Am. J. Trop. Med. Hyg., 80(5), 2009, pp. 832–836
Copyright © 2009 by The American Society of Tropical Medicine and Hygiene
832
* Address correspondence to Márcia Marinho, Universidade Estadual
Paulista–Unesp-FOA-Medicina Veterinária-Campus de Araçatuba,
Rua Clóvis Pestana, 793, CEP: 16050-680, Araçatuba, São Paulo,
Brazil. E-mail: mmarinho@fmva.unesp.br
Pulmonary Disease in Hamsters Infected with Leptospira interrogans:
Histopathologic Findings and Cytokine mRNA Expressions
Márcia Marinho,* Itamar Souza Oliveira-Júnior, Cristina Maria Rodrigues Monteiro ,
Silvia Helena Perri, and Reinaldo Salomão
Department of Animal Health and Production, Microbiology Laboratory FOA, Unesp-Estadual Paulista
University, Araçatuba, São Paulo, Brazil; Inflammatory Mediators Laboratory, Geriatrics and Gerontology
Division, Federal University of São Paulo, Brazil; Infectious Diseases Division,
Federal University of São Paulo, Brazil
Abstract. Our aim was to evaluate the pulmonary changes induced by Leptospira interrogans infection in hamsters,
and the gene expression of endogenous mediators in lung fragments during 28 days of observation. The animals were
euthanized on days 4, 7, 14, 21, and 28 post-inoculation. Histopathologic lung analysis showed hemorrhage, pneumonia,
alveolar congestion, and infiltrated cellular areas, with increasing severity until day 21 post-inoculation. Tumor necrosis
factor (TNF)-a mRNA expression enhanced in first days with peak on day 4 and slightly decreased in the final phase.
The interleukin (IL)-10 remained relatively constant throughout the period, with the exceptions of days 4 and 14. The
endothelial nitric-oxide synthesis (eNOS) showed an increased expression on day 4, followed by an augment on days 7
and 14, and remaining constant up to day 28 post-infection. Our results demonstrate that inoculation of L. interrogans
sorovar Icterohaemorrhagiae induced pulmonary lesions, including pulmonary hemorrhage, supporting that the lung is a
target organ.
INTRODUCTION
Leptospirosis is a globally important zoonotic disease
caused by infection with pathogenic Leptospira species.
1
It
affects humans in all continents, in both rural and urban areas,
particularly in developing countries of warm and humid cli-
mate.
2
Vihn and others
3
extracted a glycolipoprotein (GLP)
present in the cell wall of a strain of Leptospira interrogans
serovar Copenhageni that presented a cytotoxic effect against
L929 fibroblast cells in vitro. It was later demonstrated that the
GLP induced cytokine production in peripheral blood mono-
cytes from healthy volunteers.
4,5
The presence of inflamma-
tory cytokines has also been confirmed in sera of patients with
leptospirosis.
6
Marinho and others
7,8
showed that high levels
of tumor necrosis factor (TNF)-a and interleukin (IL)-6 in
the supernatant of peritoneal macrophage cellular culture
of genetically selected mice inoculated with a sample of
Leptospira interrogans serovars Canicola was determined by
immunoenzymatic assays. The lungs are an important target
organ in leptospirosis presenting hemorrhagic pneumoni-
tis with varying degrees of severity.
9,10
The pathophysiology
of pulmonary injury in leptospirosis is poorly understood.
Vascular pulmonary injury is thought to be the outcome
of immunologic mechanisms with a disseminated intravas-
cular coagulation-like reaction caused by Leptospira tox-
ins.
11
Observation under electronic microscopy revealed that
the primary lesion occurs in pulmonary capillary endothe-
lial cells.
12
Andrade and others
13
concluded that leptospiro-
sis profoundly influences the sodium transport capacity of
alveolar epithelial cells and that inadequate handling of pul-
monary fluid can affect the pulmonary function, increasing
the chance of lung injury. Damage to the pulmonary endothe-
lium occurs without evidence of disseminated intravascu-
lar coagulation.
14–16
Nally and others
15
found that in infected
guinea pigs, immunoglobulin and C3 were deposited along
the alveolar basement membrane in a pattern similar to
the one seen in Goodpasture’s syndrome. This finding needs
to be confirmed for human leptospirosis, but it is indica-
tive of the underlying autoimmune process observed in the
severe pulmonary hemorrhagic syndrome.
17
The role of
inflammatory mediators, such as cytokines, in the pathophysi-
ology of sepsis-induced acute lung injury has been extensively
studied.
18
We have previously shown that TNF-a and IL-6
were detected in high levels of bronchoalveolar lavage
(BAL) in rats injected intraperitoneally with Escherichia
coli.
19
In this study we aimed to evaluate the expression
of tissue TNF-a, IL-10, and endothelial nitric-oxide synthesis
(eNOS) mRNA levels in an experimental model of Leptospira-
induced lung dysfunction, assessed by functional and
histologic parameters.
MATERIAL AND METHODS
Animals. The animal experiments were conducted with
approval from the Research Ethics Committee of the Federal
University of São Paulo (São Paulo, Brazil). Male golden
hamsters ( Mesocricetus auratus), weighing 120 to 150 g,
were divided into five groups, each group with six ani-
mals. Each experimental set was comprised of a group with
five inoculated hamsters and one non-infected hamster
per checking point. The hamsters were infected with 10
3
Leptospira of a virulent strain, culture grown in Ellinghausen–
McCullough–Johnson–Harris (EMJH) liquid medium
(Becton Dickinson, Cockeysville, MD) by intraperitoneal
(IP) injection of 1 mL and observed for 4, 7, 14, 21, and
28 days. Negative control animals were injected with 1 mL of
EMJH liquid medium alone.
Inoculum. Leptospira interrogans serovar Icterohae-
morrhagiae (strain n
o
11437) was provided by a FIOCRUZ
Laboratory, Brazil, and maintained in semi-solid Fletcher
medium.
Euthanasia and lung collections. The animals were euth-
anized at the end of the respective day using a 1 mL/100 g
body weight of euthanasia solution sodium pentobarbital
(Tiopentax, Cristália, São Paulo, Brazil) by IP injection. At the