Parasite Immunology, 1997: 19: 137–143
A comparison of mucosal inflammatory responses to Giardia muris in
resistant B10 and susceptible BALB/c mice
P.VENKATESAN 1 , R.G.FINCH 2 , & D.WAKELIN 1
1
Department of Life Science, University of Nottingham, Nottingham NG7 2RD, UK
2
Department of Microbiology, University of Nottingham, City Hospital, Nottingham NG5 1PB, UK
SUMMARY
In the first three weeks of primary Giardia muris infections
B10 mice clear infection more rapidly than BALB/c mice.
There is evidence that interferon-g contributes to the rela-
tive resistance of B10 mice. The nature of the functional
contribution of interferon-g is unclear and does not relate to
the secretory or serum antibody response. Mucosal inflam-
matory events in these strains have been studied. Apart from
a small rise in both strains of goblet cell and mucosal mast
cell numbers, associated with release of mast cell protease-1
in serum, no inflammatory infiltrate was observed at the time
trophozoites were cleared from the intestinal lumen. Inhibi-
tion of mast cell products (5-hydroxytryptamine and hista-
mine) by cyproheptadine enhanced the intensity of infection
in both strains. The relative resistance of B10 mice could not
be explained in terms of the mucosal inflammatory response.
Keywords Giardia muris, mucosal inflammation, mast
cells, histamine, 5-hydroxytryptamine, nitric oxide
Correspondence: P.Venkatesan
Current address: Department of Infection and Tropical Diseases,
Birmingham Heartlands Hospital, Birmingham B9 5ST, UK
Received: 10 April 1996
Accepted for publication: 29 November 1996
q 1997 Blackwell Science Ltd
INTRODUCTION
The regulation of infection with Giardia is under immune
control, as immunodeficient humans and experimental ani-
mals suffer protracted infections. Primary Giardia muris
infections in two panels of B10 and BALB H-2 congenic
strains of mice provide a good model for analysis of
mechanisms of immune control. During the first three
weeks B10 strains clear infection more rapidly than
BALB strains, and on a BALB background MHC haplotype
influences the course of infection (Venkatesan, Finch &
Wakelin 1993). Antibody is known to contribute to immune
clearance (Snider et al. 1985) but when the timing, titre and
specificity of secretory and serum antibodies were compared
between the panels no demonstrable difference was found to
explain the relative resistance of the B10 strains (Venkate-
san, Finch & Wakelin 1996). Two representative strains,
BALB/c and C57B110(B10)/ScSn (B10), have been studied
in detail. Unlike BALB/c mice, mesenteric lymph node cells
from B10 mice produce interferon-g and specific blockade
of this cytokine results in enhanced levels of infection in the
latter strain (Venkatesan et al. 1996).
There is conflicting, indirect evidence on the importance
of intestinal mucosal inflammation in resistance to giardia-
sis. In co-infections of G. muris with Trichinella spiralis
there was a significant reduction in the G. muris infection
during the intestinal phase of T. spiralis infection and this
was proportional to the mucosal inflammatory response
(Roberts-Thomson, Grove & Stevens 1976a). In contrast
Ferguson & Munro (1988) found that mucosal inflammation
induced by a graft versus host reaction did not suppress a
G. muris infection. One aspect of the immune/inflammatory
response which has attracted interest in recent years is the
biochemical attack of pathogens by nitric oxide and oxygen
radical species. In fact anti-oxidant systems are described in
parasites and these may serve as their defence (Callahan,
Crouch & James 1988). Both nitric oxide and oxygen radical
production are stimulated by interferon-g. We have invest-
igated whether the relative resistance of B10 mice can be
137

P.Venkatesan, R.G.Finch & D.Wakelin
explained in terms of their cellular and biochemical mucosal
inflammatory response.
MATERIAL AND METHODS
Animals
Six to eight week old, female, specific pathogen free mice
were purchased from Harlan Olac Ltd, Bicester, UK. The
principle strains of mice used were BALB/c and B10.
G. muris
G.muris cysts were provided by Professor G Faubert of
McGill University, Montreal, Canada. They were stored at
48C in phosphate buffered saline (PBS), pH 7:2, and con-
tinually passaged through BLAB/c mice. Mice were
infected orally using a standard inoculum of 103 cysts in
0:3 ml Hanks Balanced Salt Solution (HBSS). Infection was
monitored by quantifying two h faecal cyst output by the
method of Roberts-Thomson et al. (1976b).
