Arq. Bras. Med. Vet. Zootec., v.60, n.3, p.

667-674, 2008

Pulmonary, microbiological and hematological changes in Crotalus durissus terrificus

(Serpentes, Viperidae) parasitized by nematodes of the genus Rhabdias
(Nematoda, Rhabdiasidae)

[Alterações Pulmonares, microbiológicas e hematológicas em Crotalus durissus terrificus (Serpentes, Viperidae)

parasitadas pelos nematódeos do gênero Rhabdias (Nematoda, Rhabdiasidae)]

K.R. Santos1, R.K. Takahira2, V.L.M. Rall3, C. Calderón1, J.L. Sequeira2, R.J. Silva3*

1
Aluno de pós-graduação - FMVZ-UNESP – Botucatu, SP
2
Faculdade de Medicina Veterinária e Zootecnia – UNESP – Botucatu, SP
3
Instituto de Biociências - UNESP – Botucatu, SP
Distrito de Rubião Júnior
18618-000 - Botucatu, SP

ABSTRACT

This study reported the pulmonary, microbiological, and hematological alterations in Crotalus durissus
terrificus parasitized by nematodes of the genus Rhabdias. Histological, microbiological, and
hematological analysis were performed on parasitized (n=6) and non-parasitized (n=6) snakes.
Granulocytic and mononuclear cell infiltrates in the pulmonary parenchyma and epithelium were also
observed during the histological analysis of parasitized snakes. Microbiological analysis of parasitized
animals revealed the following Gram-negative bacteria: Citrobacter divergens, Burkholderia cepacia,
Stenotrophomonas maltophilia, Proteus vulgaris, Enterobacter sakazakii, Enterobacter ammnigenus,
Pseudomonas aeruginosa, Pantoea sp. and Providencia rettgeri. In non-parasitized snakes, the following
species were identified: B. cepacia, Pseudomonas fluorescens, and Acinetobacter baumanii. Increased
levels of plasmatic protein, decreased lymphocyte counts, and normal red blood cell values were observed
in parasitized animals.

Keywords: snake, Crotalus durissus terrificus, Rhabdias spp., histopathology, microbiology, hematology

RESUMO

Este trabalho relata as alterações pulmonares, microbiológicas e hematológicas em Crotalus durissus

terrificus parasitadas pelo nematódeo do gênero Rhabdias. As análises histológicas, microbiológicas e
hematológicas foram realizadas em serpentes parasitadas (n=6) e não parasitadas (n=6). Foram
observados infiltrados de células granulocíticas e mononucleares no parênquima pulmonar durante a
análise histopatológica das serpentes parasitadas. A análise microbiológica revelou as seguintes
bactérias Gram-negativas; Citrobacter divergens, Burkholderia cepacia, Stenotrophomonas maltophilia,
Proteus vulgaris, Enterobacter sakazakii, Enterobacter ammnigenus, Pseudomonas aeruginosa, Pantoea
sp. e Providencia rettgeri. Nas serpentes não parasitadas foram identificadas: B. cepacia, Pseudomonas
fluorescens e Acinetobacter baumanii. Nos animais parasitados observaram-se: aumento da
concentração de proteína plasmática, diminuição da contagem de linfócitos, e valores normais de
hematimetria.

Palavras-chave: serpente, Crotalus durissus terrificus, Rhabdias spp., histopatologia, microbiologia,

hematologia

Recebido em 28 de agosto de 2007

Aceito em 13 de março de 2008
*Autor para correspondência (corresponding author)
E-mail: reinaldo@ibb.unesp.br
 Santos et al.

