. Bernard’s lily	Non-toxic.‡§	Native	Severe	Severe vomiting and diarrhoea.
2016	Dog	Crassula perforata variegata	Variegated necklace vine	No information.	Native	No signs	Asymptomatic.
2016	Dog	Duranta repens	Pigeon berry	Iridoid glycosides (durantoside I, II and III); saponins; alkaloids (narcotine).	Alien	No signs	Asymptomatic.
2016	Rabbit	Echveria subsessilis	Morning beauty	No information.	Alien	No signs	Asymptomatic.
2016	Dog	Euphorbia marginata	Snow-on-the-mountain	Latex§; phorbol esters; triterenoids.†	Alien	Moderate	Vomiting.
2017	Dog	Ficus carica	Common fig	Latex§; fluranocoumarins, flavenoids, triterpenes and sesquiterpine glycosides.†	Alien	No signs	Asymptomatic.
2016	Dog	Mammillaria toluca	Mammillaria	No information.	Alien	No signs	Asymptomatic.
2016	Dog	Melia azedarach	Chinaberry tree	Triterpenoid limonoids§ triterpines, kulinone, kulacton, meliantrol, meliatoxins and alkaloids.†	Alien	No signs	Asymptomatic.
2016	Dog	Nerium oleander	Oleander	Oleandrine and cardenolides.†	Alien	Severe	Protracted vomiting and collapsed today. Resuscitated with fluids and epinephrine.
2016	Dog	Phoenix sylvestris	Silver date palm	Non-toxic (Indian date).	Alien	Moderate	Weak, with watery diarrhoea.
2017	Cow	Sarcostemma viminale	Caustic bush	Latex§; Sarcovimicide A and other steroid glycosides.†	Native	Severe	Lots of salivation and animal cannot lift its head.
2017	Dog	Zantedeschia aethiopica	Calla lily	Calcium oxalates.†§	Native	No signs	Asymptomatic

Mind-Altering and Poisonous Plants of the World. Timber Press; 2008.

*(45).

†Data from Wink M and Van Wyk B-E.

‡Data from Toxinz database.

§Data from AfriTox database.

Plants and mushrooms involved

Most reported cases involved plants (n=20, table 1), while mushrooms accounted for six cases (table 2). Cases involving plant species for which no records of poisoning in literature could be found were Echeveria subsessilis (one case involving a rabbit), Mammillaria toluca and Phoenix sylvestris. In 11 cases, the plants and mushrooms involved were not identified to species level.

Table 2

List of the poisoning cases due to fungi reported to the Poisons Information Helpline of the Western Cape, jointly run by the Poisons Information Centres at the Red Cross War Memorial Children’s Hospital and Tygerberg Hospital in South Africa from June 2015 to November 2017 with information on year of reporting, animal species involved, suspect fungus species, active principles, origin of the fungus species, severity of intoxication and clinical signs

Year	Animal poisoned	Suspected fungus species	Origin of fungus species (native/alien/unknown)	Severity of intoxication (no sign/mild/ moderate/severe/death)	Clinical signs
September 30, 2017	Dog	Mushroom	Unknown	No signs	Dog is asymptomatic.
February 15, 2017	Dog	Mushroom	Unknown	Mild	Dog showing convulsive behaviour could also have ingested seagro organic plant food or ant-trap on intravenous drip and giving AC.
May 29, 2016	Dog	Small white mushrooms	Unknown	No signs	Puppy is asymptomatic.
March 6, 2016	Dog	Mushrooms - unidentified	Unknown	Mild	Dog’s nose is warm but otherwise asymptomatic.
February 28, 2016	Dog	Mushroom	Unknown	No signs	Dog is asymptomatic.
January 24, 2016	Dog	Garden mushroom	Unknown	No signs	Dog is asymptomatic.

Clinical signs and outcomes

We found that the majority of the reported cases showed no clinical signs (n=12), followed by less than a third of cases showing mild symptoms (n=8), while few cases showed moderate and major symptoms (n=3, figure 1). Most animals with clinical signs of poisoning recovered with treatment. The most common clinical signs were hypersalivation, vomiting, diarrhoea and weakness. An intoxication in a cow from Sarcostemma viminale was reported with the animal exhibiting hypersalivation and weakness possibly due to the presence of pregnane glycosides.44 Severe symptoms developed in three dogs as a result of exposure to Nerium oleander, Chlorophytum comosum and cycad species, the last of which resulted in death after a dog ingested seeds of a cycad species.

Figure 1

Categories of plant and mushrooms species involved in animal exposures.

Categories of the origin of species

Cases associated with alien plant species accounted for 10 out of 26 episodes, while unknown taxa were responsible for 12 out of 26 cases (ie, Clivia species, Lycoperdon species, Malva species, Cycad and mushrooms). Calls related to native species were much fewer in comparison (ie, C comosum, Crassula perforata variegata, S viminale, Zantedeschia aethiopica) (figure 2).

