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Studies on the population kinetics and pathology of experimental Trichostrongylus Colubriformis (Giles, 1892) infections in lambs

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ChiejinaSN_1972redux.pdf (48.37Mb)
Date
1972
Author
Chiejina, Samuel Nnagbo
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Abstract
 
 
The host -parasite relationship of sheep and the nematode Trichostrongylus colubriformis was studied in terms of the population dynamics of the parasite in the host and the pathological and pathophysiological outcome of such a relationship.
 
Two different patterns of prolonged daily infections which were intended to simulate two distinct epidemiological situations, and a limited number of single infections were used. The course of the infections was monitored by means of regular faecal egg counts, differential post -mortem worm counts, determination of plasma or serum protein changes and measurement of gastrointestinal plasma loss. At the completion of each of the experiments suitable infected and worm -free lambs were used to study the macroscopic, histological and ultra - structural changes in the mucosa of the proximal small intestine.
 
It was shown that the trend in the faecal egg counts of lambs exposed from early post -natal life to an escalating infection with T.colubriformis followed a characteristic pattern. Faecal egg counts increased logarithmically during the first 12 weeks of exposure to this pattern of infection. The egg count curve thus reflected the pattern of infection during most of this period. In most lambs the peak egg count which was reached soon after the 12th week was maintained for the rest of the experimental period. There was no evidence of an abrupt decline in faecal egg counts.
 
The population of T.colubriformis in these lambs increased steadily to a peak of about 100,000 worms by the 16th week. This large burden remained fairly stable for the rest of the experimental period despite repeated daily infections or a single heavy challenge infection. During this period exsheathed infective larvae of T.colubriformis could be recovered from the freshly - collected faeces of the lambs especially within 24 to 48 hours after the challenge infection. It thus appears that the early exposure of the lambs to T.colubriformis infections did not result in the lambs tolerating re- infection by this parasite but instead conferred strong resistance to a heavy challenge infection which produced clinical disease in previously uninfected worm -free controls of similar age. There was no evidence that the populations of T.colubriformis in these lambs were regulated by either self -cure reactions or by a mechanism involving continual and rapid turnover of worms.
 
The faecal egg count of older lambs infected daily with 5,000 larvae of T.colubriformis was also characteristic. Egg counts rose rapidly to a peak 28 to 40 days after first infection and then declined exponentially at a rate which varied with the individual lamb and its age.
 
As in the younger lambs the infection appeared to be cumulative during the first 4 weeks when the numbers of worms which succeeded in establishing themselves in the lambs far exceeded those being lost. Thereafter the rate of increase in worm populations was reduced as the host became increasingly more resistant tothe establishment of new infections. Prom about the 10th week onwards most lambs were virtually totally refractory to either the continued daily infections or to a single heavy challenge infection. Large numbers of exsheathed infective larvae of T.colubriformis could be recovered from freshly- collected faeces of such lambs.
 
In most lambs a peak worm burden of 90,000 to 100,000 was reached by the 8th week after first infection. In some lambs this peak burden remained fairly stable for about 4 weeks before an apparently exponential decline occurred. In more resistant lambs, however, this decline commenced soon after the peak burden was reached.
 
Four manifestations of acauired resistance were observed in most lambs following prolonged daily infections with T.colubriformis, namely: - 1. Resistance to the establishment of new infections 2. Inhibition of ovulation of female worms 3. Stunting of adult worms 4. An exponential loss of worms
 
It is concluded that the immunological control of T.colubriformis infections in lambs under conditions of continual re- infection is achieved through these phenomena which are probably separate and distinct aspects of the host resistance mechanism.
 
T,colubriformis infections in lambs were often accompanied by a marked hypoproteinaemia which was essentially a hypoalbuminaemia, the magnitude of which was directly related to the severity of the disease. Radiotracer studies showed that a protein- losing enteropathy was the most probable cause of the hypo - proteinaenia. This daily leakage of plasma into the gut was not accompanied by the loss of red blood cells.
 
The intestinal plasma loss was a sensitive index of the pathogenicity of T.colubriformis, in lambs. Furthermore a significant positive correlation was found between the worm burden of the lambs and their terminal intestinal plasma loss. The prolonged leakage of plasma proteins into the gut at an excessive rate constitutes a derangement of the host's plasma protein metabolism and probably has important physiological and biochemical consequences to the parasitized lamb.
 
Regular monitoring of the gastro- intestinal plasma loss of Iambs during prolonged infections was made possible by the development of a new method for the in -vivo labelling of plasma proteins, in which ⁵¹Cr as ⁵¹CrCl₃ was administered subcutaneously in a water -in -oil emulsion. A simple but reliable in-vitro test system was also devised and used to evaluate various emulsions for their rate of release of ⁵¹Cr. Both the in-vitro and in-vivo tests showed that the most satisfactory emulsions for use in the measurement of gastro- intestinal plasma protein leakage in lambs would be those with the following compositions : -
 
1. Arlacel A concentration of 8 to 12 percent
 
2. Phase volume of 35 to 50 percent and
 
3. Tween 80 concentration of 0 to 5 Percent
 
The macroscopic, histological and ultrastructural features of the mucous membrane of the -proximal small intestine of lambs with trichostrongylosis were remarkably similar to those commonly seen in malabsorption syndromes in man. The most notable feature was marked stunting of the villi or, in severe cases, total loss of villi. These findings support the suggestions of other workers who have found similar chances in a variety of aetiologically unrelated conditions in man and animals that these changes arc a non -specific reaction of the small intestinal mucosa to damaging agents. The significance of these morphological changes in intestinal physiological functions in lambs, especially digestion and absorption, is uncertain.
 
No evidence was found from the ultrastructural studies to suggest that defects in the zonulae occludentes between adjacent epithelial cells were responsible for the increased permeability of the parasitized mucous membrane to plasma proteins. It is considered more probable that the areas of epithelial erosion and ulceration which were demonstrated histologically and ultrastructurally were the sites of the increased plasma protein leakage into the gut. Such mucosal damage is more likely to be caused directly by the parasite rather than by pharmacologically active substances. It is therefore improbable that a mechanism which involves a local anaphylactic reaction leading to increased gut permeability to plasma proteins is important in the regulation of populations of T.colubriformi s in most lambs. However the kinetics of the worm populations in two of the experimental lambs suggested that such a mechanism might have been involved in the relatively rapid expulsion of worms which occurred in these lambs.
 
URI
http://hdl.handle.net/1842/27785
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