Sokoto Journal of Veterinary Sciences, Volume 14 (Number 1). April, 2016 REVIEW ARTICLE Sokoto Journal of Veterinary Sciences (P-ISSN 1595-093X/ E-ISSN 2315-6201) Ngulde et al/Sokoto Journal of Veterinary Sciences (2016) 14(1): 1-9 http://dx.doi.org/10.4314/sokjvs.v14i1.1 An Overview of carnea subspecies fistulosa toxicosis in ruminants SI Ngulde*, MB Tijjani & LN Giwa-Imam

Department of Veterinary Physiology, Pharmacology and Biochemistry, University of Maiduguri, PMB 1069 Maiduguri, Nigeria

*Correspondence: Tel.: +2348028797746, E-mail: [email protected] Abstract Ipomoea carnea subsp. fistulosa () is identified and confirmed as a poisonous to animals in many parts of the world. It is evergreen and common in Sahel region of Nigeria where there is lack of green pasture in most part of the year. It contains two toxic principles, swainsonine and calystegines causing neurological condition called acquired lysosomal storage disease. Its toxicological status is not determined in the region despite risk of poisoning. Therefore it is being reviewed for its toxic effects, epidemiology, pathogenesis, clinical presentations, pathology, diagnosis and management. More attention should be paid to the plant as potential source of toxins for domestic animals in the Sahel region of Nigeria.

Keywords: Clinical presentation, Epidemiology, Goats, Ipomoea carnea, Pathogenesis, toxins, Sahel region Received: 12-11-2015 Accepted: 17-03-2016

Introduction Ipomoea carnea subspecies fistulosa is a plant appear reddish brown when ripe (de Balogh et al., belonging to the family convolvulaceae. It is called 1999; Arbonnier, 2004). shrubby (de Balogh et al., 1999). It is In Borno State, Nigeria, I. carnea subs fistulosa is often called as Kafi Kansila (better than a planted as a hedge plant both in villages and towns councilor) in the Northern Nigeria because it is and also grows as a wild plant along river-banks used for the control of erosion that some elected and refuse dumping sites. It is an evergreen plant. councilors cannot do for their ward. It grows on Farm animals especially goats often browse on it almost all types of soil but especially on well- during the dry season. drained sandy soil, close to river-banks and swamp Ipomoea carnea subsp. fistulosa has been edges (Arbonnier, 2004). It is a plant of tropical identified and confirmed as a poisonous plant in America but it has now spread all over the tropical many parts of the world. In Mozambique, it was and subtropical regions of the world. It was reported that about 10% of goats died within 12 probably introduced to West Africa from Arabia by months of exposure to the plant (de Balogh et al., Pilgrims of Mecca (Goncalves, 1987; Austin & 1999). This evergreen plant seems to be the only Huaman, 1996; de Balogh et al., 1999; Arbonnier, shrub that is available during the period of long dry 2004). season in Maiduguri. Despite its presence, its Ipomoea carnea subsp. fistulosa (Plate I) is a shrub status is yet to be determined in this Sahel region that is up to 3 m long. It is densely leafed and where green pastures are not readily available in branches from the base. The stems are grey-green most parts of the year. It might be a potential and puberulous, leaves elongate to elliptical 10-25 source of poisoning to animals in the region cm long. The flowers are 5-8 cm long, pink to pink- thereby causing economic loss to the farmers. purple, cluster, funnel shaped and posses 5 lobes. Therefore, it is being reviewed for its various toxic The fruits are ovoid and angular 1-2 cm long and effects to farm animals that consume it.

