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Applied and Environmental Microbiology, December 2000, p. 5301-5305, Vol. 66, No. 12
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Quantifying Translocation of Listeria
monocytogenes in Rats by Using Urinary Nitric Oxide-Derived
Metabolites
R. Corinne
Sprong,1,*
Marco F. E.
Hulstein,1 and
Roelof
van der
Meer1,2
Department of Nutrition, Quality and Safety, NIZO Food
Research, 6710 BA Ede,1 and Wageningen
Center for Food Sciences, 6700 AN
Wageningen,2 The Netherlands
Received 18 May 2000/Accepted 29 September 2000
 |
ABSTRACT |
The urinary nitric oxide metabolites NO2
and NO3 (summed as NOx) are a
noninvasive, quantitative biomarker of translocation of salmonella from
the intestinal lumen to systemic organs. Listeria monocytogenes is a food-borne gram-positive pathogen that can also cross the intestinal epithelium. In this study, we tested the
efficacy of urinary NOx as a marker of listeria
translocation. Rats (eight per group) were orally infected with
increasing doses of L. monocytogenes; control rats received
heat-killed listeria. The kinetics of urinary NOx and
population levels of listeria in feces were determined for 7 days.
Another group of rats was killed 1 day after infection to verify
translocation by culturing viable listeria from systemic organs. Oral
administration of increasing doses of L. monocytogenes
resulted in a time- and dose-dependent increase in urinary
NOx excretion. Translocation was a prerequisite for
inducing a NOx response, since heat-killed L. monocytogenes did not elevate NOx excretion in urine.
Fecal counts of listeria also showed dose and time dependency.
Moreover, the number of viable L. monocytogenes cells in
mesenteric lymph nodes also increased in a dose-dependent manner and
correlated with urinary NOx. In conclusion, urinary
NOx is a quantitative, noninvasive biomarker of listeria translocation.
| |
INTRODUCTION |
Listeria monocytogenes is
a food-borne gram-positive pathogen that is able to translocate across
the gut epithelium, resulting in listeriosis, i.e., systemic infection.
Most healthy adults experience a limited infection, with at most mild
influenza-like symptoms or, in some cases, gastroenteritis (2, 13,
30). However, listeriosis is extremely dangerous for pregnant
women, causing abortions and stillbirths, and for newborn, elderly, and immunocompromised individuals, causing meningitis, meningoencephalitis, or sepsis (13, 14, 18, 21, 30). In Europe, the incidence of
listeriosis is increasing (2, 14). The rate of mortality caused by listeriosis, excluding abortions, is one of the highest among
bacterial infections. Overall fatality rates of 24 to 44% have been
reported (2, 14, 18, 21). Because of the property of
pathogens to acquire resistance to antibiotics, new approaches to
prevent listeriosis deserve attention. Luminal factors such as gastric
acidity, antimicrobial bile salts and fatty acids, and pancreatic
enzymes contribute to the intestinal nonspecific defenses by killing
pathogens. Therefore, changing the composition of the diet and thus
changing the composition of gastrointestinal contents may affect
colonization and translocation of L. monocytogenes. To study
the efficacy of food components, an animal model of food-derived listeriosis with a quantitative, reliable, and accurate biomarker for
translocation is required. Translocation of L. monocytogenes is observed in rats (24, 28) and mice (26),
making them suitable models. Classically, translocation of listeria in
animal models is determined by microbiological culturing of lymphoid organs (24, 26, 28). This approach has some disadvantages. First, culturing of organs is invasive, demanding killing of animals. Consequently, many animals are needed when more than one time point is
necessary, e.g., when kinetics of both translocation and colonization
have to be determined. Second, microbiological culturing only measures
viable bacteria and not those already killed by immune cells and is
therefore not representative of the total amount of translocated
pathogens. Our laboratory has previously shown that urinary nitrate and
nitrite (summed as NOx), which reflects the production of
nitric oxide (NO) by phagocytic cells (15), is a
quantitative biomarker of salmonella translocation and is useful in
studying the efficacy of functional food components on salmonella
infection (5, 6, 27). Upon translocation, L. monocytogenes infects mesenteric lymph nodes (MLNs), spleen, and
liver (24, 26, 28), resulting in infiltration of neutrophils and monocytes (7). These leukocytes, together with
hepatocytes, Kupffer cells, and splenic macrophages, are able to induce
NO synthase (12, 22, 23, 25, 33). It has been shown that L. monocytogenes induces NO synthase in murine spleen cells
(33) and macrophages (25) and increases the
concentration of NOx in serum and urine when systemically
administered in mice (4, 16). Thus, urinary NOx
may also be a quantitative biomarker of listeria translocation.
