INFECTION AND IMMUNrrY, Feb. 1975, p. 395-404 Vol. 11, No.

2
Copyright i 1975 American Society for Microbiology Printed in U.SA.

Synergism Between Trichuris suis and the Microbial Flora of

the Large Intestine Causing Dysentery in Pigs
J. M. RUTTER AND R. J. S. BEER
Agricultural Research Council, Institute for Research on Animal Diseases,
Compton, Newbury, Berkshire, England
Received for publication 2 October 1974

The role of the microbial flora of the large intestine in experimental Trichuris
suis infection was studied by comparing the clinical syndrome in conventionally
reared (CR) pigs, specific pathogen-free pigs, and gnotobiotic pigs. The disease
in CR pigs was characterized by a severe mucohemorrhagic enteritis; in contrast,
a mild catarrhal enteritis was observed in specific pathogen-free and
gnotobiotic pigs. Spirochaetes and vibrio-like organisms were observed only in
CR pigs and increased during the clinical phase of the disease. The clinical
syndrome was not transmitted by oral administration of intestinal or fecal
material from infected CR pigs to CR pigs free of T. suis. Smaller numbers of T.
suis produced diarrhea in CR pigs and significantly reduced the growth rates of
infected animals; clinical signs and the reduction in growth rate was prevented
by incorporating an antibacterial substance (dimetridazole) in the food. Al-
though clinical trichuriasis closely resembles swine dysentery, the two syndromes
seem to be distinct. The present results suggest that a microbial component acts
synergistically with T. suis to produce the severe clinical syndrome in CR pigs,
but identification of the microbial component and the mechanism by which
clinical signs are produced await further studies of the bacterial flora of the large
intestine of pigs.

The nematode Trichuris suis is present in
fattening pigs throughout the world (8) and its
widespread occurrence, usually in light infec-
tions, has given the impression that the parasite
presents no serious problem to animal health.
However, severe outbreaks of trichuriasis asso-
ciated with high mortality have been recognised
in the U.S.S.R. in Europe and in the U.S.A. (5).
Natural and experimental infections of weaned
pigs with T. suis causes a severe mucohemor-
rhagic diarrhea and death (6, 7, 21, 27), and this
syndrome closely resembles clinical descrip-
tions of the disease termed swine dysentery (1,
18, 36). Swine dysentery causes serious losses to
the pig industry and there have been numerous
attempts to define its etiology. At first, Vibrio
coli was thought to be responsible (14, 23, 26,
28), but several workers have been unable to
reproduce the disease with cultures of V. coli (2,
3, 13). More recently, a spirochaete has been
incriminated in swine dysentery (33, 35), and
the disease can now be reproduced in pigs by
feeding cultures of a large spirochaete classified
as type 1 (32) or Treponema hyodysenteriae
(19). Spirochaetes have been observed invadfing
within and between the cells of the colonic
epithelium of pigs with swine dysentery (18, 32),
395
and Beer and Rutter (7) reported that large
spirochetes, apparently morphologically dis-
tinct from T. hyodysenteriae, had invaded the
mucosa of the large intestine of pigs experimen-
tally infected with T. suis; these results sug-
gested that the migrating T. suis larvae may
damage the mucosal epithelium of the large
intestine and allow penetration of microorga-
nisms that contribute to the clinical signs that
follow T. suis infection. The present study was
part of an investigation of the role of bacterial
infection in the clinical syndrome that follows
experimental T. suis infection. In the first three
experiments, the syndrome was compared in
conventionally reared (CR), specific pathogen-
free (SPF), and gnotobiotic pigs; in the subse-
quent experiments the effect of an antibacterial
substance on T. suis infection in CR pigs was
investigated.
MATERIALS AND METHODS
AImimals. Trichuris-free, CR piglets from a herd
with no history of swine dysentery were weighed and
assigned to different groups using random numbers so
that the total weight of each group was approximately
equal. Each group was housed in separate pens in the
same building. The SPF pigs were second generation
396 RUTTER AND BEER INFECT. IMMUN.