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Epidemiology The plant I. carnea subsp. fistulosa is distributed through out the tropical and subtropical regions of the world. It is cultivated as an ornamental and in hedges and windbreaks but in some areas, it escapes from cultivation and become established in disturbed areas such as roadsides, river-banks and other moist areas (de Balogh et al., 1999). Intoxication by the plant in goats, sheep, cattle and horses has been reported in Brazil since 19th Century (Neiva & Penna, 1916). It has been reported in other countries such as Sudan (Idris et al., 1973), India (Tirkey et al., 1987), Indonesia (Bahr, 1983) and Mozambique (de Balogh et al., 1999). All ages of either sex are affected and the condition is more severe in goats but some Plate I: The plant Ipomoea carnea in Maiduguri, farmers reported that suckling kids and lambs are Nigeria not affected (Nath & Pathak, 1995 ; de Balogh et al., 1999). The animal must continuously ingest the to be 0.11% and 0.14% in 2002 and 0.01% and plant for a minimum of three weeks for 0.05% in 2003, while Barbosa et al. (2007) found spontaneous toxicosis to establish (Radostits et al., out to be 0.05% and 0.01%, respectively. 2006; Barbosa et al., 2007). Intoxication is Swainsonine is more toxic than calystegine. This common in dry season where this plant may be was demonstrated in mice where swainsonine was the only green pasture available (de Balogh et al., suggested to be more toxic than calystegines and 1999). castanospermines but mice could not be a good Clinical signs of intoxication by this plant begin to model because of their great resistance to diseases appear during the 3rd and 4th month after the end (Stegelmeier et al., 2008). containing of the rainy season. In Mozambique, the herdsmen swainsonine in excess of 0.001% are considered as called the condition “Canudo” (named after the poisonous (Molyneux et al., 1994). Such stalk of the plant) or “mata cabra” (goat killer). concentration should exceed the threshold dose Also, some animals appear to develop addiction to that would completely saturate the enzyme α- ingest it even when there are other pastures mannosidase. A daily dose of swainsonine 1 and available (de Balogh et al., 1999, Radostits et al., 1.5 mg/Kg were observed to decrease the levels of 2006). However, recent studies conducted on α-mannosidase after one day of treatment to sheep and goats revealed that there was no 53±17 and 39±l2 nM respectively. Both levels had significant difference between experienced and similar mannosidase activities (Stegelmeier et al., naïve animals in consuming the plant suggesting 1994). The minimal toxic dose (LD50) in goats was no addiction (Oliveira-Junior et al., 2015). estimated to be 60 mg/kg for the plant I. Intoxication causes α-mannosidosis and this has sericophylla (swainsonine content = 0.05% of the been reproduced experimentally following total dry matter) (Barbosa et al., 2007). administration of the plant materials in both farm Swainsonine resulted in about 60% reduction of α- and laboratory animals (Huxtable et al., 1982; de mannosidase activity. Calystegine B2 and C1 Balogh et al., 1999; Armien et al., 2007). showed no inhibition of β-glucosidase. Instead, it increases the activity of the enzyme up to 1.5 Toxic principles folds. It is then suggested that calystegines B2 and Two toxic principles, swainsonine and calystegins C1 act as chemical chaperones that enhance B1, B2, B3, and C1 (Figure 1) have been identified in proper folding of the enzyme for smooth I. carnea subsp. fistulosa (de Balogh et al., 1999; trafficking to the lysosomes (Ikeda et al., 2003). Hueza et al., 2005). The concentrations of these Apart from I. carnea subspecies fistulosa, I. riedelii alkaloids in fresh leaves of the plant are about and I. sericophylla, other plants that are known to 0.002% (swainsonine) and 0.0045% (calystegines) contain the toxic principle, swainsonine, include I. while the seed of the plants contain as much as carnea subsp. carnea, Swainsona galegifolia, S. ten times higher than those of the leaves and brachycarpa, S. canescens, S. grayana, S. luteola, S. flowers (Haraguchi et al., 2003). However, the Procubens, S. swainsonoides, Astragalus concentration of the toxic principles varies from lentiginosus, A. Emoryanus, A. Mollissimus, time to time even within the same species. Oxytropis serica and O. Ochrocephalata (Radostits Barbosa et al. (2006) found out that the et al., 2006), Sida carpinifolia (Driemeier et al., swainsonine content of I. sericophylla and I. riedelii 2000; Colodel et al., 2002) and Turbina spp (Loretti 2

