T H E AMERICAN JOURNAL OF CLINICAL PATHOLOGY
Vol. 37, No. 5, pp. 470-474
May, 1962
Copyright © 1962 by The Williams & Wilkina Co.
Printed in U.S.A.
T H E ABSENCE OF E O S I N O P H I L S IN RATS INFECTED WITH RADIATED
TRICHINELLA
SPIRALIS
VITO SCARDINO, M.D., AND HERMAN ZAIMAN, M.D.
WITH THE TECHNICAL ASSISTANCE OF JUSTO DIAZ
Department of Pathology, Albert Einstein College of Medicine, Yeshiva University,
New York 61, New York
The occurrence of eosinophilia in human
and experimental trichinosis is well known
and has recently been reviewed by Gould.1
Whether the eosinophilia is initiated by the
maturing or adult nematodes, or both,
within the intestine or by the second generation larvae remains unknown. Inasmuch as
neither of these possibilities necessarily excludes the other, it is conceivable that both
stages are eosinophilogenic. The experiments
described here were designed to investigate
the eosinophilic response of rats subjected
to trichinous infections limited to the intestine. This is made possible by the fact
that exposure of Trichinella spiralis larvae
to appropriate doses of roentgen radiation
eliminates their reproductive capacity. In
the absence of a second generation, the infection is limited to the intestine. 4 ' 6
E X P E R I M E N T A L STUDY
Procedures
Holtzman rats, housed in individual cages,
fed Purina Lab. Chow,* and given water ad
libitum, were used in these experiments.
Larvae for infection were procured from
rats infected with Trichinella spiralis approximately 2 months earlier. The rats were
sacrificed, skinned, and eviscerated. The
carcasses were ground up and digested in a
solution of 1 per cent pepsin and 0.5 per cent
concentrated hydrochloric acid, which was
continually agitated by bubbling air. After
Received, October 25, 1961; accepted for publication February 7, 1962.
Dr. Scardino was Chief Resident in Pathology,
and he is presently Visiting Instructor in Pathology. Dr. Zaiman is Assistant Professor of
Pathology (Parasitology).
This work was supported by Grant No. E-2G12
from the National Institutes of Health.
* Ralston-Purina
Company,
Saint
Louis,
Missouri.
470
digestion at 37 C. for 12 hr., the mixture was
passed through a metal strainer (20 meshes
per square inch). The larvae were washed
with tap water several times by means of
decantation.
For inoculation, an appropriate volume of
a suspension of worms (determined previously by dilution counts) was placed in
15-ml. centrifuge tubes. Having settled, the
larvae were drawn into a tapered glass pipet
fitted with a rubber bulb. The pipet was
introduced deep into the esophagus of the
anesthetized (ether) rat and the larvae
deposited therein by means of compressing
the rubber bulb.
Radiation was provided by a 250-kv.
Westinghouse Duocondex machine. The irradiation factors were as follows: 250 kv.,
15 ma., a half-value layer of 1.5 mm. of Cu.
The larvae were divided into aliquots and
were placed 18.5 cm. from the source of the
roentgen rays; they received the radiation
at the rate of 785 r per min. Larvae were irradiated with either 12,000, 16,000, or
20,000 r of roentgen rays. The specific
amounts will be indicated for each group.
Nonirradiated larvae were also used for
infection.
Eosinophils were counted by means of a
direct method, as follows: each rat was put
in a small cylindrical metal cage; its tail was
cut, the first drop of blood was wiped off,
and subsequent drops of blood were drawn
into a white blood cell pipet to mark 1. The
pipet was then filled with diluting fluidf to
mark 2. The pipet was shaken for 2 min. and
permitted to settle for 3 min. It was again
agitated for at least 1 min. before the chambers of a Neubauer bright-line hemocytomf The diluting fluid was made up fresh by
mixing 1 part of a stock solution of phloxine, 0.1
per cent in propylene glycol, with 2 parts of
distilled water.