stock from parents that were derived by hysterotomy; diarrhea, and were depressed. By day 26, the
the SPF pigs were free from enteric disease and were infected pigs were emaciated and had profuse
housed in a separate building. In the first three diarrhea, which in most cases contained fresh
experiments, CR and SPF pigs were fed Vitasukla 17 blood and large quantities of mucus. The unin-
(Vitamealo, Beecham Agricultural Products); in sub- fected pigs showed no clinical signs. The cumu-
sequent experiments, CR pigs were fed dry meal
containing 50% barley, 15% wheat, 20% wheatings, lative totals of the mean changes in body weight
and 15% proprietary concentrate ad libitum. Water of the pigs are shown in Fig. 1. During the first
was provided ad libitum for all animals. The piglets 14 days after infection, the control pigs grew
were weaned immediately prior to infection with T. faster than the infected group; after 14 days,
suis. Gnotobiotic piglets were derived and maintained growth of the infected pigs was reduced and the
in plastic isolators (30, 34). pigs lost weight from day 20 until they were
Infection procedure. Infective T. suis ova were killed.
suspended in saline and given to the piglets by (ii) Necropsy lesions. A progressive enteritis
stomach tube. The procedures for extraction of eggs was present in the infected pigs; this was
from feces and culture to the infective stage have been initially catarrhal but later became mucohem-
described (5a).
Clinical observations and weight gains. All pigs orrhagic. Fourteen days after infection the
were examined daily for the onset of clinical signs and wall of the large intestine was thickened and
weighed at frequent intervals. edematous, and the lumen contained large quan-
Necropsy procedures. Pigs were slaughtered by tities of clear mucus. After 20 days, the intesti-
immobilization with etorphine hydrochloride and ace- nal contents contained large quantities of mu-
promazine maleate (Immobilon, Reckitt and Cole- cus, fresh blood, and necrotic debris that sepa-
man), followed by intracardiac injection of pentobar- rated from the underlying mucosa. In some
bitone sodium (Euthatal, Abbott Laboratories) and cases, the lesion progressed to become a thick,
exsanguination. The abdomen was opened, the intes- necrotic pseudomembrane that covered the
tines were removed, and the mesentery was cut so
that the large intestine could be divided into three mucosal surface of the large intestine. No le-
equal parts. The large intestine was opened longitudi- sions were observed in the uninfected animals.
nally, its macroscopic appearance was noted, and The histopathological results will be described
samples were taken for bacteriological, histological, in a separate communication.
and microscopy examination. The mucosal surface of (iii) Microbiology. Large numbers of T. suis
the large intestine was scraped to remove the mucosa were recovered from the large intestines of
from the underlying submucosal layer, then the infected pigs (range 14,200 to 53,500, mean
scrapings were digested and the number of T. suis 32,500). Bacterial cultures of fecal samples from
were counted (7).
Microscopy examinations. Fecal samples and in- all pigs before infection with T. suis yielded
testinal contents were diluted and examined (7). predominantly coliform bacteria, gram-nega-
Bacteriological procedures. Rectal swabs were tive anaerobic bacteria, lactobacilli, and strep-
cultured on bovine blood agar, MacConkey agar, and tococci; small numbers of vibrio-like organisms
brilliant green agar and incubated aerobically at 37 C, (VLO) and spirochetes of different morphology
or on neomycin bovine blood agar and DeMan, Rogosa were present in some of the pigs. Similar
and Sharpe agar incubated anaerobically in anaerobic
jars (Baird and Tatlock Ltd). Fecal samples and GROWTH RATE OF CONVENTIONALLY REARED PIGS INFECTED
intestinal contents were diluted 1:2 (wt/vol) in saline WITH LARGE NUMBERS OF TRKCHLRIS SUIS
and filtered through a 0.65-nm membrane filter (Mil-
lipore Corp.) and then the filtrate was cultured on
bovine blood agar or dropped onto a 0.22-nm mem- 30 1
brane filter disk (Millipore Corp.) placed on the plate.
Cultures were incubated anaerobically for at least 4 z
4

days.
20
Histological procedures. Tissues removed at ne-
cropsy were fixed in 10% neutral buffered formalin,
embedded in paraffin wax, sectioned 5-nm intervals,
and stained by hematoxylin and eosin, Gram, Giemsa,
10
or Warthin-Faulkner stain (11).