Sokoto Journal of Veterinary Sciences, Volume 14 (Number 1). April, 2016 et al., 2003). Only calystegines are found in the storage disease in animals. This is because the plants Solanum dimidiatum, S. fastigiatum and S. calystegines tested in cultured human lymphoblast boriensis (Borros et al., 1987). Both swainsonine potentiate rather than inhibit the lysosomal α- and calystegines are in Ipomoea sp Q6 (calobra) galactosidase and β-glucosidase. CalystegineC1 has and I. polpha (Molyneux et al., 1995). potent activity against lysosomal β-glucosidase while Calystegine B3 has moderate activity against Pathogenesis α- and ß- mannosidase (Ikeda et al., 2003). Continuous ingestion of the plant I. carnea subsp. Alpha-mannosidosis is the most important fistulosa causes a disease condition in animals acquired lysosomal storage diseases of animals called acquired lysosomal storage disease. It is induced by the swainsonine containing plants. It is induced by the toxic principles of the plant, characterized by wide spread neurovisceral swainsonine and calystegines. Swainsonine is cytoplasmic vocuolation that disrupt lysosomal capable of inhibiting lysosomal enzymes α- function, normal cellular metabolism and mannosidase and Golgi mannosidase II (Colegate eventually cell death (Armien et al., 2007). et al., 1979; Molyneux & James, 1982; Armien et Vacuolation develop because of accumulation of al., 2007). In the brain, GABAnergic cerebellar oligosaccharides in the lysosomes. The nervous neurons showed most degenerative changes system is most affected but endocrine, (Armien, 2000). Inhibition of these enzymes will immunologic, digestive and cardiovascular lead to accumulation of incompletely processed functions may also be affected (Stegelmeier et al., oligosaccharides in the lysosomes. The 1999). It is associated with increased phagocytosis oligosaccharides include α-mannosyl and β-N- activity and hydrogen peroxide production by glucosamine moieties (Dorling et al., 1980; Alroy et macrophages (Hueza et al., 2003). It has al., 1985). Lectinhistochemistry by Armien et al. depolarizing neuromuscular blocking activity (2007) revealed that α-glucose mannose, α- (Abdulhadi et al., 1986). In rats the toxic principles glucose, β-(1-4)-N-acetylglucosamine and N- of I. carnea may cross the placenta because acetylmuramic acid are found on lysosomal prenatal administration to dams of 6-20 days membranes of all tissues while β-D-galactose on gestation produced irreversible lesions in 7-day old Kuppfer cells and galactose-β-(1-3)-N- pups and reversible lesions in the dams (Hueza et acetylgalactosamine on brain perivascular cells al., 2003). and renal tubular epithelium. The calystegines constitute the second toxic Clinical signs principles in I. carnea subsp. fistulosa. Calystegine The clinical signs of intoxication by I. carnea subsp. B2 and C1 inhibit β-glucosidase and α- and β- fistulosa in both spontaneous and experimental galactosidase enzymes, respectively (Molyneux et poisoning are similar. It has been described (de al., 1993). Inherited lysosomal disease of humans, Balogh et al., 1999; Armien et al., 2007) as follows. Gaucher’s disease and Fabry’s disease, are similar First signs may be noticed after three weeks of to the toxicosis induced by inhibition of α- and β- regular consumption of the toxic plant. Initial sign galactosidase, respectively (Dorling, 1984). These is usually anorexia and in the first week there diseases are characterized by epileptiform seizures would be mild intention tremors, incoordination and vacuolation of Purkinje cells. However, the calystegines seem to have little effect in lysosmal and reluctance to move when disturbed. In intention tremors, incoordination and falling when disturbed or frightened. There will be symmetrical ataxia, head tremors, hyperesthesia, high stepping gait, progressive weight loss and in some animals diarrhea and pale mucous membranes may be observed (de Balogh et al., 1999; Armien et al., 2007). Other signs include dilated nostrils, posterior paresis (Plate IIa), abduction of hindquarters, opisthotonus, strabismus, nystagmus, hypermetria and dysmetria (Plate IIb). Head raising test (that is, raising the head of the animal for one minute and then suddenly releasing it) is followed by severe intention tremors. There