Intestinal washings and sera
Intestinal washings and sera were stored at ¹308C. Intest-
inal washings were collected from the small intestine after
removal, ligation, instillation of 3 ml PBS, massage for one
minute, centrifugation of contents and collection of the
supernate.
Histology
Maximal histological changes in infected mice occur about
10 cm from the gastroduodenal junction (Buret, Gall &
Olsen 1990). Segments of intestine from this region were
fixed in Carnoy’s fixative. After processing 5 mm sections
were stained with either haematoxylin and eosin (for intra-
epithelial lymphocyte [IEL] and inflammatory cell counts)
or with Alcian blue/Astra blue, counterstained with safranin
O (for mast cell and goblet cell counts). Cell counts were
made from 25 villus:crypt units (VCU) per slide.
Mouse mast cell protease-1 (MMCP-1) ELISA
Sera were assayed for MMCP-1 by the method of Huntley
et al. (1990), using a commercial ELISA kit (Moredun
Research Institute, Edinburgh, UK).
Cyproheptadine
The mast cell products 5-hydroxytryptamine and histamine
were blocked with 15 mg/kg cyproheptadine (Sigma, UK) in
138
13653024, 1997, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3024.1997.d01-189.x by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [21/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Parasite Immunology
0:2 ml saline, injected intra-peritoneally (ip) daily from day
5–20 of the experiment. Control mice were given saline
alone.
Anti-oxidant enzyme assays
Preparations of trophozoite proteins were made by disrupt-
ing trophozoites in distilled water and freeze-thawing. Using
fresh preparations three anti-oxidant enzymes were assayed
— catalase by the method of Aebi (1984), glutathione-S-
transferase (GST) by the method of Alin, Danielson &
Mannervik (1985) and superoxide dismutase (SOD).
The assay for SOD was based on inhibiting the reduction
of nitroblue tetrazolium (NBT, Sigma, UK) as measured by
a change in absorbance at 560 nm. The reaction mixture
consisted of 27 ml 50 mM potassium phosphate buffer, pH
7:8, 1:5 ml L-methionine (300 mg/10 ml buffer) (Sigma,
UK), 1 ml NBT (14:1 mg/10 ml buffer) and 0:75 ml 1%
Triton X-100. 0:9 ml of the reaction mixture was placed in
cuvettes and to this was added 10 ml of riboflavin (4:4 mg/
100 ml buffer) (Sigma, UK) and 0:1 ml of a serial dilution of
trophozoite proteins or distilled water as control. The OD
560 nm was measured before and after exposing cuvettes to
ultraviolet light for two min.
Nitric oxide (NO)
NO is rapidly converted to nitrite and then nitrate ions.
Serum and intestinal washings were assayed for nitrate by
the Griess reaction after nitrate had been converted to
nitrite by Aspergillus nitrate reductase (Sigma, UK)
(Green et al. 1982). NO production was inhibited in vivo
by NG -monomethyl-L-arginine (L-NMMA, Sigma, UK),
administered by daily gavage of 15 mg in 0:2 ml PBS on
day 8-11 of infection. Control mice were given PBS alone.
The latter experiment was only performed in B10 mice as
interferon-g had previously been implicated in resistance in
this strain and not in BALB/c mice.
Statistical methods
The value P < 0:05 was taken as the level of significance.
The Mann-Whitney U-test was used for statistical analysis.
P and U values were derived from published tables (Siegel
1956).
RESULTS
Course of infection
The course of G. muris infection in BALB and B10 congenic
strains is shown in Figure 1 and has been described previously
q 1997 Blackwell Science Ltd, Parasite Immunology, 19, 137–143

Volume 19, Number 3, March 1997
Figure 1 The course of primary Giardia muris infection in (a) BALB and (b) B10 panels of H-2 congenic strains of mice. Experimental groups of
eight mice were infected orally on day 0 with 103 G.muris cysts and the course of infection monitored by weekly 2 h faecal cyst output. The limit
of detection is 250 cysts as shown by the horizontal line. (a) W BALB/c; e BALB/K; A BALB/B. (b) X B1O.D2n; O; B1O.BR; B B1O.
(Venkatesan et al. 1993). By day 21 post infection there is a
100 fold difference in cyst counts between BALB and B10
strains. The overall intensity and duration of infection is
reduced in B10 strains. On a BALB background there are
significant MHC related differences in the course of infec-
tion. The histological studies described below concentrated
on representative strains of the two panels, namely BALB/c
and B10.
