Veterinary Microbiology 172 (2014) 339–344

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Veterinary Microbiology
journal homepage: www.elsevier.com/locate/vetmic

Short Communication

Canis lupus familiaris involved in the transmission of

pathogenic Yersinia spp. in China
Xin Wang a,1, Junrong Liang a,1, Jinxiao Xi b,1, Jinchuan Yang c,1, Mingliu Wang d,1,
Kecheng Tian e,1, Jicheng Li e, Haiyan Qiu a, Yuchun Xiao a, Ran Duan a,
Haoshu Yang a, Kewei Li a, Zhigang Cui a, Meiying Qi f, Huaiqi Jing a,*
a
National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention,
State Key Laboratory for Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of
Infectious Diseases, Beijing, China
b
Gansu Provincial Centre for Disease Control and Prevention, Lanzhou, China
c
Xuzhou Municipal Centre for Disease Control and Prevention, Xuzhou, China
d
Guangxi Zhuang Autonomous Region Center for Disease Control and Prevention, Nanning, China
e
Guizhou Provincial Centre for Disease Control and Prevention, Guiyang, China
f
Qinghai Institute for Endemic Diseases Control and Prevention, Xining, China

A R T I C L E I N F O A B S T R A C T

Article history: To investigate canines carrying pathogens associated with human illness, we studied their
Received 31 December 2013 roles in transmitting and maintaining pathogenic Yersinia spp. We examined different
Received in revised form 28 March 2014 ecological landscapes in China for the distribution of pathogenic Yersinia spp. in Canis lupus
Accepted 18 April 2014 familiaris, the domestic dog. The highest number of pathogenic Yersinia enterocolitica was
shown from the tonsils (6.30%), followed by rectal swabs (3.63%) and feces (1.23%). Strains
Keywords: isolated from plague free areas for C. lupus familiaris, local pig and diarrhea patients shared
Canine the same pulsed-field gel electrophoresis (PFGE) pattern, indicating they may be from the
Pathogenic Yersinia spp.
same clone and the close transmission source of pathogenic Y. enterocolitica infections in
Multi-host pathogens
these areas. Among 226 dogs serum samples collected from natural plague areas of
Pulsed-field gel electrophoresis
Zoonosis
Yersinia pestis in Gansu and Qinghai Provinces, 49 were positive for F1 antibody, while the
serum samples collected from plague free areas were all negative, suggested a potential
public health risk following exposure to dogs. No Y. enterocolitica or Yersinia
pseudotuberculosis was isolated from canine rectal swabs in natural plague areas.
Therefore, pathogenic Yersinia spp. may be regionally distributed in China.
ß 2014 Elsevier B.V. All rights reserved.

1. Introduction

Yersiniosis is a zoonosis found worldwide with three

* Corresponding author at: National Institute for Communicable
Disease Control and Prevention, Chinese Center for Disease Control
and Prevention, State Key Laboratory for Infectious Disease Prevention
and Control, 155 Changbai Road, Changping District, 102206 Beiing,
China. Tel.: +86 10 58900758; fax: +86 10 58900070.
E-mail address: jinghuaiqi@icdc.cn (H. Jing).
1
These authors contributed equally to this study.
human and animal pathogens, Yersinia enterocolitica,
Yersinia pestis, and Yersinia pseudotuberculosis. Y. pestis
causes plague, a disease of rodents or other wild mammals
usually transmitted by fleas and often is fatal; Y.
pseudotuberculosis and Y. enterocolitica are enteric food
and water-borne pathogens, they are entero-pathogens,
and can cause mesenteric lymphadenitis and septicemia
(Achtman et al., 1999; Spinner et al., 2010).

http://dx.doi.org/10.1016/j.vetmic.2014.04.015
0378-1135/ß 2014 Elsevier B.V. All rights reserved.
340 X. Wang et al. / Veterinary Microbiology 172 (2014) 339–344