INTRODUCTION historesin (2-hydroxyethyl methacrylate) and

4µm sections were stained with hematoxylin-
Several species of amphibians and reptiles can be eosin and examined with a computerized system
parasitized by rhabdiasid nematodes (Yamaguti, for image analyses3. The morphology of the
1961). Nematodes of the genus Rhabdias have lungs and cell counts were evaluated using these
been found in the lungs of several species of slides. The cell counts were performed within ten
Brazilian snakes (Vicente et al., 1993; Araújo et 0.3mm2 areas, observed at a magnification of
al., 1999; Silva et al., 2001) and high infection 400x.
rates with these nematodes have been reported in
Crotalus durissus terrificus. Silva et al. (2001) Microbiological examinations were performed
studied the frequency of nematodes in 24 C. d. with other lung fragments, which were collected,
terrificus specimens and found infection rate of put in tubes with Brain-Heart Infusion broth
70.8% with pulmonary nematodes. (BHI)4, and incubated at 30°C for 24 hours. After
incubation, samples of broth were plated onto
Rhabdiasid nematodes inhabit the snake lungs media selective for Pseudomonas (cetrimid)3,
and can affect the state of health of these Aeromonas (starch ampicillin agar)3, and Gram-
animals. It has been reported that Rhabdias spp. negative enteric bacilli (xylose lysine
can cause a “verminous” pneumonia, deoxycholate agar and McConkey agar), and
characterized by a gaping mouth, wheezing, and were incubated at 30°C for 24 hours. After this
exudates from the trachea (Klingenberg, 1993; period, the typical colonies were transferred to
Mader, 1996). tubes containing tryptic soy agar (TSA)3, and
incubated under the same conditions. The strains
However, studies on the effects of the parasitism were tested for oxidase production and seeded in
of those helminths on the snake respiratory triple sugar iron agar (TSI)3 before incubating at
system are rare. The objective of this 30°C for 24 hours. After the preliminary
investigation was to report the pulmonary, biochemical results, the isolates were identified
microbiological, and hematological alterations in using the API 20 kit5 for identification of
C. d. terrificus parasitized by nematodes of the Enterobacteriaceae or the API 20 NE kit for
genus Rhabdias. identification of non-fermenting Gram-negative
bacilli.
MATERIAL AND METHODS
Blood (0.5ml) was directly collected from the
This study was performed from March 2003 to vena cava immediately after euthanasia in 3%
February 20051. Fecal samples of recently ethylene diaminetetra-acetic acid (EDTA)
captured adult C. d. terrificus snakes from the anticoagulant solution. The complete blood cell
Botucatu region, State of São Paulo, Brazil, were counts were performed in a Neubauer chamber
analyzed by fecal flotation test (Hoffman, 1987) using 0.01% toludine blue in saline solution. The
and 12 snakes were grouped as parasitized (n=6) correction for thrombocytes was based on a
and non-parasitized (n=6) by rhabdiasid differential cell count of 200 cells. Hemoglobin
nematodes. levels were determined by the
cyanmethemoglobin method by centrifuging the
The snakes were euthanised with thiopental cyanmethemglobin reagent-blood mixture
sodium2 given intramuscularly. Lungs were for three minutes and measuring
collected for histological and microbiological spectrophotometrically (Jain, 1993; Feldman et
analyses and blood was collected for al., 2000; Raskin, 2000). The packed cell volume
hematological examination. was determined by the microhematocrit method,
centrifuging microhematocrit tubes at 12,000 x g
For histological evaluation, lungs samples were for five minutes. The differential leuckocyte
preserved in 10% formalin and then embedded in counts were performed on blood smears stained

1
This study was approved by the Ethics Commission 3
(53/2002-CEEA) of the Universidade Estadual Paulista, Lite Qwin 2.5, Leica Microsystems - Wetzlar, Germany.
4
Botucatu, SP OXOID - São Paulo, Brazil.
2
Thiopentax, Cristália - Itapira, SP, Brazil. 5
Biomérieux - Marcy l'Etoile, France.