Inflammatory response
Histological slides were examined from five mice each of
BALB/c and B10 strains on days 0, 7, 10 and 14 post
infection. On day 7 trophozoites covered the whole surface
of villi but numbers then declined, this decline being more
marked in B10 mice. Unlike BALB/c mice very few
trophozoites could be seen in B10 mice on day 14. Tropho-
zoites were seen embedded in strands of mucus which
separated from the epithelial surface as an artefact of slide
preparation.
The predominant cells in the lamina propria were mono-
nuclear and included plasma cells and monocytes. Very
occasionally eosinophils and polymorphonuclear cells were
seen, < 1 per 10 villi. During the first two weeks of infection
there was no discernible increase in these inflammatory cells
or swelling of villi. Villus atrophy and crypt hyperplasia
were not seen. There were no significant strain differences in
the number of IEL/100 epithelial cells (Figure 2a). Despite
obvious differences in trophozoite load the appearance of
BALB/c and B10 villi were the same.
Mast cells
In both strains mast cell numbers increased till day 10 and
q 1997 Blackwell Science Ltd, Parasite Immunology, 19, 137–143
13653024, 1997, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3024.1997.d01-189.x by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [21/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Mucosal inflammatory responses in murine giardiasis
then fell (Figure 2b). In B10 mice there was a three-fold
increase in mast cell numbers, while in BALB/c mice
numbers increased by a half. On all days except day 14
BALB/c mice had significantly higher counts (P ¼ 0:014,
U ¼ 0). Serum MMCP-1 was measured in two experiments,
measurements occurring at different intervals (Figure 3).
MMCP-1 levels rose significantly from baseline in both
strains in both experiments in the first two weeks (BALB/c -
P ¼ 0:014, U ¼ 0 and P ¼ 0:004, U ¼ 0; B10 - P ¼ 0:014,
U ¼ 0 and P ¼ 0:004, U ¼ 0 in the two experiments
respectively). There was slight variation in the timing of
peak serum levels between experiments. Only on day 10 in
the first experiment (Figure 3a) was serum MMCP-1 sig-
nificantly higher in B10 mice. There were no significant
strain differences in MMCP-1 levels in the second experi-
ment (Figure 3b). On administration of cyproheptadine to
both strains the course of infection was the same as controls
until day 21 (Table 1). On that day the faecal cyst counts
were ten-fold higher in the treated group (BALB/c:
P ¼ 0:002, U ¼ 1; B10: P ¼ 0:001, U ¼ 0).
Goblet cells
Goblet cell numbers increased very slightly, but significantly
in both strains (P ¼ 0:014, U ¼ 0) [Figure 2c]. BALB/c mice
has significantly more goblet cells than B10 mice on days 10
(P ¼ 0:029, U ¼ 1) and 14 (P ¼ 0:014, U ¼ 0).
Anti-oxidant enzymes
Catalase was not detected. GST was found at a concentration
of 35:5 mU/mg and SOD at a concentration of 2393 mU/mg
(means from three separate assay experiments).
139

P.Venkatesan, R.G.Finch & D.Wakelin
Nitric oxide
Nitrate was not detectable in intestinal washings. In B10
mice L-NMMA effectively turned off NO production as
demonstrated by decreased levels of serum nitrate in the
treated group. In fact in three out of five mice serum nitrate
was not detectable in the L-NMMA treated group and only
low concentrations were found in the remaining two mice.
However this had no effect on the clearance of infection in
B10 mice (Table 2).
DISCUSSION
Previous histological studies in giardiasis have been largely
concerned with architectural and functional changes in the
small intestine (Ferguson, Gillon & Munro 1990). In
humans there is a range of pathological changes, from
total villous atrophy to normality with or without associated
deficiencies in disaccharidase activity. Biopsy specimens
140
13653024, 1997, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3024.1997.d01-189.x by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [21/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Parasite Immunology
Figure 2 Five mice per experimental group were sacrificed on the
days shown post infection and 25 villus-crypt units examined per
mouse. Mean counts þ standard error of the mean (SEM) are shown
for (a) intra-epithelial lymphocytes (IEL)/100 epithelial cells, (b)
mast cells and (c) goblet cells. A BALB/c; B B1O.
show infiltrates of polymorphonuclear and mononuclear
cells with increased numbers of IEL (Zamcek et al. 1963,
Yardley, Takano & Hendrix 1964, Wright & Tomkins 1977,
Gillon 1985). In experimental animal models similar find-
ings have been made (Gillon, Al Thamery & Ferguson 1982,
Olveda, Andrews & Hewlett 1982, Buret et al. 1990). Apart
from studies on IEL, inflammatory infiltrates have not been
correlated with the course of infection in these models.