Figure 1: Glycosidase inhibitory-alkaloids in Ipomoea Carnea (de Balogh et al., 1999)

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Plate II: (a) Posterior paresis and (b) Hypermetria/dysmetria, Source: Armien, 2000. will be muscle hypertonia of the head, neck and Pathology legs, and sternal recumbency with forelimbs rigid Clinical pathology and stretched forward. Appetite remains normal. Clinicopathogical changes appear to fluctuate Depression, lacrimation and nasal discharge occur within the normal ranges. Aspartate amino in some animals (de Balogh et al., 1999; Armien et transferase (AST), blood urea nitrogen (BUN), a., 2007). Despite the severity of the condition, creatine levels and total protein remain normal (de affected pregnant does and ewes deliver Balogh et al., 1999; Armien et al., 2007). Also apparently healthy kids/lambs but they may be experimental poisoning with I. sericophylla and I. affected if they suckle affected nannies (Armien et riedelii in goats showed the serum levels of al., 2007; Ríos et al., 2012). In contrast, Gotardo et protein, albumin and glucose, and serum activities al. (2011) and Gotardo et al. (2012) reported that of gamma-glutamyltransferase (GGT) and AST as pregnant goats experimentally fed with I. carnea well as packed cell volume (PCV), red blood cell had teratogenic effect on feotuses and kids (RBC), white blood cell (WBC), haemaglobin (HB), delivered had significant behavioral alterations. mean corpuscular volume (MCV) and mean Ultrasonography revealed decreased foetal corpuscular haemoglobin concentration (MCHC) movement and there was increased number of values remained within normal ranges (Barbosa birth defects compared to the non-treated group. etal., 2007). Moreover, experimental ingestion of Similarly, chronic locoweed (Astragalus) Astragalus mollissimus var. mollissimus in cattle intoxication causes cardiovascular and showed no variation in serum biochemistry and reproductive disorders in ruminants and this urinalysis except hypoalbuminaemia and reduced include altered libido, infertility, abortion and levels of serum thyronine. However, increase in placental abnormalities (Stelgemeier et al., 1995). alanine amino transferase (ALT) and decrease in Also Sida carpinifolia poisoning was associated haemoglobin content at high dose of ingestion of with neonatal motalities and abortion in Anglo- the toxic plant I. carnea subsp. fistulosa was Nubian and Saanen goats (Driemeier et. al., 2000). reported (Schumaler-Henrique, 2003). Severe The above-mentioned signs develop in animals central nervous system sign is associated with high that have been ingesting small amount of various level of up to 10 fold increase of creatinihe kinase doses of the poisonous plant for a minimum of 3 (CK) (de Balogh et al., 1999). weeks. However goats fed solely on similar plant I. riedelii (0.14% swainsonine dry matter content) as Gross lesions the only feed developed signs within 11 days and The affected carcass of I. carnea subsp. fistulosa died after 22 days of daily ingestion of the plant intoxication is emaciated, has pale mucous (Barbosa et al., 2006). Animals that continuously membrane and there may be congestion of feed on this plant inevitably dies because of meninges, marked asymmetry and atrophy of inability to move and feed or because of cerebellum, slight oedema of spinal cord and/or neurological lesions of vegetative centre mild hydropericardium (de Balogh et al, 1999; controlling cardiovascular and respiratory Armien et al., 2007). In some instances, there may functions (Stelgemeier et al., 1999; Armien et al., be no significant gross lesions (Armien et al., 2007; 2007). Barbosa et al., 2007). Gastrointestinal dysfunction and metabolic disorders such as altered gastrointestinal tract enzyme secretions and 4

