TOXICOLOGICAL EVALUATION OF THE PLANT Xanthium strumarium IN PIGS IN ZIMBABWE

Original paper

TOXICOLOGICAL EVALUATION OF THE PLANT Xanthium strumarium IN PIGS IN ZIMBABWE

C. MASVINGWE

, M. MAVENYENGWA

1 Preclinical Veterinary Studies, Faculty of Veterinary Science, University of Zimbabwe, Box MP167, Mount Pleasant, Harare, Zimbabwe, 2 Central Veterinary Research & Diagnostic Laboratory, Box CY 551, Causeway, Harare, Zimbabwe.

ABSTRACT: Six healthy porkers of the Mukota breed were fed ad libitum either crushed burs (fruits) or the two-leaf seedling stage of Xanthium strumarium at 2% of body weight.

Major clinical signs were depression, vomiting, abdominal pain, weakness, recumbency, paddling convulsions terminating in death from 6 to 96 hours after ingestion. Gross pathological findings included ascites with fibrin strands, enlarged, congested and friable livers with accentuation of lobulation on the capsule. Microscopically, acute hepatic congestion and hemorrhage, centrilobular hepatocyte necrosis, with occasional binucleation together with discoid lysis of skeletal and cardiac muscle fibers were remarkable changes. Binucleation of hepatocytes and degenerative changes in active muscles have not been reported before in relation to cocklebur plant toxicosis.

These findings suggest that X. strumarium is a potential cause of sudden death in pigs extensively reared in Zimbabwe.

KEY WORDS: Xanthium strumarium toxicosis, hepatocyte necrosis, striated muscle fiber and renal tubular degeneration, Zimbabwe.

INTRODUCTION

Xanthium strumarium is often found on wastelands, roadsides and pastures which are subject to occasional flooding. It has been recognized to cause losses in cattle (6,7,9), goats (9), pigs (1,7,8) sheep (8) and diminished weight gain in poultry (3). The clinical signs and macroscopic and microscopic lesions in pigs and cattle have been described (1,5,8).

The toxic principle of X. strumarium is a sulfated glycoside, carboxyatractyloside, found in the seeds and the two-leaf seedling stage (1,4,8). The mature plant is reported as non-toxic (1), although toxicosis has been reported in cattle which had ingested mature plants with burs (9) despite the general belief that ingestion of burs should be limited by mechanical injury during mastication.

X. strumarium is widely distributed in Zimbabwe where it is often found as a noxious weed on maize fields, along roadsides, wastelands and around cattle kraals. It is known to occur on the sandy river beds in the Matebeland province where it would be accessible to extensively reared pigs and cattle and be responsible for intoxication of these animals. However, because the toxicity of this plant is largely unknown in this country, it has not been implicated for causing livestock losses.

The aim of this study was to determine whether X. strumarium occurring in Zimbabwe had the toxic potential ascribed to cocklebur species in Australia, North America, and Yugoslavia as described by other workers (1,7) and to explore differences, if any, in the distribution of the pathological lesions.

MATERIALS AND METHODS

The experiment was conducted in two phases to evaluate the effect of the burs and the two-leaf seedlings of X. strumarium, which are the plant stages known to contain the toxic principle.

PHASE 1. Mature burs were collected from a maize field soon after harvesting. The burs were crushed and fed ad libitum to two healthy porkers of the extensively reared indigenous pigs of the Mukota breed, in community, at 2% of the total body weight. The dose ingested by each pig was, therefore, not controllable.

PHASE 2. The burs were allowed to dry over winter and spring and then germinated. Seedlings were harvested at the two-leaf stage and frozen until the adequate amounts were collected. The seedlings were then thawed and fed ad libitum to four healthy porkers of the same breed at 2% of the total body weight as described for phase 1.

In experiment phase 1, one pig fed the crushed burs was placed on a normal diet after it had survived 24 hours of exposure. All animals were allowed water ad libitum at all times. Animals were closely monitored for clinical signs every hour for the first 12 hours. The pig that survived 24 hours of exposure to burs was, thereafter, monitored every 3 hours. All the pigs were necropsied after death. At each necropsy, tissue samples from the liver, kidney, heart, spleen, tongue, Longissimus dorsi, intestine and brain were collected and fixed in 10% buffered formalin. Formalized tissues were routinely processed following standard techniques and stained with hematoxylin and eosin

RESULTS

All the animals showed clinical signs of depression, dyspnea, ataxia, a staggering gait, circling, lateral recumbency with convulsive paddling movements of the legs, terminating in coma and death. Progression of clinical signs was slowest in the single pig fed burs that died after 96 hours. The other pig had died after 11 hours, while all 4 pigs fed the two-leaf seedlings died between 6 and 12 hours after exposure. Mortality was 100% in both studies.