RESULTS
Experiment 1: (i) experimental T. suis in- 0 10 20 30 40
fection in CR pigs. Nine pigs were each in- DAYS AFTER INFECTION
fected with 100,000 T. suis ova and 10 pigs were -*UNINFECTED GROUP (10 PIGS)
* INFECTED GROUP (9 PIGS)
left as uninfected controls. The infected pigs PIG KILLED
Aa

began passing loose feces after 10 days, and by FIG. 1. Growth of CR pigs infected with large num-
day 18 several pigs had lost their appetite, had bers of T. suis.
VOL. 11, 1975 SYNERGISM CAUSING DYSENTERY
bacteria were present after T. suis infection,
and from 12 days, increased numbers of VLO
and spirochetes were detected by phase contrast
microscopy in fecal samples from the infected
pigs. Increased numbers of these organisms
were present in mucosal scrapings from the
large intestine of infected compared with con-
trol pigs; both VLO and spirochetes increased
in some infected pigs, but in others, spirochetes
or VLO increased.
(iv) Microscopy. In sections stained by the
Warthin-Faulkner method, the crypts of the
large intestine of uninfected pigs frequently
contained small rod-shaped or curved bacteria.
From 15 days after infection, many organisms
were present in the excessive mucous secretions
on the surface of the large intestine of infected
pigs compared with the controls; the bacteria
were numerous adjacent to T. suis larvae (Fig.
2) and did not stain by Gram's method. Few
bacteria were present in the crypts of the
infected pigs.
A few organisms were seen adjacent to the
mucosal epithelium in sections of the large
intestine of control pigs by electron microscopy,
but large numbers of bacteria were present in
['
I
0 .I
FIG. 2. Bacteria (B) proliferating adjacent to a T. suis larva (L) in the large intestine of a CR pig killed 27
days after infection. Warthin-Faulkner stain. x 753.
397
infected pigs adjacent to T. suis larvae (Fig. 3);
these included rod-shaped or curved bacteria
approximately 400 nm in diameter and up to 1.5
Am long. Few spirochetes were seen and there
was little evidence of microbial invasion of the
surface epithelium.
Experiment 2: attempts to transmit the
clinical syndrome to pigs free of T. suis.
Diarrheic feces containing blood and mucus
were collected from pigs 18 days after infection
with T. suis; the material was diluted in an
equal volume of phosphate-buffered saline and
50 ml was given by stomach tube to each of six
weaned pigs. Four days later, each pig was given
20 ml of material collected from pigs with
clinical disease 22 days after infection with T.
suis. After a further 7 days, each pig was given
20 ml of material containing blood, mucus, and
desquamated epithelium collected from the
large intestine of a pig that was killed when
moribund 23 days after T. suis infection. No
clinical signs were observed after dosing with
these preparations. Infective T. suis ova had
not developed in the donor pigs and we con-
cluded that the bacteria alone could not initiate
the disease syndrome.
--
W.~-
r
-
40..
I
10, .:;
,b .
398 RUTTER AND BEER INFECTr. IMMUN .

,: w @wt v

V IL.

,h' £- 8

c)e-I.4
i! ,'-*,9 S :

¢f.s: - Ati .. .9)

i .' ' * '?

FIG. 3. Bacteria proliferating adjacent to the epithelium of the large intestine of a CR pig killed 25 days after
infection with T. suis. x23,700.