Sokoto Journal of Veterinary Sciences, Volume 14 (Number 1). April, 2016 reflexes as well as neurological disorders which et al., 2007). The cytoplasmic vacuoles in neurons include difficulty to move and graze, and anorexia and other cells are mostly optically empty but may be responsible for weight loss and emaciation some individual vacuoles may have amorphous associated with this condition just as it was membranous fragments, vesicles, reticular or attributed in locoism (Stelgemeier et al., 1999). dense granules, opaque globules of osmeophilic materials (Plate IIIa) (Armien et al., 2007). Histopathology The most prominent histopathologic lesions are Diagnosis observed in the central nervous system but In the diagnosis of I. carnea subsp. fistulosa pancreas, kidneys, liver, intestine and lymph nodes toxicosis, the following conditions have to be are also affected. There would be diffuse neuronal considered (Armien et al, 2007). There should be cytoplasmic vacuolation, axonal degeneration and history of existence of the plant in large quantities, astrogliosis of cerebral cortex, Purkinje cells in accessible and ingested by the animal cerebellum brain stem, and dorsal and ventral continuously for several weeks before clinical signs horn neurons of the spinal cord (de Balogh et al., develop. Affected animals will have clinical signs 1999; Armien et al., 2007). Lesions are more that include bilateral symmetrical ataxia, paresis, prominent in cerebral cortex, corpus striatum and propioceptive deficit, abnormal and postural thalamus. The hematoxyline and eosin (H and E) reactions. There must be cytoplasmic vacuolation stained sections revealed neurons that have of neurovisceral tissues at histopathology. distended foamy cytoplasm containing many small Differential diagnosis includes toxicosis by other vacuoles (de Balogh et al., 1999; Armien et al., plants that contain swainsonine and/or 2007). There are dispersed Nissl substance, and calystegines (e.g. locoism). Inherited α- spongiosus of the optic tract. Also, vacuolation of mannosidosis, β-mannosidosis, ganliosidosis and oligodendrocytes, endothelial cells and mucopolysaccharidosis have similar clinical and perivascular cells of the central nervous system. pathological pictures with those of acquired Axonal degeneration is characterized by spheriod lysosomal storage diseases (Radostits et al., 2006). formation and this is most prominent in the granular layer and white matter of the cerebral Management cortex (Armien et al., 2007). Clinical recovery occurs following cessation of Purkinje neurons of the cerebellum are affected ingestion of the toxic plant by affected animal. This and appear shrunken, condensed cytoplasm with is possible when the case of poisoning is not too hyperchrornatic nuclei or there may be complete advanced or prolonged. Daily regular ingestion of loss of the cells and development of vacuolation, small amount of Ipomoea species in goats for up gliosis and astrocytes proliferation. Spheroids and to 70 days and then the plant is withdrawn, may torpedoes are also observed. Spheroids (Plate IIIb) be followed by disappearance of clinical signs are characterized by axonal expansion and within 6 days. However this may not be possible if accumulation of dense bodies, mitochondria, the plant is consumed for up to 120 days. Recovery microtubules and intermediary filaments where as is associated with complete reversal of all torpedoes are enlargement of the proximal neurological signs (Radostits et al., 2006; de segments of Purkinje axons (de Balogh et al., Balogh et al., 1999; Barbosa et al., 2007). Also, 1999). In more prolonged cases, it is characterized Barbosa et al. (2006) reported that goats that by moderate astrogliosis especially in areas with continued to ingest the swainsonine containing more severe neuronal and axonal degenerations. plants for up to 20-28 days after the appearance of Astrocytes contain intense eosinophilia and plump clinical signs recovered within 4-14 days after cytoplasmic processes, and the nuclei are suspension of the plant. Therefore, there is eccentric, large and indented (Armien et al., 2007). possibility for animals to recover fully from Also vacuolation are observed in the neurons of poisoning within short period if they have not the submucosal and mesenteric plexus of the small grazed on the plant for too long. However, animals intestine and in the epithelial cells of the kidney that have developed addiction and continue to (Armien et al., 2007), pancreatic acinar cells (Plate ingest this plant in preference of other feed need IVa) (de Balogh et al., 1999; Armien et al., 2007), to be culled (Barbosa et al., 2007). Massive follicular cells of thyroid glands (Plate IVb), destruction of the plant that is accessible to the macrophages in lymph nodes (Plate IVc), animals has been practiced as a control measure. hepatocytes and Kupffer cells (Plate IVd). There This involves the collaboration of agricultural are reduced number of mature secretory granules extension agents and village heads and is followed of endocrine and exocrine pancreatic cells by marked reduction of number of animals (Armien, 2000; Schumaler-Henrique, 2003; Armien affected (de Balogh et al., 1999).