In plague free areas, Canis lupus familiaris are a
potential source of human infections for Y. enterocolitica
and Y. pseudotuberculosis (Hetem et al., 2013; Murphy
et al., 2010; Stamm et al., 2013; Wang et al., 2010). While,
in natural plague areas, Shepherd dogs have a habitat of
eating diseased or dead marmot, the primary host of Y.
pestis in the endemic region, and therefore dogs may be
infected with Y. pestis. However, canines were thought to
be resistant to Y. pestis infection (Rust et al., 1971), so they
are believed to be a sentinel for surveillance (Li et al.,
2008).
Here we selected different ecological landscapes
including plague free areas, natural plague areas, and
conducted a study to investigate the distributions of
Yersinia spp. in C. lupus familiaris in China.
collected (Table 1); 126 serum, rectal swab and tonsil of
dogs were also collected in Guizhou southwest China
(Table 1).
2.1.2. Natural plague areas
We selected present natural plague areas Gansu and
Qinghai provinces northwest China for investigation. On
these areas, we collected 105 blood and rectal swab
samples in Gansu and 121 from Qinghai for each dog
(tonsil samples were not taken from shepherd dogs as they
were aggressive) (Table 1).
The locations of each sampling provinces were shown
in Fig. 1.
2.2. Bacterial isolation and identification

Blood samples from dogs were used for isolation of Y.

2. Materials and methods
2.1. Study areas and sampling
2.1.1. Plague free areas
324 specimens of feces were collected in Xuzhou,
Jiangsu Province on the eastern coast of China during five-
years routine surveillance. For the special investigation,
670 serum, rectal swab and tonsil of the dogs were
collected in Jiangsu (Table 1). 190 serum, rectal swab and
140 tonsil of dogs in Guangxi southeast China were
pestis using the conventional method (Zhang et al., 2012).
For other Yersinia spp., sample enrichment (tonsil and
rectal swabs) was performed using enrichment in phos-
phate-buffered saline with sorbitol and bile salts (PSB) at
4 8C for 21 d to isolate strains (Liang et al., 2012). Nucleic
acids from all enrichment (except serum) were extracted
using a DNA nucleic acid extraction kit (Tiangen, China).
The Y. enterocolitica conserved gene foxA, the pathogenic
gene ail; and the inv gene of Y. pseudotuberculosis were
amplified (Liang et al., 2012). The samples positive for one

Table 1
Yersinia spp. isolation details and detection results.

Different Province Types of Numbers Results

ecological samples
landscapes
Y. Positive Y. Y. Y. Y.
pestis for F1 enterocolitica pseudotuberculosis frederiksenii/ kristensenii
antibody intermedia
Pathogenic Non-pathogenic

Natural plague Gansu Serum 105 0 27 – – – – –

areas Feces 0 – – – – – – –
Rectal 105 – – 0 1 0 0 0
swab
Tonsil 0 – – – – – – –
Qinghai Serum 121 0 22 – – – – –
Feces 0 – – – – – – –
Rectal 121 – – 0 2 0 0 0
swab
Tonsil 0 – – – – – – –

Plague free Jiangsu Serum 670 – 0 – – – – –

areas Feces 324 – – 4 37 0 0 0
Rectal 670 – – 94 12 0 0 0
swab
Tonsil 670 – – 94 12 0 0 0
Guangxi Serum 190 – 0 – – – – –
Feces 0 – – – – – – –
Rectal 190 – – 5 5 10 2 0
swab
Tonsil 140 – – 5 5 10 2 0
Guizhou Serum 126 – 0 – – – – –
Feces 0 – – – – – – –
Rectal 126 – – 3 11 4 6 2
swab
Tonsil 126 – – 3 11 4 6 2

Note: the serum, tonsil and rectal swab were matched set of collected samples for each dog in each province; the feces were only collected in Jiangsu
province.
 X. Wang et al. / Veterinary Microbiology 172 (2014) 339–344 341