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CHINE
472
Vol. 37
SCARDINO AND ZAIMAN
4050
GROUP A, NO LARVAE
GROUP B, NON-IRRADIATED LARVAE
GROUP C, IRRADIATED) 12,000r) LARVAE
GROUP D, IRRADIATED (I 6,000r) LARVAE
GROUP E, IRRADIATED (20,000r) LARVAE
TOTAL NUMBER OF RATS - 25
NUMBER OF RATS IN EACH GROUP-5
EACH POINT USUALLY REPRESENTS THE
MEAN OF THE 5 RATS IN THE SPECIFIC GROUP
£ 3750
LJ 3450
•J 3150
^ 2850O 2550-
5 2250o
(j. 1950
u
CL 1650
|3 I 3 5 0 -
a 1050
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8
750
45
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150-
' I ' I ' I ' I' I M ' I' I ' I ' I ' I' I' I I I
I ! ! ' I
4 6 8 10 12 14 16 18 2 0 2 2 2 4 2 6 2 8 3 0 3 2 3 5 3 7 3 9 4 1 4 3 4 5
49 52 54 56 59
DAYS
FIG. 1. Levels of circulating eosinophils per cubic millimeter of tail blood in adult rats
infected with 6000 nonirradiated or irradiated (roentgen rays) Trichinella spiralis larvae.
eter were filled. T h e total number of
eosinophils in each of the 9 large squares in
both chambers was counted and the average
number multiplied by 200 and divided by 18.
I n reality, they were simply multiplied by 11,
which is equivalent to 200 divided by 18.
T h e results were reported in cubic millimeters of blood.
I n order to determine the n u m b e r of
muscle larvae present in any rat, its skinned,
eviscerated carcass was digested in pepsin
and hydrochloric acid, as outlined above.
T h e volume of the water containing the
total number of washed worms released by
digestion was brought to 500 ml., and counts
were made on aliquots. T h e mean number of
larvae observed per millimeter was multiplied by 500, in order to determine the total
number of larvae present. When few larvae
were found in a digest, the number and size
of the aliquots searched were increased and
appropriate factors were used for multiplication.
sham infection consisting of 2 ml. of t a p
water per os. Each of the nits in group B
was infected with 0000 nonirradiated larvae.
T h e rats in groups C, D , and E each received
6000 irradiated larvae. Larvae given to rats
in group C received 12,000 r, those used to
inoculate group 1) received 16,000 r, and
those used for infection of group E received
20,000 r.
Eosinophils were counted at frequent
intervals. A prcinfection count was made and
recorded as day zero. From the 3rd to the
28th day of infection, eosinophil counts were
made on a daily basis. Thereafter, they wero
made with less frequency but usually on
alternate days with few exceptions. These
can readily be determined by reference to
Table 1.
T h e experiment was terminated 59 days
after infection. All surviving animals were
sacrificed, skinned, eviscerated, and digested; and the total number of worms present in their musculature was determined.
Protocol
RESULTS
Twenty-five young adult rats, each weighing 200 or more Gm., were divided into 5
equal groups, each consisting of 4 males and
1 female. Each rat in group A received a
The eosinophil counts are listed in Table 1
and Figure J. 7'jxamination of the data revealed the following:
1. A conspicuous cosinophilia was dc-
May 1962
TRICHINELLA
SPIRALIS
TABLE 2
T H E N U M B E R O F LARVAE R E C O V E R E D BY M E A N S
OF D I G E S T I O N O F CARCASSES OF R A T S INOCULATED P E R Os W I T H 6000 T B I C H I N E L L A LARVAE
SUBJECTED TO V A R I O U S D O S E S O F R O E N T G E N
RAYS
Rat Number
A-l
A-2
A-3
A-4
A-5
B-1
B-2
B-3
B-4
B-5
Number of Larvae Recovered
0
0
0
0
0
220,000
250,000
620,000 > Average
75,000 294,000
325,000
473
INFECTION
3. Those rats which were infected by
larvae irradiated with 20,000 r did indeed
develop an eosinophilia which was first noted
on the 14th day, and peaked twice with an
intervening trough. The peak eosinophil
counts were 1310 (tolls per cu. mm. on the
15th day and 1135 cells per cu. mm. on
day 23.
Table 2 records the number of larvae recovered by means of digestion of the rat
carcasses at the conclusion of the experiment. From the table it is readily apparent
that those groups which harbored no muscle
larvae revealed no eosinophilia. It is also apparent that radiation at 20,000 r did not
guarantee reproductive sterilization of the
Trichinella used to infect the rats in group E.
DISCUSSION
C-1
C-2
C-3
C-4
C-5
0
0
0
0
0
D-l
D-2
D-3
D-4
D-5
0
0
0
0
0
E-1
E-2
E-3
E-4
E-5
15,000'
500
3,500 Average
200 4140
1,500
veloped by those rats which were infected
with nonradiated larvae. Starting on the 5th
or 6th day of infection, the eosinophil counts
rose to an average peak of 3840 cells per cu.
mm. on the 10th day of infection. Thereafter, it declined in an irregular fashion to
reach preinfection levels on the 59th day of
infection. A second peak of 2300 cells was
observed on the 32nd day of infection.