668 Arq. Bras. Med. Vet. Zootec., v.60, n.3, p.667-674, 2008
 Pulmonary, microbiological and hematological…

by Giemsa. Total plasma protein levels were Microbiological examinations of parasitized and
measured using an Atago refractometer (Jain, non-parasitized snake lungs showed that only
1986). one (16.7%) of the parasitized animals did not
present bacterial growth, while in the other five
Erythrocytic data from the parasitized and non- (83.3%), nine bacteria species were identified. In
parasitized animals were compared by the Student t contrast, in the non-parasitized animals, bacterial
test. Leucogram data were analyzed by the Mann- growth was only observed in 33% and only three
Whitney non-parametric test. Statistical bacterial species were identified (Table 1).
significance was set at 5%. All statistical analyses
were carried out using the SigmaStat 2.0 software Hematological evaluation of the parasitized and
(Jandel Corporation). non-parasitized snakes demonstrated only an
increase in plasma protein concentration
RESULTS (P=0.011) in parasitized animals. For the other
hematological variables, differences were not
The histological evaluation of parasitized snake
observed among the experimental groups
lungs showed the presence of granulocytic and
(P>0.05) (Table 2). Leucometric analysis only
mononuclear infiltrates. These alterations were also
observed in some non-parasitized animals, but at a
showed a decrease in lymphocyte cell counts
lower level (Fig. 1). The medians of granulocytic (P=0.009) in parasitized animals. For the other
cell counts of the parasitized and non-parasitized leucometric variables, differences were not
snake lungs were 14.8 and 0.95, respectively observed among the experimental groups
(P<0.05) (Fig. 2). (P>0.05) (Table 3).

Figure 1. Histopathology of Crotalus durissus terrificus lung. (A-B) Parasitized by nematodes of the genus Rhabdias;
pulmonary parenchyma and epithelium showing a large amount of granulocytic cell infiltrates (arrows). (C-D)
Pulmonary parenchyma and epithelium from a non-parasitized animal. HE. (A, B, and D, magnification of 1000x; C,
magnification of 400x).

Arq. Bras. Med. Vet. Zootec., v.60, n.3, p.667-674, 2008 669
 Santos et al.

30

25 *
Number of granulocytic cells

20

15

10

0
Non-parasitized Parasitized
Figure 2. Distribution of the medians of granulocytic cell counts in histological sections of Crotalus
durissus terrificus lungs parasitized (n=6) and non-parasitized (n=6) by nematodes of the genus Rhabdias.
Each boxplot represents 25-75 percentile values, with the median as an internal line; the error bars
represent the 10 and 90 percentiles; the circles represent the outliers. *P<0.05.

Table 1. Bacteria identified in the lungs of Crotalus durissus terrificus, parasitized (n=6) and non-
parasitized (n=6) by nematodes of the genus Rhabdias
Snake Parasitized Snake Non-parasitized
2 Citrobacter divergens 1 Acinetobacter baumanii
Burkholderia cepacia
Stenotrophomonas maltophilia
7 Negative 3 Negative
8 Proteus vulgaris 4 Negative
9 Enterobacter sakazakii 5 Negative
Enterobacter amnigenus
Pantoea sp.
10 Pseudomonas aeruginosa 6 Burkholderia cepacia
Pantoea sp. Pseudomonas fluorescens
11 Providencia rettgeri 12 Negative
Proteus vulgaris

670 Arq. Bras. Med. Vet. Zootec., v.60, n.3, p.667-674, 2008
 Pulmonary, microbiological and hematological…

Table 2. Erythrogram findings in the lungs of Crotalus durissus terrificus parasitized (n=6) and non-parasitized
(n=6) by nematodes of the genus Rhabdias
Erythrocyte Thrombocyte Hemoglobin PCV Plasma MCV MCHC
Animal
(N/µl) (N/µl) (g/dl) (%) proteins (g/dl) ( Fl ) (%)
Non-parasitized
1 625,000 12,269 9.5 34 3.0 548 27.9
3 565,000 13,938 8.3 29 3.8 518 28.6
4 552,500 12,640 10 32 3.2 582 31.3
5 400,000 15,000 8.3 27 3.2 675 30.7
6 355,000 10,634 7.4 29 4.4 816 25.8
12 525,000 13,920 9.5 27 4.4 514 35.2
Mean 503,750 13,066 8.8 30 3.7 608 30.0
SD 104,088 1,547 0.9 2.8 0.6 117 3.2
Parasitized
2 485,000 4,331 8.5 32 4.3 687 26.1
7 475,000 17,750 7.6 26 4.6 547 29.2
8 375,000 4,187 6.4 21 4.6 560 30.4
9 475,000 9,056 8.5 30 4.8 631 28.3
10 352,500 17,250 7.9 26 4.6 738 30.3
11 320,000 17,000 8.3 22 4.2 687 37.7
Mean 413,750 11,596 7.8 26 4.5 641 30.0
SD 72,968 6,529 0.8 4.3 0.2 76 3.9
PCV: packed cell volume; MCV: mean corpuscular volume; MCHC: mean corpuscular hemoglobin concentration; SD:
standard deviation.

