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Mesocestoides corti in the rat: Comparisons of Mesocestoides corti infections in rats and mice
fnfernolronal Journolfor Printed in Great Briroin.
Parasitology
Vol. 14, No. 4, pp. 391-394.
1984 0
002&7519/&1/$3.00+0.00 Pergumon Press Ltd. Society/or Pwtrsitology
1984 Ausfrolicm
MESOCESTOIDES COR TI IN THE RAT: COMPARISONS OF MESOCESTOIDES COR TI INFECTIONS IN RATS AND MICE ANNE
M. BARTON,ELIZABETHA.WASHINGTON,AIMORNC.STEWART~~~
WARWICKL.NICHOLAS Department
of Zoology,
Australian
National
University,
GPO Box 4, Canberra,
A.C.T.
2601, Australia
(Received 19 August 1983) Abstract-BARTON A. M., WASHINGTON E. A., STEWART A. C. and NICHOLAS W. L. 1984. Mesocestoides corti in the rat: Comparisons of Mesocestoides corfi infections in rats and mice. Internotional Journalfor Parasitology 14: 391-394. Infections of M. corti in rats were compared with those in mice. The recoveries of parasites and their distribution were examined for 60 days after infection. During this period continuous and extensive multiplication occurred in mice. In rats there was an initial multiplication of tetrathyridia in the first 10 days followed by a decline in numbers. The relative distribution of tetrathyridia between the peritoneal cavity and liver was similar in both hosts. INDEX KEY WORDS:
Mesocestoides corti; tetrathyridia;
INTRODUCTION THE second larval stage or tetrathyridium of the North American cestode Mesocestoides corti, occurs naturally in the body cavities and viscera of a number of reptiles and mammals (Eckert, von Brand & Voge, 1969). The course of infection and the host’s response to the tetrathyridia have been studied extensively in laboratory mice. These can be infected orally by stomach tube, or by the more common experimental practice of injecting the tetrathyridia into the peritoneal cavity (Specht & Voge, 1965). In mice, the tetrathyridia enter the liver and begin to multiply within 10 days. Multiplication then continues in the peritoneal cavity until the mouse eventually dies, usually within a year of infection. Even though the mouse attains a degree of resisthe massive multiplication indicates an tance, inability to control the infection. A less permissive host could provide information about control mechanisms which are lacking in the mouse. There have been few reports of studies examining M. corti infections in hosts other than mice, but Specht & Voge (1965) noted that tetrathyridia could infect laboratory rats where they did not multiply as extensively as in mice. More recently, another group found that passaging the parasite through rats for 2 weeks affected the extent of its multiplication when returned to mice (Zodda & Thorson, 1982). In this paper we compare the course of M. corti infection in the rat with that in the mouse. We also examine the effect of the source of tetrathyridia, 391
rats; mice; multiplication.
whether from mice, rats or in vitro culture, outcome of infection in the subsequent host.
on the
MATERIALS AND METHODS The M. corti population was maintained in inbred CBA/H mice, and experimental studies were carried out in female CBA/H mice IO-14 weeks old at infection, or female Wistar rats which were IO-15 weeks old. The tetrathyridia were recovered from the peritoneal cavity of mice or rats and washed several times in sterile phosphate buffered saline (PBS). These were then transferred directly to the next host or first cultured in vitro. Tetrathyridia described as “from rats” were collected from mice and passaged through rats for 8 days before transfer to other experimental animals. Those destined for in vitro culture prior to transfer were collected aseptically and washed in saline containing 30 i.u. ml-l penicillin, 2.5 rg ml-t fungizone and 50 pg ml-t streptomycin sulphate. They were then cultured in Dulbecco’s Minimum Essential Eagle’s Medium (Commonwealth Serum Laboratories, Melbourne. Australia) in tissue culture flasks for 3 days at 37°C. Direct (Kawamura, 1969) and indirect (Weir, 1969) fluorescent antibody tests were used to detect host antigen on the tegument of parasites from mice and rats, and from in vitro cultures. Recipient animals were anaesthetised with ether and infected by intraperitoneal injection using an 18 gauge needle. Mice were given 20 tetrathyridia and rats were given 100 tetrathyridia to compensate for the difference in host body weight. Rats infected orally were anaesthetised and 100 tetrahyridia were administered in saline by stomach tube. The numbers of parasites present in experimental animals were determined 10, 20, 40 and 60 days after infection. Tetrathyridia were washed from the
ANNE
392
peritoneal cavity with PBS into a collecting dish, and those in the liver were recovered by macerating the organ then digesting it in 3% porcine pancreatin (5 x ) (Nutritional Biochemicals or Fluke AC Buchs SG) and 5% NaHC03 at 37°C. Mouse livers were incubated for between 1% and 2 h and rat livers for between 5l/2 and 6 h. The results were analysed using the Wilcoxon two sample test for unpaired samples (Sokal& Rohlf, 1969).