Therefore, a strictly controlled experiment was performed with rats
that were intragastrically infected with increasing doses of L. monocytogenes. Urinary NOx and viable listeria in
lymphoid organs and feces were measured.
| |
MATERIALS AND METHODS |
Bacterial culturing.
L. monocytogenes 4B (clinical
isolate, B1242 from the collection of our institute) was routinely
stored at 
80°C in brain heart infusion broth (Difco, Detroit,
Mich.) containing 20% (vol/vol) glycerol. Stock solutions were quickly
thawed, plated on listeria-selective PALCAM plates (Merck, Darmstadt,
Germany), and then incubated aerobically at 37°C for 18 h.
Subsequently, a few colonies were inoculated in brain heart infusion
broth, followed by overnight incubation at 37°C under aerobic
conditions. Bacterial cells were collected by centrifugation (15 min at
3,500 × g), washed three times in sterile saline, and
resuspended in saline containing 3% (wt/vol) sodium bicarbonate. The
virulence of the strain used was sustained by routine oral passage in
Wistar rats, followed by isolation from spleen and liver at day 3 after
oral administration.
Animals and infection.
The experimental protocol was
approved by the animal welfare committee of Wageningen University,
Wageningen, The Netherlands. Male Wistar rats (specific pathogen free,
WU; Harlan, Horst, The Netherlands), 9 weeks old with a body weight of
approximately 325 g, were individually housed in metabolic cages.
The environmental temperature (22 to 24°C), relative humidity (50 to
60%), and dark-light cycle (light, 0600 to 1800 h) were kept constant.
The rats were fed purified diets consisting of 20% casein, 63%
glucose, 5% cellulose, 4% corn oil, and vitamins and minerals
according to the AIN-93 recommendation (25), except for
choline, which was added as choline chloride instead of choline
tartrate, and calcium, which was added as calcium phosphate
(CaHPO4 · 2H2O; 180-mmol/kg diet) instead of calcium carbonate (125-mmol/kg diet). Diets were supplied as
a porridge with 68% dry weight (dry diets mixed with double-distilled water) to minimize food spilling and subsequent contamination of urine
and feces. Rats were given free access to food and demineralized drinking water. Food intake and body weight were recorded every 2 to 4 days preinfection and daily postinfection.
After 2 weeks of habituation to diets and housing conditions, four
groups of 16 rats were orally infected by gastric gavage with 1 ml of
saline containing 3% (wt/vol) sodium bicarbonate with either 8 × 107, 8 × 108, or 8 × 109 viable L. monocytogenes cells or 8 × 109 heat-killed L. monocytogenes cells (90 min
at 60°C). This range is comparable to previously reported doses used
in animal models of oral listeria infection (17, 24, 26).