Figure 2

Severity of clinical signs of animal exposure to plants and mushrooms according to Gwaltney-Brant.43

Discussion

Limitations

The major limitation of the study is the limited number of cases reported; moreover, there is uncertainty as to whether the reported cases reflect the actual situation with regards to animals being affected (mostly dogs reported) and severity. Furthermore, there is the possibility that owners may call the poison centre reporting as poisonings, symptoms actually due to other medical conditions. It is also a weakness that other underlying causes of the symptoms described were not ruled out by veterinary professionals, in particular when plant poisoning was suspected but the involved plants were believed to be non-toxic. The plant/mushroom variables analysed in this study were limited by the lack of description of some of the reported species, since not all the plants and mushrooms could be identified to a species level. Nevertheless, it should be considered that toxicity can often be similar throughout a broader taxon, thus specific classification is not always essential. Moreover, the correct classification of the plants according to their characteristics may be challenging for the public. Certain information was not available, such as the age of the animals involved. Our study was limited with regards to the quantity ingested; however, this is not unique due to the subject of study being animals.

Incidence of plant and mushroom poisoning in animals

Our results confirmed that animal poisoning exposures to plant and mushrooms are important in the world. In South Africa, 3.3 per cent of all plant–mushroom related calls involved animals, which is similar to the situation in Germany where animal-related calls accounted for at most 3.7 per cent of all poison calls received.30 Poisoning was most commonly reported in dogs. Notwithstanding our small sample size, this finding is consistent with previous studies that indicated higher poisoning exposures from accidental poisoning in dogs.21–23 28 29 45–48 As for the other animals, we had just one report concerning a cow and one on a rabbit. This fact could possibly be attributed, among various reasons, to a poor reporting of cases due to lack of knowledge of the existence of facilities such as the PIH.37

Our findings are in line with those of studies carried out in Germany, Italy and the USA, which demonstrated that many reported cases of animal poison exposures showed no clinical signs and that few cases result in fatalities.22 25 28 30 31 45 Furthermore, our study was similar to a previous research carried out in Italy over two 10-year periods (2000–2010 and 2000–2011), which showed that the most common clinical signs observed in poisoning episodes involving dogs and cats were hypersalivation, vomiting, diarrhoea and weakness, whereas diarrhoea and depression were the most frequently reported in cases concerning ruminants.22 28 This study has also described a dog fatality due to a cycad species that are generally known to possess toxic compounds such as cycasin.49 50 In this regard, it would be useful to implement the indications of McFarland and others,30 who suggested the importance of a systematic collection of data concerning poisoning episodes, for example, establishing sentinel laboratories and clinics throughout the country to perform a correct risk evaluation as well as to improve the outcomes.

This study revealed that the majority of poisonings were caused by alien plant species, followed by plants and mushrooms that could not be identified to a species level (predominantly mushrooms), while native plants only accounted for a few reported cases. The most common toxic plants reported in literature, which were also reported in this study, include Brugmansia candida,51 Melia azedarach,45 52 N oleander,24 28 Duranta repens53 54 and Euphorbia marginata,55 56 whereas the less common plants, both in this study and in previous literature, include E subsessilis, Ficus carica L., M toluca and P sylvestris. However, this could be attributed to the fact that most of the plants are ornamental plants; hence, the exposure of pets is likely.53 According to the study by Caloni and others,28 which focused on plant poisonings in domestic animals in Italy between 2000 and 2011 and revealed causative species that are also present in South Africa, N oleander was responsible for nine poisoning cases in dogs, of which one case resulted in death. Due to the increased globalisation, many plants are moved around the world for various purposes such as pot plants or for gardening.57 However, since these plants did not naturally occur in the area of introduction, people have little to limited knowledge about their toxicity in both humans and animals.57

The episode of intoxication recorded in a cow due to the ingestion of S viminale with the animal exhibiting hypersalivation and weakness probably due to the presence of pregnane glycosides44 is new in the literature. In South Africa, the most common episodes involving cows are exposures to cardiac glycoside-containing plants, mainly N oleander, species that has been frequently implicated also in the southern USA, where it is very common, and in Brazil.41 58–60 Our findings are similar to those reported in other studies, which showed that the native plants that were the primary causes of animal poisoning around the world.28 44 There are few studies reporting animal poisoning from C comosum and Crassula perforata variegata.61 In livestock, the exposures generally occur when the hay or silage are contaminated by poisonous plants or when forage alternatives are not accessible. Other causes are drought, recently burned pastures, introduction of animals in new areas with different plants and factors like climate and livestock/pastures management.41 62

Conclusion

This is one of the first studies to access poison centre reported records of animal poisoning at national scale in South Africa, and the data described provide useful information on animal exposure to plants and mushrooms in this country. The dog was the most reported species, and the most implicated group of plants were those not native to South Africa, probably because this species, which generally share the owner’s domestic environment, is more likely to come in contact with ornamental plants that are usually native to other geographical regions. The results indicated that there seem to be an under-reporting of intoxication incidences and that there is the need to implement strategies to stimulate the reporting of the cases. Moreover, more attention should be paid to prevention of poisoning in animals and that there is a need to engage the public for future surveillance and to enable people to recognise potentially hazardous plants and reduce the risk of poisoning in animals. Finally, strengthening the case management and increasing the pharmacovigilance would be beneficial to improve the survival and presentation of animal-related cases of poisoning.