peritoneal cavities and livers appeared similar in both hosts (Fig. 1). After 10 days, the majority of parasites were recovered from the liver, while after 20 days, the distribution between peritoneal cavity and liver was about equal. At later time intervals, the majority were recovered from the peritoneal cavity. In oral infections of rats (Table 2), recoveries were very low, but parasites persisted for at least 40 days. The fluorescent antibody tests showed that antigens with characteristics of the host were present on the parasite’s tegument. These antigens were lost after 3 days in vitro. Rat antigens were lost from the tegument of rat tetrathyridia and replaced by mouse antigens 8 days after transfer from rat to mouse and vice versa. Figures 2 and 3 compare the recoveries of tetrathyridia from mice and rats respectively according to the origin of the parasites, ie. from the same or different host, or after in vitro culture. The recoveries were similar regardless of the parasites’ origin with one exception. Those rats infected with cultured tetrathyridia were significantly greater after 20 and 40 days, than recoveries from rats given parasites from either rats or mice.
RESULTS
The tetrathyridia of M. corti multiplied during the first 10 days of infection and invaded the livers of both rats and mice. In mice, the parasite continued to multiply throughout the period of investigation, but in rats the numbers of tetrathyridia declined by the 20th day and thereafter remained low (Table 1). No trace of dead or disintegrating parasites were found to account for the decline in recoveries at this stage. The difference in susceptibility of mice and rats is clearly evident in comparison of the degree of multiplication at each time interval (Table 1). Regardless of the multiplication differences the relative distribution of tetrathyridia between the
TABLE
~-RECOVERIES
OF M.
cord
Number
I.J.P.VOL.14. 1984
M. BARTON eta/.
TETRATHYRIDIA FROM MICE AND PERITONEALINJECTION
RATS INFECTED BY INTRA-
of tetrathyridia
(s.E.)
Days after infection
Number of animals per group
Mice infected 10 20 40 60
with 20 tetrathyridia 10 67.7 10 190.5 10 463.6 9 642.7
( 7.3)* (38.0)’ (60.0)* (58.3)*
26.8 94.3 373.0 416.2
( 3.5)* (18.3)* (49.7)* (50.81)*
40.9 96.2 90.6 226.5
( 5.9)?$ (20.5)t (17.4)$ (29.7):
3.39 9.53 23.18 32.14
Rats infected 10 20 40 60
with 100 tetrathyridia 9 154.2 10 55.4 9 80.8 5** 36.4
(23.6)* (11.6) ( 6.4fi( (13.9fil
30.6 27.0 62.0 28.4
( 3.4) ( 8.2) ( 5.0)* (14.2)
123.6 (22.3)* 28.4 ( 5.9)& 18.8 ( 3.9) 8.0( 3.7)s
1.54 0.55 0.81 0.36
Total
recovered-mean
Peritoneal cavity
Liver
Multiplication
Female CBA/H mice were infected with tetrathyridia taken from mice, and female Wistar were infected with tetrathyridia taken from rats. *Significantly different from all other values in the same column at p = 0.05. t*Q%ignificantly different from other means with same superscript at p = 0.05. **Original number of rats in this group was five.
Number of tetrathyridia recovered-mean (range)
Davs after infection
Number of animals per group
Total
10 20 40
10 10 8
11.9 (5-20) 13.7 (O-50) 18.4 (9-29)
Female Wistar rats were infected
Peritoneal cavity 1.9 (O-6) 0.9 (O-5) 0.75 (O-4)
with 100 tetrathyridia
Liver
10.0 (4-10) 12.8 (0.49) 17.6 (9-28) by stomach
tube.
Multiplication
0.12 0.14 0.18
rats
I.J.P.
VOL.