Viability and the exact number of L. monocytogenes cells in
the inocula were determined by plating on PALCAM. Rats were killed by
inhalation of carbon dioxide at either day 1 or day 7 after
inoculation. Those killed at day 1 of the infection (eight per group)
were used to measure translocation by enumerating viable L. monocytogenes cells in organs. Their MLNs, spleen, and liver were
removed aseptically, weighed, and homogenized (Ultraturrax model Pro
200; Pro Scientific, Inc., Monroe, Conn.) in sterile saline. For
counting of L. monocytogenes cells, 10-fold dilutions were
plated on PALCAM, and plates were subsequently incubated aerobically at
37°C for 36 h. The detection limit for tissue homogenates was
1.7 log10 CFU/ml of homogenates, which implies detection
limits of 1.7 log10 CFU/MLN, 2.1 log10 CFU/spleen, and 2.2 log10 CFU/g of liver (wet weight),
respectively. The other rats were used to determine translocation and
colonization parameters in urine and feces, respectively. Complete 24-h
urine samples were collected daily, starting 2 days before infection until the end of the experiment. Oxytetracycline (Sigma, St. Louis, Mo.; approximately 100 times the MIC for most aerobes) was added to the
urine collection tubes in order to prevent bacterial growth. Urinary
NOx was measured with Griess reagent as described before (27). Recovery of a nitrate standard added to urine ranged
from 92 to 111%. The total listeria-induced increase in
NOx during 7 days was calculated by (
total
NOxi) (7 × NOxb), where
NOxi represents the infection-induced excretion of
NOx and NOxb represents the mean daily
NOx excretion before infection (baseline excretion). Fresh
fecal samples were collected 1 day before infection and at days 1, 3, 5, and 7 of infection. Viable L. monocytogenes cells in
feces were enumerated by plating on PALCAM as described for lymphoid
organs. Detection limits were 1.7 log10 CFU/ml for fecal homogenates, which implies a detection limit of 2.5 log10
CFU/g (wet weight).
Statistics.
Results are expressed as means ± standard
errors (n = 8). Data were checked for normality and
homogeneity of variances by using Shapiro-Wilks's test and Levene's
test, respectively. When normally distributed, differences between
groups were tested by analysis of variance (ANOVA), followed by
Student's t test (one sided) with Bonferroni correction for
multiple comparisons. Otherwise, differences between groups were tested
with the nonparametric Kruskal-Wallis test. Correlation was determined
by using Pearson's product moment. Differences were regarded
significant if P < 0.05. Statistical measurements were
performed with a commercially available statistical package (STATISTICA
edition 1999; StatSoft, Inc., Tulsa, Okla.).
| |
RESULTS |
Rat growth and food intake.
Body weight gain was not affected
by the dose of L. monocytogenes administered. Mean body
weight was 324 g at the start of the experiment, whereas the mean
final body weight was 375 g. Food intake was not significantly
affected by the dose of L. monocytogenes given. Before
infection, average food intake was 23.1 g/day. After infection, mean
food intake was 21.1 g/day.
Intestinal colonization and translocation of Listeria.
Intestinal colonization was determined by enumerating viable L. monocytogenes cells in feces. Figure
1 shows the kinetics of fecal excretion
of viable L. monocytogenes. On day 1 after inoculation, high
levels of listeria were excreted. L. monocytogenes excretion
declined gradually to the detection limit within 1 week after
inoculation. Fecal excretion of viable L. monocytogenes was
dose dependent. As expected, no viable L. monocytogenes
could be detected in feces of rats that received 8 × 109 heat-killed bacteria. No clinical signs of diarrhea
were observed during the course of infection.
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FIG. 1.
Fecal excretion of L. monocytogenes before
and during infection with different doses of this pathogen. Viable or
heat-killed cells (8 × 109) were orally administered
on day 0. Data are expressed as means ± standard errors of eight
rats per group. DL, detection limit. Values on the same day not sharing
the same letter are significantly different (P < 0.05), as determined by ANOVA followed by Student's t
test with Bonferroni correction.
|
|
Translocation was measured by counting the number of viable listeria
cells in lymphoid organs 1 day after inoculation. MLNs
of rats
receiving 8 × 10
9 heat-killed
L. monocytogenes cells were sterile (Fig.
2). The
amount of
L. monocytogenes cells in MLNs of rats infected with
viable bacteria
depended on the dose administered. MLN weight
was not affected by
infection (131 ± 51, 188 ± 40, 127 ± 22, and
109 ± 27 mg for heat-killed listeria at 8 × 10
7, 8 × 10
8, and 8 × 10
9 CFU, respectively).
No viable pathogens could be detected in
the spleens and livers of
infected rats.