Table 3. Leucogram findings in the lungs of Crotalus durissus terrificus parasitized (n=6) and non-parasitized
(n=6) by nematodes of the genus Rhabdias
Leukocyte Lymphocyte Monocyte Heterophil Basophil Eosinophil Azurophil
Animal
N/µl N/µl N/µl N/µl N/µl N/µl N/µl
Non-parasitized
1 6,606 1,981.8 66.1 3,038.8 462.4 132.1 924.8
3 8,186 5,730.0 81.9 818.6 491.2 409.3 654
4 7,110 4,450.4 142.2 1,493.1 284.4 142.2 497.7
5 3,750 2,437.5 300.0 187.5 262.5 262.5 300
6 11,992 8,633.7 239.9 2,038.5 0 120.0 959.3
12 10,080 4,637.0 504.0 806 0 0 4,133.0
Median 7,648 4,543.7 191 1,155.9 273.4 137.1 789.8
SIQR 1,737 1,646.5 109.5 616.3 231.2 71.3 230.8
Parasitized
2 3,150 913.5 0 1,228.52 0 220.5 787.5
7 9,053 3,892.6 0 1,720.0 0 271.6 3168.4
8 12,563 879.3 1,381.9 8,416.8 0 376.8 1507.5
9 3,351 1,105.8 0 1,340.3 0 0 904.7
10 4,485 897.0 0 1,524.9 179.4 0 1883.7
11 3,230 871.1 323 775.2 0 0 1550.4
Median 3,918 905.3 0 1,432.6 0 110.2 1,528.9
SIQR 2,912 113.3 161.5 246.0 0 135.8 489.5
SIQR: semi-interquartile range

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 Santos et al.