The present study has compared mucosal inflammatory
responses to G. muris in relatively resistant (B10) and
susceptible (BALB/c) strains of mice, concentrating on the
early phase of primary infections. By day 14 post infection
clear cut differences in trophozoite numbers are seen
between these strains, with very few trophzoites being
present in B10 mice. If the inflammatory response contri-
butes to the relative resistance of B10 mice differences
between strains in the inflammatory response should be
apparent at this time.
In both BALB/c and B10 mice IEL counts were similar
q 1997 Blackwell Science Ltd, Parasite Immunology, 19, 137–143

Volume 19, Number 3, March 1997
Figure 3 Mean levels of serum mucosal mast cell protease-1 in ng/ml6 SEM in two separate experiments with (a) five mice per experimental
group and (b) four mice per experimental group. W BALB/c; B B1O.
and there was no eosinophil or polymorphonuclear infiltrate.
Studies in humans have shown eosinophil and polymorpho-
nuclear infiltrates, but this was beyond the acute phase of
infection when parasite numbers were already declining
(Zamchek et al. 1963; Yardley et al. 1964). Both mast cell
and goblet cell numbers increased but these changes were
very small, especially when compared with the changes seen
in helminthic infections. The relatively susceptible BALB/c
strain had higher counts of both these cells but the relatively
resistant B10 strain has a proportionately greater increase in
mast cell numbers. Although mast cell numbers were small
there was evidence of mast cell activation through secretion
of MMCP-1 into serum.
Mast cells have long been thought to be important in
giardiasis as mast cell deficient Wf /Wf mice are more
Table 1 The influence of cyproheptadine on primary Giardia muris
infection
BALB/c B10
Cyproheptadine 40:3 1:06
631:4 60:38
Control 4:75 0:07
64:27 60:05
P value 0:002 0:001
U value 1 0
Six female mice in each experimental group were infected with 103
G. muris cysts on day 0 and the course of infection monitored by
measuring two h faecal excretion of cysts. Between days 5–20
cyproheptadine (15 mg/kg in 0:2 ml saline) or 0:2 ml saline control
was administered daily intra-peritoneally. Day 21 mean cyst count
(×10¹4 Þ 6 SD.
q 1997 Blackwell Science Ltd, Parasite Immunology, 19, 137–143
13653024, 1997, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3024.1997.d01-189.x by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [21/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Mucosal inflammatory responses in murine giardiasis
susceptible than normal or heterozygote Wf /þ mice
(Erlich et al. 1983). Erlich et al. (1983) found that blockade
with cyproheptadine of the mast cell products 5-hydroxy-
tryptamine and histamine impaired clearance of infection in
BALB/c mice. We confirm this finding in BALB/c mice and
extend it to B10 mice. The effect of cyproheptadine and the
activation of mast cells, as indicated by MMCP-1, was
similar in both strains. This argues against differential
involvement of mast cell activity to account for the relative
resistance of B10 mice.
Goblet cell hyperplasia and increased mucus secretion
contribute to the intestinal mucosal response to infection
(Tse & Chadee 1991). In rats, where the rapid expulsion of
Nippostrongylus brasiliensis has been attributed to the
trapping of worms in the mucus layer (Miller, Huntley &
Table 2 The influence of L-NMMA on primary Giardia muris infec-
tion in B10 mice
Days post infection
7 12
L-NMMA 12:2 3:7
69:5 65:2
Control 19:2 6:25
618:5 64:0
P value NS NS
Five female mice in each experimental group were infected with 103
G. muris cysts on day 0 and the course of infection monitored by
measuring two h faecal excretion of cysts. Between days 8–11
L-NMMA (15 mg in 0:2 ml PBS) or 0:2 ml PBS control was
administered by daily gavage. NS ¼ not significant. Mean cyst count
(×10¹4 ) 6SD.
141

P.Venkatesan, R.G.Finch & D.Wakelin
Wallace 1981), there are both quantitative and qualitative
changes in mucus secretion (Ishikawa, Horii & Nawa 1993).
It is difficult to quantify mucus secretion in the mouse or
collect sufficient mucus for analysis, and goblet cell num-
bers may not reliably indicate total mucus secretion.