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Plates III: Cerebellum, Purkinje cell (a) showing empty vacuoles with some amorphous/osmeophilic materials, and (b) cytoplasmic vacuolation (arrow head) and axonal spheroid (arrow). Source: Armien et al., 2007

Plate IV: Cytoplasmic vacuolation in various organs of a goat experimentally poisoned with Ipomoea carnea. Source: Armien, 2000

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Conclusion evaluate the possibility of the toxic effect of the Ipomeoa carnea subsp. fistulosa is not an plant. indigenous plant in this locality but has now spread everywhere both in urban and rural areas, Recommendations as well as in the wild. It contains two toxic There is need to determine hazard of the plant in principles, swainsonine and calystegines. Alpha terms of pattern of distribution and its population (α)-mannosidosis is the most important acquired density in our local environment as the plant is all lysosomal storage disease induced by ingestion of over Northern Nigeria. The nature of the plant in this plant. This condition is characterized by the Sahel region should be determined as neurological impairments and generalized concentration of the toxic principles varies from cytoplasmic vacuolation of various tissues of the time to time even within the same species. There body. The status of this plant is not determined in is need to develop a checklist for veterinarians as the Sahel region but risk of poisoning cannot be well as its differentials to enable easy diagnosis. denied. This is because of the long dry season, free Just like other ornamental plants that are closely range management system practiced, intoxication guarded against animals, domestically grown plant is slow and often reversible, addiction may occur should also be fenced to keep away from animals. and there is no assessment plan on ground to

References Abdelhadi AA, Elkheir YM, Hassan T & Mustafa AA in goats in the state of Paraiba, (1986). Neuromuscular blocking activity Northeastern Brazil. Toxicon, 47(4): 371- of a crude aqueous extract of 379. Ipomoea fistulosa. Clinical and Barbosa RC, Riet-Correa F, Lima EF, Medeiros RM, Experimental Pharmacology and Guedes KM, Gardner DR, Molyneux RJ, de Physiology,13(2): 169-171. Melo LE (2007). Experimental Alroy J, Orgad U, Ucci AA & Gavris VE (1985). swainsonine poisoning in goats ingesting Swainsonine toxicosis mimics Ipomoea sericophylia and Ipomoea riedelii lectinhistochemistry of mannosidosis. (Convolvulaceae). Pesquisa Veterinária Veterinary Patholology, 22(4): 311-3116. Brasileira, 27(10): 409-414. Arbonnier M (2004). Trees, shrubs and Lianas of Barros SS, Riet-Correia F, Andujar MB, Motta A & West African Dry Zones, CIRAD MARGRAF Schild AL (1987). Solanum fastigiatum var. Publishers MNHN. Pp 281. fastigiaturn and Solanuna subsp. Armien AG (2000). Vergleichendeklinische und poisoning in cattle: ultrastructural morphoogische changes in the cerebellum. Pesquisa Untersuchungenzurspontanen und Veterinária Brasileira, 7(1): 1-5. experimentellenVergiftungdurch Ipomoea Colegate SM, Huxtable CR & Dorling PR (1979). fistulosa (Convolvulaceae) bei Ziegen Spectroscopic investigation of Inaugural-Dissertation zur Erlangung des swainsonine and α-mannosidase inhibitor Doktorgradesbeim Fachbereich isolated from Swainsona canescens. Veterinarmedizin der Justus-Liebig- Australian Journal of Chemistry, 32: 2257- UniversitatGießen. 2264. http://geb.uni- Colodel EM, Gardner DR, Zlotowski P & Driemeier qiessen.de/qeb/voltexte/2000/212/pdf/A D (2002). Identification of Swainsonine as rmienMAnibal-2000-02-12.pdf, retrieved a glycoside inhibitor responsible for Sida 05-08-2008. carpinfolia poisoning. Veterinary & Armien AG, Tokarnia CH, Peixoto PV & Frees K Human Toxicology, 44(3): 177-178. (2007). Spontaneous and experimental de Balogh KKIM, Dimande AP, van der Lugt JJ, glycoprotein storage disease of goats Molyneux RJ, Naude TW & Welman WG induced by Ipomoea carnea subsp. (1999). A lysosomal storage disease fistulosa (Convolvulaceae). Veterinary induced by Ipomoea carnea in goats in Pathology, 44(2): 170-184. Mozambique. Journal of Veterinary Austin DF & Huaman ZA (1996). Synopsis of Diagnostic Investigation, 11(3): 266-273. Ipomoea (Convolvulaceae) in the Dorling PR, Huxtable CR & Colegate SM (1980). Americas. Taxon, 45(1): 3-38. Inhibition of lysosomalα-mannosidase by Barbosa RC, Riet-Correa F, Medeiros RMT, Lima EF, swainsonine, an indolizidine alkaloid Barros SS, Gimeno JE, Molyneux RJ & isolated from Swainsona canescens. The Gardner DR (2006). Intoxication by Biochemical Journal, 191(2): 649-651. Ipomoea sericophylla and Ipomoeariedelii 7