At post-mortem examination, all the pigs had ascites with fibrin strands, enlarged, congested and friable livers with accentuation of lobulation on the capsule. The gall bladder walls were edematous. Ecchymotic epicardial hemorrhages and dark discoloration of the myocardium were observed. Hemorrhagic duodenitis, involving the pylorus was seen in both pigs fed burs and 2 pigs fed seedlings. The stomachs of pigs fed crushed burs were distended with gas.

On microscopic examination, the livers showed diffuse acute congestion and hemorrhage, centrilobular necrosis, reactive Kupffer cells and occasional binucleation of hepatocytes (Figure 1). Moderate fatty change of the liver was also present in the pig that died 96 hours after exposure. Myocardial and endocardial congestion and edema with granular degeneration of myofibers were observed. Zenker's necrosis with complete dissolution of some skeletal muscle fibers was consistently present, and more severe on the tongue (Figure 2). Sections of the Longissimus dorsi examined had no histopathological changes. Changes in the kidneys comprised cortical congestion and cytogenic edema of tubular epithelial cells with hyalin casts formation in the tubular lumen. The brain showed congestion, hemorrhage and degeneration of neurons in the cerebellum.

DISCUSSION

This study, although limited by availability of experimental animals and housing facilities preventing inclusion of control groups and individualized housing, respectively, has provided valuable information to the farming community of Zimbabwe where the toxicity of cockleburs was hitherto unknown.

Clinical signs, macroscopic and microscopic findings in this study are similar to those described in literature (1,2,5,8) with the exception of the severe degenerative changes in the active striated muscles of the tongue and heart. Carboxyatractyloside has been positively identified as the toxic principle in cockleburs (8). It is most probable that X. strumarium occurring in Zimbabwe also contains carboxyatractyloside accounting for the lesions described herein and in agreement with the pathology already published (8). Luciani et al. (5) and Witte et al. (9) described the mechanism of toxicity of carboxyatractyloside as an inhibitor of oxidative phosphorylation and translocation of adenine nucleotides across mitochondrial membranes. Therefore, it is expected to affect organs receiving a high blood supply corresponding to the metabolic demand. This study, has shown that active skeletal muscles such as the tongue are affected while less active muscles as the Longissimus dorsi are spared. The degenerative changes in striated muscle of the tongue and heart and binucleation of hepatocytes have not been reported previously.

In this study, hemorrhagic gastroenteritis in both groups of pigs seems to confirm the findings of Witte et al. A longer lag period between ingestion and death was observed in pigs fed crushed burs (11-96 hours) than those fed seedlings (6-12 hours). This could be attributed to the time required to release the toxin out of the burs (8).

This study shows that X. strumarium occurring in Zimbabwe is as toxic as cockleburs occurring in Australia, North America, and Yugoslavia. This plant should, therefore, be considered a differential for cases of sudden death in extensively reared pigs where acute centrilobular hepatocyte necrosis and hemorrhage dominate the histopathological findings.

ACKNOWLEDGEMENTS

We acknowledge, with thanks, the technical assistance of Messrs. S. Mavi at the National Herbarium at Harare, W. Shumba, E. Muradzikwa, S. Gowe, R. Tewe and E. Marumani. The critical suggestions from Prof. K. Mohan during the preparation of the manuscript are sincerely appreciated. We are indebted to the Department of Veterinary Services for the provision of experimental animals and processing of tissues and to the University of Zimbabwe Research Board for financial assistance.

FIGURE 1. The liver: binucleation of hepatocytes.

FIGURE 2.
The tongue showing Zenker's necrosis and complete dissolution of muscle fibres.

REFERENCES

Received 24 March 1997

Accepted 24 November 1997

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• 08 STUART BP., COLE RJ., GOSSER HS. Cocklebur (Xanthium strumarium L. var. strumarium) intoxication in swine: review and redefinition of the toxic principle. Vet. Pathol., 1981, 18, 368-83.
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CORRESPONDENCE TO:

C. MASVINGWE - Department of Preclinical Veterinary Studies, Faculty of Veterinary Science, University of Zimbabwe, Box MP167, Mount Pleasant, Harare, Zimbabwe.

Publication Dates

• Publication in this collection
  26 Nov 1998
• Date of issue
  1998

History

• Received
  24 Mar 1997
• Accepted
  24 Nov 1997