There is indirect evidence to suggest mucus may play a
part in clearance of Giardia infection. Studies in vitro show
that mucus can promote or inhibit adherence and growth of
Giardia intestinalis, depending on concentration and source
of the mucus (Zenian & Gillin 1985). In gerbils there is
circumstantial evidence that increased mucus secretion,
stimulated by a high fibre diet, reduces epithelial attachment
and the intensity of infection with G. intestinalis (Leitch
et al. 1989). Our histological observation of trophozoites
trapped in mucus may support a role for mucus in vivo.
However in comparing strains it is difficult to ascribe the
relative resistance of B10 mice to the goblet cell response as
relatively susceptible BALB/c mice had higher numbers of
goblet cells.
The presence of anti-oxidant enzymes in G. muris suggests
that resisting radical species may be important in vivo. The
presence of SOD has been described before (Lindmark
1980) but GST has not. In vitro the adherence of Giardia
intestinalis trophozoites to a glass surface can be inhibited
by granule enzymes or oxygen radicals (Crouch et al. 1991).
To assess their role in vivo we have attempted to measure
radical production by isolated intestinal mucosal leucocytes
using a chemiluminescence method after Ovington, Smith &
Joysey (1990). These attempts were unsuccessful and made
it difficult to interpret the efficacy of pentoxifylline admin-
istered to mice to inhibit radical production. When pentoxi-
fylline was administered, in a dose established in other
systems to block radical production (Kremsner et al. 1991),
we found that the course of infection in both BALB/c and B10
strains was not altered. However, as described here, a demon-
strably effective dose of L-NMMA, used to inhibit NO
production, had no effect on the course of infection in B10
mice. Interferon-g stimulates the production of NO and
oxygen radicals, but from this data we do not have any
conclusive evidence to suggest that they are responsible for
the relative resistance of B10 mice.
In conclusion antibody (Snider et al. 1985), mast cells and
mast cell products (Erlich et al. 1983), interferon-g (sub-
mitted for publication) and perhaps mucus contribute to the
immune clearance of G. muris. The details of how they
function is yet to be established.
ACKNOWLEDGEMENTS
P.Venkatesan was a Wellcome Trust Medical Graduate
Research Fellow. The financial support of the Wellcome
Trust is gratefully acknowledged.
142
13653024, 1997, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3024.1997.d01-189.x by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [21/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Parasite Immunology
REFERENCES
Aebi H. (1984) Catalase in vitro. Methods in Enzymology 105, 121–126
Alin P., Danielson H. & Mannervik B. (1985) Hydroxyalk-2-enals are
substrates for glutathione transferase. FEBS Letters 179, 267–270
Buret A., Gall D.G. & Olsen M. E. (1990) Effects of murine giardiasis
on growth, intestinal morphology and disaccharidase activity. Jour-
nal of Parasitology 76, 403–409
Callahan H.L., Crouch R.K. & James E.R. (1988) Helminth anti-
oxidant enzymes: a protective mechanism against host oxidants?
Parasitology Today 4, 218–225
Crouch A.A., Seow W.K., Whitman L.M. et al. (1991) Inhibition of
adherence of Giardia intestinalis by human neutrophils and
monocytes. Transactions of the Royal Society of Tropical Medicine
and Hygiene 85, 375–379
Erlich J.H., Anders R.F., Roberts-Thomson I.C. et al. (1983) An
examination of differences in serum antibody specificities and
hypersensitivity reactions as contributing factors to chronic infection
with the intestinal protozoan parasite, Giardia muris, in mice.