DISTRIBUTION
8 = 3
P
Comparison
14. 1984 OF
TETRATHYRIDIA
IN
MICE
AND
of M. corti infection
DISCUSSION
RATS
IRAT
FIG. 1. Percentage distribution of tetrathyridia the peritoneal cavity and liver in mice and rats; and 60 days after infection.
between 10, 20, 40
These results indicate that the rat is a less permissive host than the mouse, confirming observation by Specht & Voge (1965). Tetrathyridia can multiply in the rat, and in intraperitoneal infections, do so over the first 10 days. However, the number of parasites then declines and remains low. This is vastly different from the situation in mice where multiplication continues until the mouse dies. Rats can be infected orally, but there is no indication of the initial multiplication of tetrathyridia observed after intraperitoneal infections. However, low numbers of parasites do persist for at least 40 days. Specht & Voge (1965) found a similar result with oral infections in mice. In other respects, there are similarities in the course of infection in the two hosts. In both mice and rats, the parasite enters the liver within 10 days, and although numbers vary, the distribution of M corti between the peritoneal cavity and liver is similar in the two hosts. We found that the source of the parasites, whether from mice or rats, did not affect the outcome of infection at any time interval in the subsequent host. This differs from the results reported by Zodda & Thorson (1982) who noted that passaging tetrathyridia through male Wistar rats reduced the initial
nlOY%
FIG. 2. The number of parasites recovered from mice (2 s.E.) infected with tetrathyridia taken from the same host (mouse-mouse), different host (rat-mouse), or from in vitro culture (in vifro-mouse). The initial infection is indicated by the broken horizontal line.
393
in rats and mice
-
rat
,a, -
rat
,“.Yl,lO
74,
FIG. 3. The number of parasites recovered from rats (2 s.E.) infected with tetrathyridia taken from the same host (rat-rat), different host (mouse-rat), or from in vifro culture (in vitro-rat). The initial infection is indicated by the broken horizontal line.
394
ANNE M. BARTONet
multiplication in male ICR mice. After the third week though, they found that multiplication was greater in rat-mouse transfers than in mouse-mouse transfers. Zodda & Thorson (1982) present evidence suggesting the initial retardation in rat-mouse infections is due to the exchange of rat antigens on the parasite’s surface for mouse antigens, and that host antigens are continually acquired and lost. We have also noted the presence of host antigens associated with the tegument of M. corti, using direct and indirect immunofluorescence tests. In culture, we found such antigens were lost within 3 days and within 8 days in vivo. This formed the basis for our choice of times for in vitro cultures and primary passage through rats. However, even in rat-mouse transfers, where rat antigens were present, we did not observe any retardation in the parasites’ multiplication. It should be noted, however, that a different strain of mice and female rather than male hosts were used in our study. On the basis of present work, the significantly larger recoveries at 20 and 40 days from rats given cultured tetrathyridia are difficult to explain. The rat appears to be a good host for studying immune responses to the tetrathyridia of M. corti. It is a less permissive host than the mouse but the course of infection seems to be similar in other respects. Comparison of responses in the two rodents
I.J.P. VOL. 14. 1984
al.
may therefore provide clues as to why the mouse is unable to control the tetrathyridia’s multiplication. work was supported by a grant Trust Fund on the recommendation of the Australian Wool Corporation. Many thanks to Dr. M. J. Howell for commenting on the paper; Mr. I. Fox for printing figures and Mrs. D. Kjeldsen and Miss W. Lees for typing the manuscript.
Acknowledgements-This
from the Wool Research
ECKERT J., BRAND
multiplication
REFERENCES T. VON & VOGE M. 1969. Asexual
of Mesocestoides corti (Cestoda)
in the
intestine of dogs and skunks. Journal of Parasitology 55: 241-249. KAWAMURAA. JR. 1969.
Fluorescent Antibody Techniques and their Application. University of Tokyo Press, Baltimore.
SOKAL R. R. & ROHLF F. J. 1969.
Biometry. Freeman,
San Francisco. SPECHT D. & VOGE M.
1965. Asexual
multiplication
of
Mesocestoides corti tetrathyridia in laboratory animals. Journal of Parasitology 51: 268-272. WEIR D. M. 1969. Handbook of Experimental Immunology. Blackwell Scientific Publications, Oxford. ZODDA D. M. & THORSONR. E. 1982. In vivo and in vitro studies demonstrating the presence and turnover of host substances on the tegument of Mesocesfoides corti (Cestoda) tetrathyridia. Journal of Parasitology 68:
796-803.