Fig. 1. The PFGE patterns of Y. enterocolitica and Y. pseudotuberculosis, and antibody to the Y. pestis specific Fraction 1 antigen among C. lupus familiaris in
several different ecological landscapes in China. (A-1) Seasonal distribution of Y. enterocolitica from matched sets of dog tonsil and rectal swab samples from
Xuzhou, Jiangsu Province. (A-2) The detection of antibody to the Y. pestis specific Fraction 1 antigen of C. lupus familiaris in the Gansu and Qinghai foci. (A-3)
A marmot on plateau was captured by a shepherd dog. (A-4) The host of plague, marmots, moved around the caves in the prairie, the cattle were eating grass
beside them. (A-5) Three shepherd dogs on the plateau. (B) Cluster analysis of pathogenic Y. enterocolitica strains isolated from dogs and from local pig and
from diarrhea patients in Jiangsu Province. (C-1) Cluster analysis of pathogenic strains of Y. enterocolitica isolated from dogs and from local pig and from
diarrhea patients in Guangxi and Guizhou Province. (C-2) Cluster analysis of all Y. pseudotuberculosis strains isolated from dogs and local pigs in Guangxi and
Guizhou Province.

or two foxA and ail genes were then inoculated onto
Yersinia-selective agar (CIN agar, Difco) for isolation. API
20E (bioMérieux) were used to identify the isolates.
Serotypes and biotypes of the Y. enterocolitica were
followed by our previous study (Wang et al., 2008);
Serotype identification of the Y. pseudotuberculosis strains
was conducted using multiplex PCR (Bogdanovich et al.,
2003). Virulence genes (ail, ystA, ystB, virF, and yadA) of Y.
enterocolitica isolates were amplified. Pathogenic Y.
enterocolitica strains were positive for all (ail+, ystA+, virF+,
and yadA+); however, some pathogenic strains lost
virulence genes encoded on the plasmid virF and yadA ,
, but still had ail+ and ystA+ located on the chromosome
(Wang et al., 2008).
342 X. Wang et al. / Veterinary Microbiology 172 (2014) 339–344
2.3. Indirect hemagglutination test (IHA)
IHA (Suzuki and Hotta, 1979) was used to measure
the specific F1 antibody titer including a F1 antigen
inhibition control, negative and positive controls (Wang
et al., 2011). All the serum and blood samples were
tested and the titers equal to or more than 1:20 were
scored positive.
2.4. PFGE assay
The pulsed-field gel electrophoresis (PFGE) method
was used to analyze the pathogenic Y. enterocolitica and all
of the Y. pseudotuberculosis strains isolated from dogs. Y.
enterocolitica plugs were digested with 25 U NotI and
electrophoresed with a pulse time from 2 s to 20 s, for 18–
19 h at 20 V. Y. pseudotuberculosis was digested with 25 U
NotI or FseI and electrophoresed with a pulse time from 2 s
to 18 s. Clustering of the band patterns was performed
with BioNumerics software (Version 5.1) using the
unweighted-pair group method with average linkages
(UPGMA) and a Dice coefficient with a 1.5% tolerance
(Liang et al., 2012).
3. Results
Among 3684 specimens collected from dogs in this
study, we isolated 174 Y. enterocolitica strains. All of the
107 pathogenic strains were bioserotype 3/O: 3; while for
the nonpathogenic isolates, nine were 1A/O: 8, nine were
1A/O: 5, others were 1A/undetermined serotype. The
isolation rate of pathogenic Y. enterocolitica was shown to
be highest from the tonsils (6.3%), followed by rectal
swabs (3.63%) and feces (1.23%) for the dogs. However,
for Y. pseudotuberculosis, the detection rate from rectal
swabs (0.99%) was higher than tonsils (0.11%). In
Guangxi, one serotype O: 1b, three O: 14, two O: 4b,
one O: 5a, two O: 6 and one undetermined serotype of Y.
pseudotuberculosis were isolated; in Guizhou, one O: 4b,
one O: 6, one O: 8 and one undetermined serotype were
isolated. No Yersinia strains were isolated from serum
samples. In addition, eight strains of Yersinia frederiksenii/
intermedia strains and two Y. kristensenii strains were