Experiment 3: (i) experimental T. suis
infection in SPF pigs. Six pigs were infected
with 100,000 T. suis ova and five pigs were left
as uninfected controls. One infected pig passed
loose feces intermittently between 19 and 26
days after infection; otherwise there were no
clinical signs. The cumulative totals of the
mean changes in body weight are shown in Fig.
4. The uninfected pigs grew slightly better than
the infected pigs throughout the experiment
and no loss in weight occurred in the infected
pigs.
(ii) Necropsy lesions. Fifteen days after
infection, the wall of the large intestine of
VOL. 11, 1975 SYNERGISM CAUSING DYSENTERY
GROWTH RATE OF SPECIFIC PATHOGEN FREE PIGS
WITH LARGE NUMBERS OF TRKHlRIS SUIS
30
a Experiment 4: experimental T. suis infec-
20
~10
0 10 20 30
DAYS AFTER INFECTION
= UNINFEcTED GROUP (5 PIGS)
= INFECTED GROUP (6 PIGS
M KILLED
FIG. 4. Growth of SPF pigs infected with large
numbers of T. suis.
infected pigs was thickened and edematous,
and by day 20, excessive mucous production
and small petechial hemorrhages were present.
After 23 days, foci of mucosa covered by an
exudate of mucus and necrotic debris were
observed in the upper third of the large intes-
tine. No lesions were found in the uninfected
animals.
(iii) Microbiology. Large numbers of T. suis
were recovered from the large intestines of
infected pigs (range 11,600 to 50,800, mean
28,000). Before infection with T. suis, fecal
samples yielded coliform bacteria, gram-nega-
tive anaerobic bacteria, lactobacilli, and strep-
tococci; similar bacteria were recovered after
infection with T. suis and, in contrast to the
CR pigs, no VLO or spirochetes were observed.
(iv) Microscopy. A few small rods of coc-
cobacilli were present on the mucosal surface of
the large intestine and in the crypts of Lieber-
kuhn of the control piglets. In contrast, in-
creased numbers of bacteria were present in the
excessive mucous secretions of infected pigs
from 15 days after infection; in general, there
were fewer organisms than in infected CR pigs.
The bacteria varied in size from long rods to
small coccobacilli, and in Gram-stained sec-
tions, there were more gram-positive bacilli and
coccobacilli than in the infected CR pigs. In-
creased numbers of organisms were seen in sec-
tions of the large intestine of infected pigs by
electron microscopy; these were sometimes
present in vacuoles and were generally close to
T. suis larvae. The organisms were rod shaped,
399
approximately 440 nm in diameter, and up to 2
zm long (Fig. 5); granules were present in the
bacterial cytoplasm, and the organisms ap-
peared to be morphologically different from
those proliferating in CR pigs.
tion in gnotobiotic piglets. Preliminary experi-
ments indicated that T. suis ova did not hatch
in the large intestine of germfree piglets but
could be recovered intact from the slurry.
Pairs of 7-day-old germfree piglets were then
infected with a strain of Staphylococcus aureus,
a nonhemolytic strain of Escherichia coli, or a
strain of Lactobacillus spp. all isolated from CR
pigs. The piglets were given 100,000 T. suis ova
40 4 days later and, after a further 5 days, the
slurry was collected and the percentage of hatch
of T. suis ova was calculated by examining the
slurry under the microscope. The hatch was 0,
12, and 30%, respectively, indicating that colo-
nization of the intestine of germfree pigs with a
Lactobacillus spp. gave the best hatch of T. suis
ova.
Four 7-day-old gnotobiotic piglets were then
colonized with the Lactobacillus spp., and after
5 days each piglet was given 100,000 T. suis ova.
A piglet was killed 15, 22, 25, and 30 days after
infection with T. suis. No diarrhea was ob-
served during this period, and at necropsy the
lesions were confined to the cecum and first half
of the large intestine; initially, the intestinal
wall became thickened and, later, excessive
clear mucus was present in the intestinal lu-
men. No petechial hemorrhages or necrotic
debris were observed. The numbers of T. suis
recovered were 1,049 to 9,740 (average 4,160).
Experiment 5: effect of dimetridazole on
severe clinical trichuriasis in CR pigs. Two
groups of seven pigs (groups 1 and 2) were each
given 100,000 T. suis ova and eight pigs were left
as uninfected controls (group 3). Group 1 re-
ceived 0.05% (wt/wt) dimetridazole (1,2-
dimethyl-5-nitroimidazole, 8595 RP, Emtryl,
May and Baker Ltd.) as a food additive from
day 13, when clinical signs developed, to the
end of the experiment. The development of
clinical signs was delayed in group 1, but by day
25, most of the pigs in groups 1 and 2 had typi-
cal signs of T. suis infection. The pigs were
slaughtered 32 days after infection. Large num-
bers of T. suis were recovered from group 1
(range 1,600 to 36,200, mean 22,800) and group
2 (range 200 to 36,400, mean 13,800). At ne-
cropsy, the lesions in the large intestine of pigs
in group 1 were less severe than those of group
2. In general, the degree of damage to the large
intestine was related to the numbers of T. suis
400 RUTTER AND BEER INFECT. IMMUN.