Parasitology
Vol. 14, No. 4, pp. 391-394.
1984 0
002&7519/&1/$3.00+0.00 Pergumon Press Ltd. Society/or Pwtrsitology
1984 Ausfrolicm
MESOCESTOIDES COR TI IN THE RAT: COMPARISONS OF MESOCESTOIDES COR TI INFECTIONS IN RATS AND MICE ANNE
M. BARTON,ELIZABETHA.WASHINGTON,AIMORNC.STEWART~~~
WARWICKL.NICHOLAS Department
of Zoology,
Australian
National
University,
GPO Box 4, Canberra,
A.C.T.
2601, Australia
(Received 19 August 1983) Abstract-BARTON A. M., WASHINGTON E. A., STEWART A. C. and NICHOLAS W. L. 1984. Mesocestoides corti in the rat: Comparisons of Mesocestoides corfi infections in rats and mice. Internotional Journalfor Parasitology 14: 391-394. Infections of M. corti in rats were compared with those in mice. The recoveries of parasites and their distribution were examined for 60 days after infection. During this period continuous and extensive multiplication occurred in mice. In rats there was an initial multiplication of tetrathyridia in the first 10 days followed by a decline in numbers. The relative distribution of tetrathyridia between the peritoneal cavity and liver was similar in both hosts. INDEX KEY WORDS:
Mesocestoides corti; tetrathyridia;
INTRODUCTION THE second larval stage or tetrathyridium of the North American cestode Mesocestoides corti, occurs naturally in the body cavities and viscera of a number of reptiles and mammals (Eckert, von Brand & Voge, 1969). The course of infection and the host’s response to the tetrathyridia have been studied extensively in laboratory mice. These can be infected orally by stomach tube, or by the more common experimental practice of injecting the tetrathyridia into the peritoneal cavity (Specht & Voge, 1965). In mice, the tetrathyridia enter the liver and begin to multiply within 10 days. Multiplication then continues in the peritoneal cavity until the mouse eventually dies, usually within a year of infection. Even though the mouse attains a degree of resisthe massive multiplication indicates an tance, inability to control the infection. A less permissive host could provide information about control mechanisms which are lacking in the mouse. There have been few reports of studies examining M. corti infections in hosts other than mice, but Specht & Voge (1965) noted that tetrathyridia could infect laboratory rats where they did not multiply as extensively as in mice. More recently, another group found that passaging the parasite through rats for 2 weeks affected the extent of its multiplication when returned to mice (Zodda & Thorson, 1982). In this paper we compare the course of M. corti infection in the rat with that in the mouse. We also examine the effect of the source of tetrathyridia, 391
rats; mice; multiplication.
whether from mice, rats or in vitro culture, outcome of infection in the subsequent host.
on the
MATERIALS AND METHODS The M. corti population was maintained in inbred CBA/H mice, and experimental studies were carried out in female CBA/H mice IO-14 weeks old at infection, or female Wistar rats which were IO-15 weeks old. The tetrathyridia were recovered from the peritoneal cavity of mice or rats and washed several times in sterile phosphate buffered saline (PBS). These were then transferred directly to the next host or first cultured in vitro. Tetrathyridia described as “from rats” were collected from mice and passaged through rats for 8 days before transfer to other experimental animals. Those destined for in vitro culture prior to transfer were collected aseptically and washed in saline containing 30 i.u. ml-l penicillin, 2.5 rg ml-t fungizone and 50 pg ml-t streptomycin sulphate. They were then cultured in Dulbecco’s Minimum Essential Eagle’s Medium (Commonwealth Serum Laboratories, Melbourne. Australia) in tissue culture flasks for 3 days at 37°C. Direct (Kawamura, 1969) and indirect (Weir, 1969) fluorescent antibody tests were used to detect host antigen on the tegument of parasites from mice and rats, and from in vitro cultures. Recipient animals were anaesthetised with ether and infected by intraperitoneal injection using an 18 gauge needle. Mice were given 20 tetrathyridia and rats were given 100 tetrathyridia to compensate for the difference in host body weight. Rats infected orally were anaesthetised and 100 tetrahyridia were administered in saline by stomach tube. The numbers of parasites present in experimental animals were determined 10, 20, 40 and 60 days after infection. Tetrathyridia were washed from the
ANNE
392
peritoneal cavity with PBS into a collecting dish, and those in the liver were recovered by macerating the organ then digesting it in 3% porcine pancreatin (5 x ) (Nutritional Biochemicals or Fluke AC Buchs SG) and 5% NaHC03 at 37°C. Mouse livers were incubated for between 1% and 2 h and rat livers for between 5l/2 and 6 h. The results were analysed using the Wilcoxon two sample test for unpaired samples (Sokal& Rohlf, 1969).