isolated (Table 1).
From three plague free areas, Jiangsu, Guizhou and
Guangxi provinces, 936 matched sets of dog tonsil and
rectal swab samples were collected. In Jiangsu province,
106 Y. enterocolitica strains were isolated (7.91%); the
isolation rate from dogs was 12.99%; and no Y.
pseudotuberculosis or other Yersinia strains were isolated
(Table 1). In Guizhou Province, 14 Y. enterocolitica strains
were isolated (5.56%); isolation rate from dogs was
11.11% (14/126); and four Y. pseudotuberculosis strains
were isolated (1.59%). Furthermore, six Y. frederiksenii/
intermedia strains and two Y. kristensenii strains were
isolated (Table 1). In Guangxi province, we isolated ten
Y. pseudotuberculosis from nine dogs, with one of the dog
carrying two different kinds (two PFGE patterns) of Y.
pseudotuberculosis, so the Y. pseudotuberculosis strain
isolation rate was 3.57% (10/280); and the Y. enteroco-
litica strain isolation rate was 3.57% (10/280). Two Y.
frederiksenii/intermedia strains were isolated (Table 1).
For Jiangsu, Guangxi and Guizhou provinces, all dogs’
serum were negative by IHA (Table 1).
During the investigation, Xuzhou (Jiangsu province)
quarterly study was performed, with 94 pathogenic Y.
enterocolitica strains and 12 non-pathogenic strains were
isolated from 670 tonsil-rectal swab samples from the
dogs. Eighty-seven of the 670 canines (12.99%) were
positive for Yersinia from either or both tonsil and rectal
swab samples, which was much higher than the carrying
rate of Y. enterocolitica in tonsil (9.1%) and rectal swab
(6.72%) samples separately (Fig. 1A-1). Only 21.84% (19/
87) of the dogs had isolated strains from both tonsil and
rectal swab samples. The isolation rate of dog was different
for each quarter of the year; June (26.00%) was the highest
month, followed by March (11.00%), with September
(7.00%) being the lowest (Fig. 1A-1).
For the natural plague areas, 27 were positive for F1
antibody using IHA in Gansu. All 27 positive dogs were
pubescent, eleven of them were female; with titers of 1:40
and 1:80 for five; 1:160 for three; 1:320 for six; 1:640 and
1:1280 for four (Fig. 1A-2). Twenty-two antibody-positive
dogs were found in Qinghai in the vicinity of Gansu
Province, 21 of them were pubescent, and 19 of them were
female. The highest antibody titer was 1:1280 in one dog
(Fig. 1A-2).
The isolation rates of non-pathogenic Y. enterocolitica
strains were 0.95% (1/105) and 1.65% (2/121) for Gansu
and Qinghai respectively. No pathogenic Y. enterocolitica
strains or other Yersinia strains were isolated in these areas
(Table 1).
From 106 pathogenic Y. enterocolitica strains, 14
different PFGE patterns were obtained using NotI enzyme.
Predominant patterns were different among the three
provinces. The predominant NotI pattern K6GN11C30068
represented 52.04% (51/98) of Jiangsu strains followed by
pattern K6GN11C30021 (31.63, 31/98%). Among the three
pathogenic Y. enterocolitica strains isolated in Guizhou, two
strains were pattern K6GN11C30012 and the other was
K6GN11C30021. Four Y. pseudotuberculosis strains isolated
in Guizhou clustered into four different patterns. Ten Y.
pseudotuberculosis strains isolated in Guangxi clustered
into another ten patterns. In contrast to Y. enterocolitica, Y.
pseudotuberculosis PFGE patterns were more dispersed
(Fig. 1B and C).
36 strains from canines had the identical PFGE patterns
with the strains isolated from pigs and patients (31
K6GN11C30021 pattern in Jiangsu province; four
K6GN11C30012 pattern in Jiangsu and one in Guangxi
province). Only four strain patterns isolated from patients
in Guangxi did not have identical patterns in the local pig
or dog isolates (Fig. 1B and C).
4. Discussion
Y. pestis, Y. enterocolitica and Y. pseudotuberculosis are all
zoonotic pathogens (Mikula et al., 2012) that are recovered
from diverse animal sources, i.e. from farm animals and