Australian Journal of Experimental Biology and Medical Sciences
61, 599–615
Ferguson A. & Munro G.H (1988) Giardia muris infection in mice with
concurrent graft-versus-host reaction. Parasite Immunology 10, 589–
592
Ferguson A., Gillon J. & Munro G. (1990) Pathology and pathogenesis
of the intestinal mucosal damage in giardiasis. In Giardiasis—
Human Parasitic Diseases: Volume 3, ed. E.A. Meyer, Elsevier,
Amsterdam pp. 155–173
Gillon J., Al Thamery D. & Ferguson A. (1982) Features of small
intestinal pathology (epithelial cell kinetics, intra-epithelial lympho-
cytes, disaccharidases) in a primary Giardia muris infection. Gut 23,
498–506
Gillon J. (1985) Clinical studies in adults presenting with giardiasis to a
gastro-intestinal unit. Scottish Medical Journal 30, 89–95
Green L.C., Wagner D.A., Glogowski J. et al. (1982) Analysis of
nitrate, nitrite and (15 N) nitrate in biological fluids. Analytical
Biochemistry 126, 131–138
Huntley J.F., Gooden C., Newlands G.F.J. et al. (1990) Distribution of
intestinal mast cell proteinase in blood tissues of normal and
Trichinella-infected mice. Parasite Immunology 12, 85–95
Ishikawa N., Horii Y. & Nawa Y. (1993) Immune-mediated alteration
of the terminal sugars of goblet cell mucins in the small intestine of
Nippostrongylus brasiliensis-infected rats. Immunology 78, 303–307
Kremsner P.G., Grundmann H., Neifer S. et al (1991) Pentoxifylline
prevents murine cerebral malaria. Journal of Infectious Diseases 164,
605–608
Leitch G.J., Visvesvara G.S., Wahlquist S.P. et al. (1989) Dietary fiber
and giardiasis: dietary fiber reduces rate of intestinal infection by
Giardia lamblia in the gerbil. American Journal of Tropical Medi-
cine and Hygiene 41, 512–520
Lindmark D.G. (1980) Energy metabolism of the anaerobic protozoan,
Giardia lamblia. Molecular and Biochemical Parasitology 1, 1–12
Miller H.R.P., Huntley J.F. & Wallace G.R. (1981) Immune exclusion
and mucus trapping during the rapid expulsion of Nippostrongylus
brasiliensis from primed rats. Immunology 44, 419–429
Olveda R.K., Andrews J.S. & Hewlett E.L. & (1982) Murine giardiasis:
localisation of trophozoites and small bowel histopathology during
the course of infection. American Journal of Tropical Medicine and
Hygiene 31, 60–66
Ovington K.S., Smith N.C. & Joysey H.S. (1990) Oxygen derived free
radicals and the course of Eimeria vermiformis infection in inbred
strains of mice. Parasite Immunology 12, 623–631
q 1997 Blackwell Science Ltd, Parasite Immunology, 19, 137–143

Volume 19, Number 3, March 1997
Roberts-Thomson I.C., Grove D.I. & Stevens D.P. (1976a) Suppression
of giardiasis during the intestinal phase of trichinosis in the mouse.
Gut 17, 953–958
Roberts-Thomson I.C., Stevens D.P., Mahmoud A.A.F. et al. (1976b)
Giardiasis in the mouse: an animal model. Gastroenterology 71, 57–61
Siegel S. (1956) Non-parametric statistics: For the behavioural
sciences. McGraw-Hill, Kogakusha, Tokyo.
Snider D.P., Gordon J., McDermott M.R. et al. (1985) Chronic Giardia
muris infection in anti-IgM treated mice. I. Analysis of immunoglo-
bulin and parasite-specific antibody in normal and immunoglobulin-
deficient animals. Journal of Immunology 134, 4153–4162
Tse S.K. & Chadee K. (1991) The interaction between intestinal mucus
glycoproteins and enteric infections. Parasitology Today 7, 163–172
Venkatesan P., Finch R.G. & Wakelin D. (1993) MHC haplotype
influences primary Giardia muris infections in H-2 congenic strains
of mice. International Journal of Parasitology 23, 661–664
q 1997 Blackwell Science Ltd, Parasite Immunology, 19, 137–143
13653024, 1997, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3024.1997.d01-189.x by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [21/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Mucosal inflammatory responses in murine giardiasis
Venkatesan P., Finch R.G. & Wakelin D. (1996) Comparison of
antibody and cytokine responses to primary Giardia muris infection
in H-2 congenic strains of mice. Infection and Immunity 64, 4525–4533
Wright S.G. & Tomkins A.M. (1977) Quantification of the lymphocyte
infiltrate in jejunal epithelium in giardiasis. Clinical and Experi-
mental Immunology 29, 408–412
Yardley J.H., Takano J. & Hendrix T.R. (1964) Epithelial and other
mucosal lesions of the jejunum in giardiasis: jejunal biopsy studies.
Bulletin of John Hopkins Hospital 115, 389–406
Zamchek N., Hoskins L.C., Winawer S.J. et al. (1963) Histology and
ultrastructure of the parasite and the intestinal mucosa in human
giardiasis: effects of atarabine therapy. Gastroenterology 44, 860
Zenian A. & Gillin F.D. (1985) Interactions of Giardia lamblia with
human intestinal mucus: enhancement of trophozoite attachment to
glass. Journal of Protozoology 32, 664–668
143