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Dorling PR (1984). Lysosomal storage diseases in Tropical Animal Health & Production, 5(2): animals. In: Lysosomes in Biology and 119-123. Pathology (JT Dingle, RT Dean & W Sly, Oliveira-Júnior CA, Riet-Correa G, Lima E, Leite DM, editors) Elsevier, Amsterdam, The Pfister JA, Cook D & Riet-Correa F (2015). Netherlands. Pp 347-379. Feeding preferences of experienced and Driemeier D, Colodel EM, Gimeno EJ & Barros SS naïve goats and sheep for the toxic plant (2000). Lysosomal storage disease caused Ipomoea carnea subsp. fistulosa. Ciência by Sida carpinifolia poisoning in goats. Rural, 45(9), 1634-1640. Veterinary Pathology, 37(2): 153-159. Loretti AP, Colodel EM, Gimeno EJ & Driemeier D Gotardo AT, Pfister JA, Ferreira MB & Górniak SL (2003). Lysosomal storage disease in Sida (2011). Effects of prepartum ingestion of carpinfolia toxicosis: an induced Ipomoea carnea on postpartum maternal mannosidosis in horses. Equine Veterinary and neonate behavior in goats. Birth Journal, 35(5): 434-438. Defects Research Part B: Developmental Molyneux RJ & James LF (1982). Loco intoxication: and Reproductive Toxicology, indolizidine alkaloid of spotted locoweed doi: 10.1002/bdrb.20291. (Astragalus lentiginosus). Science, Gotardo AT, Schumaher BH, Pfister JA, Traldi AS, 216(4542): 190-191. Maiorka PC, Spinosa HS & Górniak SL Molyneux RJ, Pan YT & Goldmann A (1993). (2012). The Use of Ultrasonography to Calystegins, a novel class of alkaloid Study Teratogenicity in Ruminants: glycosidase inhibitors. Archives of Evaluation of Ipomoea carnea in Goats. Biochemistry & Biophysics, 304(1): 81-88. Birth Defects Research Part B: Molyneux RJ, James LF & Ralphs MH (1994). Developmental and Reproductive Polyhydroxy alkaloid glycosidase Toxicology, 95(4): 289–295. inhibitors from poisonous plants of global Goncalves ML (1987). Convolvulaceae- distribution: analysis and Cuscutaceae. In: Flora Zambesiaca, ed. identification. In: Plant-associated toxins: Launert E, vol. 8, Flora Zambesiaca Agricultural, phytochemical and Managing Committee, London, ecological aspects (SM Colegate & PR England. Pp 117-118. Dorling, editors) CAB International, Haraguchi M, Gorniak S, Ikeda K, Minami Y, Kato A, Wallingford, England. Pp 107-112. Watson AA, Nash R, Molyneuox RJ & Molyneux RJ, McKenzie RA, O’Sullivan BM & Elbein Asano N (2003). Alkaloidal components in AD (1995). Identification of glycosidase poisonous plant, Ipomoea carnea inhibitors swainsonine and calystegineB2 (Convolvulaceae). Journal of Agricultural in Weir Vine (Ipomoea sp. Q6 [aff. & Food Chemistry, 51(17): 4995-5000. calobra]) and correlation with toxicity. Hueza IM, Dagli ML, Gorniak SL & Paulino CA Journal of Natural Products, 58(6): 878- (2003). Toxic effects of prenatal Ipomoea 886. camea administration to rats. Veterinary Nath I & Pathak DC (1995). Induced Ipomoea & Human Toxicology, 45(6): 298-302. carnea toxicity in goats: clinical and Hueza IM, Guerra JL, Haraguchi M, Asano N & pathomorphological studies. Indian Gorniak SL (2005). The Role of alkaloids in Journal of Veterinary Pathology, 19: 19- Ipomoea carnea toxicosis: a study in rats. 21. Experimental & Toxicologic Pathology, Neiva A & Penna B (1916). Viagemcientificapelo 57(1): 53-58. Norte da Bahia, suboeste de Pernambuco, Huxtable CR, Dorling PR & Walkley US (1982). sul do Piauhi e de norte a sul de Goiaz. Onset and regression of neuroaxonal Memorias do Inst Oswaldo Cruz, 8:74-224. lesions in sheep with mannosidosis Radostits OM, Gay CC, Hinchcliff KW & Constable induced experimentally with swainsonine. PD (2006). Veterinary Medicine: A Acta Neuropathologica , 58(1): 27-33. Textbook of the diseases of cattle, horses Ikeda K, Kato A, Adachi I, Haraguchi M & Asano N sheep, pigs and goats, tenth edition. (2003). Alkaloids from the poisoning plant Saunders, Edinburgh. Pp 1870-1871, Ipomoea carnea: effects on intracellular 1949. lysosomal glycosidase activities in human Ríos EE, Cholich LA, Gimeno EJ, Guidi MG & de lymphoblast culture. Journal of Pérez OCA (2012). Experimental poisoning Agricultural & Food Chemistry, 51: 7642- of goats by Ipomoea carnea subsp. 7646. fistulosa in Argentina: a clinic and Idris OF, Tartour G, Adam SEI & Obeid HM (1973). pathological correlation with special Toxicity to goats of Ipomoea carnea. consideration on the central nervous 8