peritoneal cavities and livers appeared similar in both hosts (Fig. 1). After 10 days, the majority of parasites were recovered from the liver, while after 20 days, the distribution between peritoneal cavity and liver was about equal. At later time intervals, the majority were recovered from the peritoneal cavity. In oral infections of rats (Table 2), recoveries were very low, but parasites persisted for at least 40 days. The fluorescent antibody tests showed that antigens with characteristics of the host were present on the parasite’s tegument. These antigens were lost after 3 days in vitro. Rat antigens were lost from the tegument of rat tetrathyridia and replaced by mouse antigens 8 days after transfer from rat to mouse and vice versa. Figures 2 and 3 compare the recoveries of tetrathyridia from mice and rats respectively according to the origin of the parasites, ie. from the same or different host, or after in vitro culture. The recoveries were similar regardless of the parasites’ origin with one exception. Those rats infected with cultured tetrathyridia were significantly greater after 20 and 40 days, than recoveries from rats given parasites from either rats or mice.
RESULTS
The tetrathyridia of M. corti multiplied during the first 10 days of infection and invaded the livers of both rats and mice. In mice, the parasite continued to multiply throughout the period of investigation, but in rats the numbers of tetrathyridia declined by the 20th day and thereafter remained low (Table 1). No trace of dead or disintegrating parasites were found to account for the decline in recoveries at this stage. The difference in susceptibility of mice and rats is clearly evident in comparison of the degree of multiplication at each time interval (Table 1). Regardless of the multiplication differences the relative distribution of tetrathyridia between the
TABLE
~-RECOVERIES
OF M.
cord
Number
I.J.P.VOL.14. 1984
M. BARTON eta/.
TETRATHYRIDIA FROM MICE AND PERITONEALINJECTION
RATS INFECTED BY INTRA-
of tetrathyridia
(s.E.)
Days after infection
Number of animals per group
Mice infected 10 20 40 60
with 20 tetrathyridia 10 67.7 10 190.5 10 463.6 9 642.7
( 7.3)* (38.0)’ (60.0)* (58.3)*
26.8 94.3 373.0 416.2
( 3.5)* (18.3)* (49.7)* (50.81)*
40.9 96.2 90.6 226.5
( 5.9)?$ (20.5)t (17.4)$ (29.7):
3.39 9.53 23.18 32.14
Rats infected 10 20 40 60
with 100 tetrathyridia 9 154.2 10 55.4 9 80.8 5** 36.4
(23.6)* (11.6) ( 6.4fi( (13.9fil
30.6 27.0 62.0 28.4
( 3.4) ( 8.2) ( 5.0)* (14.2)
123.6 (22.3)* 28.4 ( 5.9)& 18.8 ( 3.9) 8.0( 3.7)s
1.54 0.55 0.81 0.36
Total
recovered-mean
Peritoneal cavity
Liver
Multiplication
Female CBA/H mice were infected with tetrathyridia taken from mice, and female Wistar were infected with tetrathyridia taken from rats. *Significantly different from all other values in the same column at p = 0.05. t*Q%ignificantly different from other means with same superscript at p = 0.05. **Original number of rats in this group was five.
Number of tetrathyridia recovered-mean (range)
Davs after infection
Number of animals per group
Total
10 20 40
10 10 8
11.9 (5-20) 13.7 (O-50) 18.4 (9-29)
Female Wistar rats were infected
Peritoneal cavity 1.9 (O-6) 0.9 (O-5) 0.75 (O-4)
with 100 tetrathyridia
Liver
10.0 (4-10) 12.8 (0.49) 17.6 (9-28) by stomach
tube.
Multiplication
0.12 0.14 0.18
rats
I.J.P.
VOL.