rs
I. i,..
;o 'L, ..

4$

A.

FIG. 5. Bacteria proliferating in vesicles in the large intestine of a SPF pig killed 35 days after infection with
T. suis. x33,600.

present; however, in some cases, there was
considerable damage and yet only small num-
bers of T. suis were recovered.
Experiment 6: (i) effect of dimetridazole on
mild clinical trichuriasis in CR pigs. Two
groups of eight pigs were given 70,000 T. suis
ova (groups 1 and 2) and eight pigs were left as
uninfected controls (group 3). Group 1 was
given 0.05% (wt/wt) dimetridazole as a food
additive throughout the experiment. Clinical
signs were confined to the infected, untreated
pigs (group 2), which began passing loose feces
16 days after infection. By day 25 all pigs in
group 2 had diarrhea, but this contained no
VOL. 11, 1975 SYNERGISM CAUSING DYSENTERY
blood or mucus. The pigs were slaughtered 32
days after infection.
The cumulative totals of the mean changes in
body weight of the three groups were analyzed
by a split-plot analysis, with the three groups as
the main plot and the number of days after
infection as the subplot. There was no signifi-
cant difference between the totals of mean
changes in body weight of groups 1 (infected,
treated) and 3 (uninfected) during the experi-
ment. By day 20, the cumulative total of mean
changes in body weight of group 2 (infected,
untreated) was significantly lower than group 3
(P < 0.01), and by day 24, the cumulative total
of mean changes in body weight of group 2 was
significantly lower than group 1 (P < 0.01);
these differences continued to the end of the
experiment.
(ii) Necropsy fmdings. Necropsy lesions
were confined to groups 1 and 2. The mucosa of
the large intestine of the majority of pigs from
group 2 was hyperemic, thickened, and edema-
tous with petechial hemorrhages and excessive
mucous production. The lesions in group 1 were
less severe compared with group 2 and fewer
pigs were affected.
(iii) Microbiology. T. suis was recovered
from group 1 (range 2,700 to 11,300, mean 6,700)
and group 2 (range 5,100 to 11,600, mean 8,600).
The numbers of spirochetes and VLO observed
in wet preparations from fecal material and in
sections stained by the Warthin-Faulkner
method were greater in group 2 compared with
group 1.
(iv) Microscopy. In general, there were more
bacteria in the mucous exudate of the large
intestine in pigs from group 2 compared with
group 1. Bacteria, including spirochetes, were
seen proliferating close to T. suis larvae in
sections of the large intestine of pigs from, group
2 by electron microscopy (Fig. 6), but few
organisms were seen in sections from the other
pigs.
DISCUSSION
The clinical syndrome and necropsy lesions of
T. suis infection are similar to those described
for swine dysentery; in both diseases there is a
profuse mucohemorrhagic diarrhea, the lesions
are confined to the large intestine, and natural
infection is most severe in young weaned pigs.
Although these similarities raise the possibility
that swine dysentery is initiated by T. suis
infection, this interpretation seems unlikely for
several reasons: severe clinical signs with T. suis
infection generally require the presence of large
numbers of the nematode; and although T. suis
401
is widely distributed in fattening pigs through-
out the world (8), there is little evidence that it
reaches sufficiently high numbers (9) to account
for the widespread occurrence of swine dysen-
tery. Furthermore, swine dysentery is charac-
terized by the presence of large numbers of
Treponema hyodysenteriae in the large intes-
tine of infected pigs and the disease can be
reproduced by oral administration of the spiro-
chete (21, 31). Although the present results
indicate that increased numbers of spirochetes
can occur in pigs with experimental T. suis
infection, we were unable to transmit the dis-
ease by feeding intestinal material from in-
fected pigs to pigs free of T. suis. Thus, swine
dysentery and experimental T. suis infection
appear to be different syndromes, and the
similar clinical signs may reflect a restricted
capacity of the large intestine to respond to
injury. These conclusions do not exclude the
possibility that some outbreaks of swine dysen-
tery may be attributable to T. suis infection,
and a closer examination of such outbreaks in
pigs housed in conditions that would favor T.
suis seems justified.
The results of the present experiments sug-
gest that a component of the bacterial flora of
the large intestine plays a significant role in the
clinical syndrome of experimental T. suis infec-
tion. CR pigs infected with large numbers of the
nematode became severely diseased, whereas
SPF pigs with similar burdens of the nematode
showed virtually no clinical signs. Necropsy
lesions in SPF pigs indicated that T. suis larvae
produce thickening of the wall of the large
intestine and excessive mucous production; a
similar lesion was present in the early stages of
infection in CR pigs, but by 20 days, there were
hemorrhages and necrosis. During this period,
large numbers of bacteria had proliferated in
the exudate and the pigs stopped eating and
growing. Bacteria also proliferated in the exu-
date of SPF pigs infected with T. suis; therefore,
it seems that different types of bacteria may
multiply in the two groups and that the postu-
lated microbial component was absent from
the SPF pigs. Because disease did not occur in
the SPF pigs, we concluded that the microbial
component is not carried within the nematode
ova.
The results of T. suis infection in gnotobiotic
piglets confirmed that in the absence of a
conventional gut flora, T. suis larvae produce
thickening of the gut wall and excessive mucous
secretion. The failure of T. suis ova to hatch in
germfree piglets is presumably related to the
gut environment. Batte and Moncol (4) stated
402 RUTTER AND BEER INFECT. IMMUN.