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FIG. 2.
Viable counts of L. monocytogenes in MLNs
after oral challenge with different doses of this pathogen. Heat-killed
or viable cells were orally administered on day 0. Listeria cells were
enumerated in MLNs by standard plating techniques 1 day after
inoculation. Data are expressed as means ± standard errors of
eight rats per group. DL, detection limit. Values not sharing the same
letter are significantly different (P < 0.05), as
determined by ANOVA followed by Student's t test with
Bonferroni correction.
|
|
Figure
3A shows the kinetics of urinary
NO
x excretion upon challenge with different doses of
L. monocytogenes. Before infection,
no differences in
urinary NO
x were observed between treatment
groups.
Heat-killed
L. monocytogenes cells did not affect
NO
x excretion. Administration of viable
L. monocytogenes, however,
increased urinary NO
x output,
starting at day 2 of the infection.
Peak values of NO
x
excretion were observed on days 3 to 4 after
inoculation. Urinary
NO
x output returned to baseline levels on
day 6 after
infection, irrespective of the dose administered.
The total
infection-induced NO
x excretion increased in a
dose-dependent
manner (Fig.
3B). The correlation coefficient between
mean viable
listeria counts in MLNs and the mean total
infection-induced NO
x per listeria dose was 0.9902 (
P = 0.01).
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FIG. 3.
Kinetics of urinary NOx excretion (A) and
total infection-induced urinary NOx (B) after oral
challenge with different doses of L. monocytogenes. Viable
or heat-killed cells (8 × 109) were orally
administered on day 0. Data are expressed as means ± standard
errors of eight rats per group. Values not sharing the same letter are
significantly different (P < 0.05), as determined by
ANOVA followed by Student's t test with Bonferroni
correction.
|
|
| |
DISCUSSION |
This study was performed to investigate the efficacy of urinary
NOx as a quantitative biomarker of translocation of
L. monocytogenes. This food-borne pathogen can colonize the
intestinal tract, invade the intestinal mucosa, and spread to systemic
organs, causing sepsis and meningitis in individuals with hampered
immune function. Colonization of listeria depended on the oral dose
(Fig. 1). Our study also showed that the number of viable listeria
cells in MLNs increased with higher doses of orally administered
L. monocytogenes (Fig. 2). We were, however, unable to
detect L. monocytogenes in spleen and liver. This may be
explained by the time point at which organs were sampled, (i.e., day 1 after infection). Although Hirose et al. (17) described that
dissimination of L. monocytogenes to spleen and liver can be
detected on day 1 after intragastric inoculation of 3 × 109 CFU in male F344/Slc rats, other oral models using mice
showed that this pathogen can be detected in the spleen only from the second day and beyond (24, 26). Species and strain
differences (F344/Slc versus Wistar rats in our study) and, probably,
the distinct diets (rodent chow versus purified diets in our study) may
account for this discrepancy. Literature data on the kinetics of
translocation to MLNs are consistent; all studies showed translocation to MLNs on day 1 after inoculation (17, 24, 26). Although the time of spreading to spleen and liver may depend on the animal model used, these studies as well as our experiment clearly show that
extraintestinal dissemination of L. monocytogenes occurs in
a dose-dependent manner in both rats and mice (26, 30).
NO synthesis is a primary reaction of phagocytic cells to microbes
(19, 23) or bacterial components such as lipopolysaccharide (19, 31) and is known to respond in a dose-dependent manner (3, 19). NO is rapidly oxidized to
NO2 and NO3
(20), which are excreted in urine (15). Our
laboratory has previously shown that urinary NOx is a more
discriminative biomarker for salmonella translocation than enumeration
of systemic bacteria from organs (27). Analysis of urinary
NOx is also noninvasive, not requiring killing of the
animals. L. monocytogenes is also known to stimulate NO
production in murine peritoneal macrophages (25) and spleen
cells in vitro (33). In vivo studies with mice have shown
that systemically administered L. monocytogenes increases
NOx in blood and urine in a dose-dependent manner (4, 16). Using the NO synthase inhibitor
NG-monomethyl-L-arginine, Boockvar et al.