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system. Pesquisa Veterinária Brasileira, and castanospermine in rats. Veterinary 32(1): 37-42. Pathology, 32(3): 289-298. Schumaher-Henrique B, Goniak SL, Dagli ML & Stegelmeier BL, James LF, Panter KE, Ralphs MH, Spinosa HS (2003). The clinical, Gardner DR, Molyneux RJ & Pfister JA biochemical, haematological and (1999). The pathogenesis and pathological effects of long-term toxicokinetics of locoweed (Astragalus administration of Ipomoea carnea to and Oxytropis subsp.) poisoning in growing goats. Veterinary Research livestock. Journal of Natural Toxin, 8(1): Communications, 27(4): 311-319. 35-45. Stegelmeier BL, Ralphs MH, Gardner DR, Molyneux Stegelmeier BL, Molyneux RJ, Asano N Watson AA RJ & James LF (1994). Locoweed & Nash RJ (2008). Comparative pathology imoxication in range cattle and sheep: of the glycosidase inhibitors swainsonine, Serum α-mannosidase activity and castanospermine, and calystegines A3, clinicopathologic, In: Plant-associated B2, and C1 in mice. Toxicologic Pathology, toxins: Agricultural, phytochemical and 36(5): 651-659. ecological aspects (SM Colegate & PR Tirkey K, Yadava KP & Mandal TK (1987). Effect of Dorling, editors) CAB International, aqueous extract of Ipomoea carnea on Wallingford, England. Pp 501-506. the haematological and biochemical Stegelmeier BL, Molyneux RJ, Elbein AD & James LF parameters in goats. Indian Journal of (1995). The lesions of locoweed Animal Science. 57: 1019-1023. (Astragalus mollissimus), swainsonine,

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