.7
_ft
V<
..
tI

,r

I. ?;
k

F, '+

L--
'-"-N

is,, I
C~...

{Ll';

I ..

FIG. 6. Bacteria including spirochetes (S) proliferating adjacent to the epithelium of the large intestine of a
CR pig killed 32 days after infection with T. suis. x81,000.

that infective ova of T. suis are softened by
stomach secretions so that the larvae are liber-
ated; the pH of the stomach contents of germ-
free piglets may be less acid than that of
gnotobiotic piglets contaminated with lactoba-
cilli, which may account for the better hatch
obtained in the latter group.
If bacteria contribute significantly to the
clinical syndrome of T. suis infection, then it
should be possible to modify the development of
the disease with antibacterial substances. Sup-
port for this view was obtained by incorporating
dimetridazole in the feed of CR piglets with
mild trichuriasis; this prevented the develop-
VOL. 11, 1975 SYNERGISM CAUSING DYSENTERY
ment of diarrhea and enabled the treated pig-
lets to grow as well as the control group.
However, dimetridazole was not effective in CR
pigs with severe clinical trichuriasis; this may
have been attributable to reduced intake of the
drug as a result of anorexia. These results are
consistent with the view that a microbial com-
ponent in CR pigs acts synergistically with T.
suis to produce the clinical signs of infection.
Microbial synergism can be defined as the
combined activity of two or more microbial
agents that separately produce minimal lesions
but together cause a more severe reaction than
would be expected from a summation of the
individual effects. T. suis produces only a
catarrhal enteritis; the microbial component in
CR pigs cannot initiate the disease in the
absence of T. suis, and it is only when the two
agents are present together that the severe
clinical syndrome occurs.
The clinical signs caused by T. suis infection
begin about 12 days after administration of the
ova; this corresponds with the time at which the
larvae protrude their posterior tips through the
mucosal surface with localized rupture of the
epithelial cells. Presumably, the emerging lar-
vae stimulate the production of excessive mucus
in which the microbial component of CR pigs
multiplies. We have not identified this mi-
crobial component or the mechanism by which
clinical signs are produced in the present study,
but the following observations are worthy of
mention: (i) we were unable to demonstrate
VLO or spirochetes in SPF pigs, and (ii) VLO
and spirochetes increased in infected pigs with
clinical signs and were reduced in infected pigs
treated with dimetridazole. Bacterial prolifera-
tion occurred predominantly in the mucous
exudate, and invasion of the mucosa did not
appear to be a significant component of the
lesion. Dimetridazole has been effective in con-
trolling swine dysentery; it has antimicrobial
activity in vitro, against spirochetes, vibrios,
fusiforms, Bacteroides, and Clostridia spp. (17);
although dimetridazole has anti-protozoal ac-