DISCUSSION when they penetrate their hosts, they can

contaminate them. The present study supports
Histological analyses of the parasitized snakes this hypothesis. The major observation in this
showed an infiltrate of granulocytic and respect was the occurrence of bacteria of the
mononuclear cells in the lungs. These alterations genus Pantoea in the lungs of snakes infected
were also observed in non-parasitized snakes, but with rabdiasid nematodes. The Pantoea is a
at a lower level. Data regarding the Gram-negative bacillus frequently isolated from
histopathology of lungs of snakes parasitized by soil, water, plants, seeds, animals, and humans
rhabdiasid nematodes are rare. Samora (1993) (Manulis and Barash, 2003). Animal and human
reported acute parasitic enteritis caused by infections by Pantoea spp. occur in debilitated
Rabdias vellardi in Bothrops moojeni. individuals; however, these bacteria are more
Kolesnikovas (1997) noted that 53% of C. d. frequently isolated from soil and plants (Asis and
terrificus infected by R. vellardi presented Adachi, 2003; Manulis and Barash, 2003). The
pneumonia; while Klingenberg (2000) reported finding of Pantoea sp. in the lungs of snakes
that verminous pneumonia in snakes is infected with Rhabdias spp. reinforces the
characterized by mouth opening, breathing hypothesis that rhabdiasid larvae can carry soil
difficulty, and exudate expulsion via trachea. microorganisms to internal organs of their hosts.
Similar results were observed in the present
study; however, there have been no reports, to There are a number of reports on the microbiota
date, on the presence of granulocytic and of snakes. However, few of these related C. d.
mononuclear cell infiltrates in association with terrificus. Moreno et al. (1973) isolated
Rhabdias spp. Infection. Although, such Citrobacter sp. (35%), Proteus vulgaris (16.4%),
histological findings were observed by Morganella morgani (=Proteus morgani)
Tucunduva et al. (2001) in an experimental study (14.4%), and Providencia rettgeri (=Proteus
of inflammation in the subcutaneous tissue of rettgeri) (13%) from feces of this host species.
Boa constrictor constrictor. However, no data regarding lungs microbiota are
available for C. d. terrificus. Thus, the data of the
Microbiological evaluations showed that 83% of present study contribute to the knowledge of the
the parasitized snakes presented bacterial growth. microbiota in this species.
In contrast, for the non-parasitized snakes, this
percentage was 33%. The number of bacterial Klingenberg (1993) reported that rhabdiasid
species found in parasitized snakes was higher nematodes can cause a “verminous” pneumonia
than the non-parasitized species (nine versus in snakes that is characterized by a gaping
three). These data suggest an association mouth, wheezing, and exudate from trachea.
between the infection by rhabdiasid nematodes Conversely, Marcus (1981) reported few, or the
and bacterial occurrence, and indicate that absence of clinical signs in snakes infected with
rhabdiasid nematode larvae can carry soil R. vellardi. Pneumonia in snakes was described
microorganisms to internal organs of their hosts. in the presence of Aeromonas hydrophila
(Marcus, 1971). Hilf et al. (1990) isolated
Rhabdiasid nematodes have a direct life cycle Proteus vulgaris in snakes from the Boidae
with a free-living generation and a parasitic family and found pneumonia in two animals that
phase. The eggs deposited in the lungs by the died. These data show that the pneumonia was
parthenogenetic females pass through the associated with lungs bacterial infection. Thus, it
respiratory system, are swallowed and then is suggested that the “verminous” pneumonia
eliminated in the feces of the host. Larvae hatch reported by Klingenberg (1993) may be caused
and first, second, and third-stage larvae develop or worsened by the microorganisms that affect
in the external environment. Infective larvae the lungs. In the case of Rhabdias spp.,
penetrate the skin and migrate to the lungs where pneumonia may be caused by soil
they become mature and produce eggs microorganisms carried to the lungs.
(Anderson, 2000).
Some bacteria identified in this study (Table 1)
First and second-stage larvae ingest have been previously described as causing
microorganisms and organic material in the pneumonia in snakes. Hilf et al. (1990) found P.
external environment (Cheng, 1986) and then, rettgeri in the lungs of Boidae snakes and

672 Arq. Bras. Med. Vet. Zootec., v.60, n.3, p.667-674, 2008
 Pulmonary, microbiological and hematological…

demonstrated that in animals with pneumonia, reptiles should be analyzed with caution since
the number of Gram-negative bacilli was external factors, such as environmental
significantly higher than in normal animals. In variations, may inhibit or intensify the response
the same study, two snakes that died as a of the animal to a disease (Feldman et al., 2000;
consequence of pneumonia were necropsied and Campbell, 2004).
the lungs were analyzed. The microbiological
analyses of the first snake revealed that its lungs The present study showed that C. d. terrificus
presented a high infection by A. hydrophila and, snakes parasitized by nematodes of the genus
in the second snake, Salmonella sp., Citrobacter Rhabdias present granulocytic and mononuclear
sp., and Enterococcus sp. were identified. cell infiltrates in their lungs, a high diversity of
microbiota, and few hematological alterations.
In the hematological examinations, few Thus, this nematode may be considered as a
alterations were detected when parasitized and significant health problem in snakes and sanitary
non-parasitized snakes were compared. Plasma handling must be employed when such animals
protein levels and lymphocyte counts were the are introduced into captivity.
only variables that presented statistically
significant differences. Plasma protein levels
were increased in parasitized snakes in relation ACKNOWLEDGEMENTS
to non-parasitized snakes; however, according to
Feldman et al. (2000) and Raskin (2000), The authors wish to thank the Fundação para o
animals from both groups presented normal Desenvolvimento da UNESP (FUNDUNESP)
levels. The observed values from hematological and the Coordenadoria de Aperfeiçoamento de
examinations were also similar to only one Pessoal de Nível Superior (CAPES) for the
hematological study carried out with Bothrops grants to K. R. dos Santos.
leucurus in Brazil (Grego et al., 2006).

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