(4) proved that listeria-mediated urinary NOx
was derived from induced NO synthase activity. Our study showed that
orally administered L. monocytogenes provoked urinary
NOx excretion in rats. Values peaked at days 3 and 4 of the
infection and gradually declined thereafter, with baseline levels
reached at day 6. These kinetics are remarkably consistent with the
kinetics reported for bacterial counts in lymphoid organs (24,
26) after oral listeria infection and with the kinetics of
inducible NO synthase mRNA in murine peritoneal macrophages (4) after intravenous administration of L. monocytogenes. Urinary NOx was proportional to the
amount of orally administered L. monocytogenes (Fig. 3) and
correlated with the number of viable counts of listeria in MLNs
(r = 0.99). Using enteroinvasive and noninvasive
pathogens, Witthöft et al. (32) showed that invasion
is a prerequisite for activation of the inducible NO synthase. In
addition, oral inoculation of a pathogenic E. coli strain
that colonizes the intestinal tract, but is incapable of translocation,
does not result in increased urinary NOx (I. M. J. Bovee-Oudenhoven, unpublished results). Therefore, translocation is
a prerequisite for induction of urinary NOx excretion. The
observation that heat-killed L. monocytogenes is ineffective
in stimulating urinary NOx excretion also indicates that
translocation is indeed obligatory for induction of the NO response by
this pathogen. Thus, urinary NOx is a suitable biomarker
for L. monocytogenes translocation and can therefore be used
to study the efficacy of functional food components in animal models of listeriosis.
The kinetics of the urinary NOx response after listeria
infection is different from that observed after salmonella infection (6, 27), which increases from day 3 and reaches peak values on days 6 and 7, returning to baseline levels on day 12 after inoculation. This may be explained by the time course of infection. Compared with listeria, salmonella infection is slowly cleared in rats.
Whereas viable listeria counts in systemic organs increase to peak
values at day 3 of the infection and are completely cleared 7 days
after inoculation (24, 28), viable salmonella counts in
lymphoid tissue start to increase at day 3 and beyond (10), with considerable amounts still detectable in MLNs at day 7 of infection (27).
It has been shown that NOx is increased in plasma and urine
of patients with acute infective gastroenteritis induced by pathogens such as salmonella, shigella, and campylobacter (1, 8, 9, 11). Plasma nitrate correlated with the severity of infection (8). Thus, besides application to the quantitative
determination of orally acquired listeriosis in animal models, urinary
NOx might also be useful to monitor the efficacy of
treatment of listeriosis in humans.
In conclusion, a dose-dependent relationship between urinary
NOx and translocation of listeria exists in a rat model of
orally acquired L. monocytogenes infection. Therefore,
excretion of NOx in urine can be used as a noninvasive
biomarker for quantifying translocation of this pathogen in animal
models and may provide a tool to study the efficacy of functional food
components. Besides this application, urinary NOx may also
be used to monitor the severity of listeriosis in humans.
| |
ACKNOWLEDGMENTS |
We thank Maria Faassen-Peters and Wilma Blauw (Small Animal
Center, Wageningen University, Wageningen, The Netherlands) for skillful biotechnical assistance and George Mahulette (NIZO Food Research) for analysis of urinary nitric oxide metabolites.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: NIZO Food
Research, Department of Nutrition, Quality and Safety, P.O. Box 20, 6710 BA Ede, The Netherlands. Phone: 31 318 659511. Fax: 31 318 650400. E-mail: Sprong{at}NIZO.nl.
| |
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Applied and Environmental Microbiology, December 2000, p. 5301-5305, Vol. 66, No. 12
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