tivity (17), the recoveries of T. suis from groups
1 and 2 in experiments 5 and 6 suggest that
the drug has no activity against the nematode.
Since spirochetes were not demonstrated in all
the infected pigs during the present study, it
seems likely that other organisms, or combina-
tion of organisms, produce the clinical signs of
T. suis infection, and further studies are neces-
sary to identify the microbial flora of the large
intestine of CR and SPF pigs.
An early lesion in the pathogenesis of swine
dysentery is catarrhal enteritis (18), and since
the disease is not produced in germfree pigs
403
with T. hyodysenteriae, it has now been sug-
gested that synergism between T. hyodysen-
teriae and a portion of the normal enteric flora
occurs in swine dysentery (16). As in the pres-
ent study, increased numbers of vibrios and
spirochetes other than T. hyodysenteriae have
been observed in swine dysentery (22, 23); how-
ever, the presence of large numbers of a par-
ticular organism in diarrheal disease does not
necessarily reflect its pathogenicity (15, 25).
In addition, the controversy regarding the
pathogenic role of T. trichiura in man may be
explained by an interaction between the nema-
tode and the gut flora; although Jung and
Beaver (24) observed that Entamoeba histo-
lytica was frequently present in association
with human trichuriasis, T. trichiura has also
been reported to be pathogenic in the absence
of E. histolytica (10). In contrast, Hartz (20)
found that no clinical signs and minimal damage
to the colonic mucosa occur in T. trichiura in-
fection. These results could be explained by
the presence or absence of microbial compo-
nents in the large intestine at the time of para-
sitic infection.
The microbial flora of the large intestine of
animals includes fusiform bacteria, vibrios, and
spirochetes (12, 13, 25, 29). Although these
bacteria are not generally regarded as being
pathogenic, they may enhance a clinical syn-
drome if they proliferate to reach numbers
greater than are normally present. This may
occur only if the ecological niche is disturbed,
e.g., by excessive production of mucus as a
result of damage to the large intestine. How-
ever, administration of the bacteria alone may
not reproduce the disease in normal animals
unless the environment of the gut is modified to
provide suitable conditions for bacterial prolif-
eration.
ACKNOWLEDGMENTS
We are indebted to C. Lane-Petter, J. Bell, N. Hammet,
M. Burrows, and C. Jay for their expert assistance, and to B.
Kitchenham for statistical analyses. We thank M. Hoare, C.
Davies, and M. Dennis for providing the gnotobiotic piglets,
P. Bland for the electron micrographs, and I. Jebbett for
preparing the photographs.
LITERATURE CITED
1. Alexander, T. J. L., and D. J. Taylor. 1969. The clinical
signs, diagnosis and control of swine dysentery. Vet.
Rec. 85:59-63.
2. Andress, C. E., and D. A. Bamum. 1968. Pathogenicity of
Vibrio coli for swine. II. Experimental infection of
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