domestic pets to free-living and captive wild animals
(Backhans et al., 2011; Doll et al., 1994; Li et al., 2008;
Weber and Lembke, 1981; Williams et al., 2013). The
 X. Wang et al. / Veterinary Microbiology 172 (2014) 339–344
animals infected with Yersinia have a high risk of
transmitting pathogenic Yersinia to humans because of
their close relationships. Our previous study showed
pathogenic Y. enterocolitica isolated from domestic dogs
may be a source of human infection (Wang et al., 2010).
Others reported a dog-associated primary pneumonic
plague outbreak in Qinghai Province of China (Hetem
et al., 2013). The breeding of C. lupus familiaris and
shepherd dogs is popular in China; even some domestic
dogs live together and share meals with their owners. Dogs
moving around public places also connect with domestic
and wild animals adding potential public health risk
following exposure to dogs (Fig. 1A-3–A-5 shown). In this
study, our five year surveillance showed Y. enterocolitica
existed widely in canine feces, adding an infection
probability for human and other animals. Strains isolated
from C. lupus familiaris, local pig and diarrhea patients
shared the same pulsed-field gel electrophoresis (PFGE)
pattern (K6GN11C30021 and K6GN11C30012), indicating
they may be from the same clone and the close
transmission source of pathogenic Y. enterocolitica infec-
tions in these areas.
The seasonal variability of Y. enterocolitica isolation was
observed in Xuzhou, with the highest rate in the summer
(second quarter) (Fig. 1A-1). This was controversial with
the life habit of Y. enterocolitica and the precise reason for
this phenomenon was not known and still need further
investigation.
Here we found canines were identified as one of the
primary reservoirs of pathogenic Y. enterocolitica; and they
also play important roles in the transmission of Y.
pseudotuberculosis among the animals to cause human
infection. Further, the distribution of Y. pseudotuberculosis
in China has distinctive regional characteristics. No strains
of Y. pseudotuberculosis were isolated from 1872 dog
samples from Jiangsu, Qinghai and Gansu Provinces.
However, Y. pseudotuberculosis isolation rate in canines
in the Guangxi southwest China, is as high as 6.43%, and
3.17% in its adjacent province, Guizhou, suggesting
regional distribution of Y. pseudotuberculosis (Liang et al.,
2012).
The results of the specific F1 antibody to Y. pestis were
significantly different between natural plague areas and
plague free areas in China. The high titer to specific F1
antigen of Y. pestis maybe reflected the biological
variations in the immune responses among different
plague foci. Furthermore, the primary host of plague-the
marmot had the close life habit with shepherd dog in
natural plague areas, and sometimes the infected rodents
could be eaten by shepherd dogs as Fig. 1A-3–A-5 shown,
indicated the high positive rate of F1 antibody in these
areas.
This was the first report of the distribution and
dissemination of pathogenic Yersinia spp. in C. lupus
familiaris in China. C. lupus familiaris and shepherd dogs
are widespread in China where these animals often live in
close association with human and other animals. Data
presented in this report suggests that three human
pathogen Yersinia may be harbored in the dog; therefore
dogs have a role in the epidemiology of Yersinia and should
not be overlooked in routine surveys for Yersinia.
343
Conflict of interest
The authors certify that they have no potential conflicts
of interest.
Acknowledgements
This work was supported by the National Natural Science
Foundation of China (General Project, No. 31100101) and
the National Sci-Tech Key Project (2012ZX10004201,
2013ZX10004203-002 and 2012ZX10004-208). We thank
Liuying Tang and Jim Nelson for critical reading and helpful
comments of our manuscript.
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