2. The number of eosinophils counted in
the tail blood of those rats which received
sham infections (group A) or infection with
larvae subjected to 12,000 r (group C) or
16,000 r (group D) remained fairly stable
around preinfection levels. At no time did
they demonstrate a clear-cut eosinophilia.
The infectivity of the nonradiated larvae
was demonstrated by the recovery of an
average of 294,000 muscle larvae from each
of the rats in group B.
Conversely, the fact that no larvae were
recovered from the carcasses of the rats in
groups C and D demonstrated that sterilization had indeed been achieved by radiation
of the larvae used for infecting these animals.
It was especially disconcerting to recover
muscle larvae from the rats in group E, inasmuch as the larvae used to infect these rats
were supposed to have been subjected to the
highest radiation dosage used. Inasmuch as
it is inconceivable that increased radiation
would have less sterilizing effect than
smaller doses, a breach in technic was
implied.
The fact that eosinophilia failed to develop in those rats which harbored no
muscle trichiiiellac suggested that the second
generation larvae were of special significance in initiating the eosinophilic response
of its host, the rat. It was particularly significant that the onset of eosinophilia, as
here recorded, closely coincided with the
known onset of migration 2 ' 3 by the second
generation larvae. Coincidence in time,
however, is not proof of a cause and effect
relation. Moreover, Pollay and associates6
have reported eosinophilia in rats as early as
3 days after infection.
The possibility that qualitative or quanti-
474
Vol. 37
SCARDINO AND ZAIMAN
tative damage, or both, was done to eosinophilogenic centers of the intestinal nematode has not been ruled out.
Inasmuch as a potent immune response is
stimulated by infection with irradiated
Trichinella*-6 the data suggest that the immune response may not be dependent on a
rise in the eosinophils found in tail blood.
tingeva un culmine de 3 cellulas per mm 3
le 14te die, e postea illo declinava in un
maniera irregular.
Nulle eosinophilia esseva demonstrate in
simile rattos, similemente inficite con le
mesme numero de trichincllas, quando istos
habeva essite sterilisate per medio de radiation roentgen.
SUMMARY
REFERENCES
Infection of young adult rats with 6000
nonirradiated Trichinella spiralis larvae
initiated an eosinophilia which was first
demonstrated on the 5th or 6th day of infection. This reached a peak of 3840 cells per cu.
mm. on the 14th day and thereafter declined
in an irregular manner.
No eosinophilia was demonstrated in similar rats, each of which was infected with the
same number of trichinellae reproductively
sterilized by means of roentgen radiation.
1. GOULD, S. E . : Trichinosis. Springfield, 111.:
Charles C Thomas, 1945, pp. 154-164.
2. G O U L D , S. E . , G O M B E R G , H . J . , B E T H E L L , F . H . ,
V I L L E L L A , J . B . , AND H E R T Z , C. S.: S t u d i e s
on Trichinella spiralis. I I . Time of initial
recovery of larvae of Trichinella
spiralis
from blood of experimental animals. Am. J .
P a t h . , 3 1 : 933-963, 1955.
3. L E V I N , A. J . : Recovery of Trichinella
spiralis
larvae in early stages of infection. J . P a r a sitol., 27: 107-113, 1941.
4. L E V I N , A. J . , AND E V A N S , T . C . : Use of r o e n t g e n
radiation in locating a n origin of host r e sistance t o Trichinella
spiralis infections.
J . Parasitol., 28: 477-483, 1942.
5. P O L L A Y , M . , W E I N , B . , AND H A R T M A N N , H . A . :
STJMMARlO IN INTERLINGTTA
Le infection de juvene rattos adulte con
innoculationes de 6000 nonirradiate larvas
de Trichinella spiralis initiava un eosinophilia que esseva primo demonstrate le 5te
o 6te die del infection. Le eosinophilia at-
Effect of A C T H upon artificially induced
trichinosis in rats with special reference t o
eosinophilia. Proc. Soc. Exper. Biol. &
Med., 86: 577-580, 1954.
6. ZAIMAN, H . , H O W A R D , R . G., AND M I L L E R , C .
J . : I m m u n e response in r a t s infected w i t h
Trichinella
spiralis
larvae subjected t o
roentgen radiation. Am. J . T r o p . Med., 10:
215-219, 1961.