DISTRIBUTION
8 = 3
P
Comparison
14. 1984 OF
TETRATHYRIDIA
IN
MICE
AND
of M. corti infection
DISCUSSION
RATS
IRAT
FIG. 1. Percentage distribution of tetrathyridia the peritoneal cavity and liver in mice and rats; and 60 days after infection.
between 10, 20, 40
These results indicate that the rat is a less permissive host than the mouse, confirming observation by Specht & Voge (1965). Tetrathyridia can multiply in the rat, and in intraperitoneal infections, do so over the first 10 days. However, the number of parasites then declines and remains low. This is vastly different from the situation in mice where multiplication continues until the mouse dies. Rats can be infected orally, but there is no indication of the initial multiplication of tetrathyridia observed after intraperitoneal infections. However, low numbers of parasites do persist for at least 40 days. Specht & Voge (1965) found a similar result with oral infections in mice. In other respects, there are similarities in the course of infection in the two hosts. In both mice and rats, the parasite enters the liver within 10 days, and although numbers vary, the distribution of M corti between the peritoneal cavity and liver is similar in the two hosts. We found that the source of the parasites, whether from mice or rats, did not affect the outcome of infection at any time interval in the subsequent host. This differs from the results reported by Zodda & Thorson (1982) who noted that passaging tetrathyridia through male Wistar rats reduced the initial
nlOY%
FIG. 2. The number of parasites recovered from mice (2 s.E.) infected with tetrathyridia taken from the same host (mouse-mouse), different host (rat-mouse), or from in vitro culture (in vifro-mouse). The initial infection is indicated by the broken horizontal line.
393
in rats and mice
-
rat
,a, -
rat
,“.Yl,lO
74,
FIG. 3. The number of parasites recovered from rats (2 s.E.) infected with tetrathyridia taken from the same host (rat-rat), different host (mouse-rat), or from in vifro culture (in vitro-rat). The initial infection is indicated by the broken horizontal line.
394
ANNE M. BARTONet
multiplication in male ICR mice. After the third week though, they found that multiplication was greater in rat-mouse transfers than in mouse-mouse transfers. Zodda & Thorson (1982) present evidence suggesting the initial retardation in rat-mouse infections is due to the exchange of rat antigens on the parasite’s surface for mouse antigens, and that host antigens are continually acquired and lost. We have also noted the presence of host antigens associated with the tegument of M. corti, using direct and indirect immunofluorescence tests. In culture, we found such antigens were lost within 3 days and within 8 days in vivo. This formed the basis for our choice of times for in vitro cultures and primary passage through rats. However, even in rat-mouse transfers, where rat antigens were present, we did not observe any retardation in the parasites’ multiplication. It should be noted, however, that a different strain of mice and female rather than male hosts were used in our study. On the basis of present work, the significantly larger recoveries at 20 and 40 days from rats given cultured tetrathyridia are difficult to explain. The rat appears to be a good host for studying immune responses to the tetrathyridia of M. corti. It is a less permissive host than the mouse but the course of infection seems to be similar in other respects. Comparison of responses in the two rodents
I.J.P. VOL. 14. 1984
al.
may therefore provide clues as to why the mouse is unable to control the tetrathyridia’s multiplication. work was supported by a grant Trust Fund on the recommendation of the Australian Wool Corporation. Many thanks to Dr. M. J. Howell for commenting on the paper; Mr. I. Fox for printing figures and Mrs. D. Kjeldsen and Miss W. Lees for typing the manuscript.
Acknowledgements-This
from the Wool Research
ECKERT J., BRAND
multiplication
REFERENCES T. VON & VOGE M. 1969. Asexual
of Mesocestoides corti (Cestoda)
in the
intestine of dogs and skunks. Journal of Parasitology 55: 241-249. KAWAMURAA. JR. 1969.
Fluorescent Antibody Techniques and their Application. University of Tokyo Press, Baltimore.
SOKAL R. R. & ROHLF F. J. 1969.
Biometry. Freeman,
San Francisco. SPECHT D. & VOGE M.
1965. Asexual
multiplication
of
Mesocestoides corti tetrathyridia in laboratory animals. Journal of Parasitology 51: 268-272. WEIR D. M. 1969. Handbook of Experimental Immunology. Blackwell Scientific Publications, Oxford. ZODDA D. M. & THORSONR. E. 1982. In vivo and in vitro studies demonstrating the presence and turnover of host substances on the tegument of Mesocesfoides corti (Cestoda) tetrathyridia. Journal of Parasitology 68:
796-803.