Accepted Manuscript Title: Vector-borne pathogens in arctic foxes, Vulpes lagopus, from Canada Author: Patricia E. Mascarelli, Stacey A. Elmore, Emily J. Jenkins, Ray T. Alisauskas, Mary Walsh, Edward B. Breitschwerdt, Ricardo G. Maggi PII: DOI: Reference:
S0034-5288(14)00352-X http://dx.doi.org/doi: 10.1016/j.rvsc.2014.12.011 YRVSC 2787
To appear in:
Research in Veterinary Science
Received date: Accepted date:
27-8-2013 11-12-2014
Please cite this article as: Patricia E. Mascarelli, Stacey A. Elmore, Emily J. Jenkins, Ray T. Alisauskas, Mary Walsh, Edward B. Breitschwerdt, Ricardo G. Maggi, Vector-borne pathogens in arctic foxes, Vulpes lagopus, from Canada, Research in Veterinary Science (2014), http://dx.doi.org/doi: 10.1016/j.rvsc.2014.12.011. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
SHORT COMMUNICATION: Vector-borne pathogens in arctic foxes, Vulpes lagopus,
2
from Canada
3 4
Patricia E. Mascarelli1, Stacey A. Elmore2, Emily J. Jenkins2, Ray T. Alisauskas3; Mary Walsh1
5
Edward B. Breitschwerdt1, Ricardo G. Maggi*1
6 7
1
8
Translational Research College of Veterinary Medicine, North Carolina State University. North
9
Carolina, USA
Intracellular Pathogens Research Laboratory (IPRL), Center for Comparative Medicine and
10 11
2
12
Saskatoon, Saskatchewan, Canada S7N EB4
Department of Veterinary Microbiology, University of Saskatchewan, 52 Campus Drive,
13 14
3
15
5E2, Canada
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N
16 17
*Corresponding Author
18
Dr. Ricardo G. Maggi, College of Veterinary Medicine, North Carolina State University, 1060
19
William Moore Dr., Raleigh, NC 27606, Phone: 919-513-8273, Fax: 919-513-6336, e-mail:
20
[email protected]
21 22 23
1 Page 1 of 8
24 25 26 27 28 29 30 31 32
Highlights: We report three vector-borne pathogens in arctic foxes, Vulpes lagopus, from Canada. Bartonella henselae is the most prevalent pathogen found (3/28) Infection with E. canis, an Anaplasma spp., and M. haemocanis was found in single individuals. This is preliminary evidence of vector borne pathogens in foxes from the Canadian arctic ecosystem.
33
Because of the relatively low biodiversity within arctic ecosystems, arctic foxes, Vulpes lagopus,
34
could serve as sentinels for the study of changes in the ecology of vector-borne zoonotic
35
pathogens. The objective of this study was to determine the molecular prevalence of 5 different
36
genera of vector borne pathogens (Anaplasma, Babesia, Bartonella, Ehrlichia, and Hemotropic
37
Mycoplasma spp.) using blood collected from 28 live-trapped arctic foxes from the region of
38
Karrak Lake, Nunavut, Canada. Bartonella henselae (n=3), Mycoplasma haemocanis (n=1),
39
Ehrlichia canis (n=1), and an Anaplasma sp. (n=1) DNA were PCR amplified and subsequently
40
identified by sequencing. This study provides preliminary evidence that vector borne pathogens,
41
not typically associated with the arctic ecosystem, exist at low levels in this arctic fox
42
population, and that vector exposure, pathogen transmission dynamics, and changes in the
43
geographic distribution of pathogens over time should be investigated in future studies.
Abstract
44 45
Keywords
46
Foxes; Canada; vector-borne; Bartonella; Mycoplasma; Ehrlichia; zoonosis
47
2 Page 2 of 8
48
SHORT COMMUNICATION
49 50
The relatively low biodiversity within arctic ecosystems could allow arctic foxes, Vulpes
51
lagopus, to serve as sentinels for the assessment of climate change on the emergence and ecology
52
of vector-borne zoonotic pathogens. In Europe, arctic fox numbers have declined due to
53
anthropogenic factors such as increased hunting pressure (Angerbjörn et al., 2004), the
54
emergence of zoonotic pathogens such as ear canker mites, the introduction of domestic cats,
55
dogs, and farmed foxes (Gunnarsson et al., 1991; Skirnisson et al., 1993), the introduction of
56
rabies derived from domestic dog importation (Macdonald et al., 2011; Nyberg et al., 1992),
57
leptospirosis introduced by cattle farming and farm-breed foxes (Egorov et al., 1996), and
58
bladderworms, also introduced via farm-breed foxes (Fernandez-Aguilar et al., 2010).
59
In North America, only the trophic interactions and intestinal parasite fauna of the arctic foxes of
60
the Canadian Arctic Tundra region have been described (Elmore et al., 2013; Samelius et al.,
61
2007). As a component of ongoing population and pathogen studies in the region of Karrak
62
Lake, Nunavut, Canada, blood samples from 28 arctic foxes were analyzed to determine the
63
molecular prevalence of 5 different genera of vector borne pathogens (Anaplasma, Babesia,
64
Bartonella, Ehrlichia, and Hemotropic Mycoplasma spp.) using DNA amplification. Briefly,
65
Bartonella testing was performed by PCR amplification of blood, and blood culture DNA
66
samples (using the BAPGM platform) as described previously (Duncan et al., 2007; Perez Vera
67
et al., 2013). Anaplasma, Babesia, Ehrlichia, and hemotropic Mycoplasma spp. infection in
68
blood samples was tested also by PCR amplification aiming at the 16SrRNA gene (Mycoplasma,
69
Ehrlichia, and Anaplasma) or the 18SrRNA gene (Babesia) (Compton et al., 2012; Maggi et al.,
70
2013a; Maggi et al., 2013b; Maggi et al., 2013c).
71 3 Page 3 of 8
72
Overall, Anaplasma, Bartonella, Ehrlichia, and hemotropic Mycoplasma spp. DNA was
73
successfully amplified and sequenced from individual Arctic foxes, whereas no Babesia DNA
74
was amplified from any sample (Table 1). Bartonella henselae was isolated from three of 28
75
foxes using an enrichment blood culture, whereas one fox each was infected with an Anaplasma
76
sp., Ehrlichia canis, and Mycoplasma haemocanis. DNA sequencing confirmed infection with B.
77
henselae SA2 in two foxes with 523/523 bp (100%) similarity to Genbank accession AF369529 ,
78
and B. henselae H1, with 494/494 bp (100%) similarity to Genbank accession NC_005956 in one
79
arctic fox. The E. canis DNA sequence shared 336/336 bp (100%) similarity to Genbank
80
accession NC_007354. The M. haemocanis DNA sequence had 100% (506/506 bp) similarity to
81
M. haemocanis (GenBank accession AY529641). To the author’s knowledge, prior studies have
82
not investigated any of these pathogens in Arctic foxes; therefore, it is not possible to determine
83
whether these vector borne infections have been present previously in Arctic foxes or whether
84
these organisms represent a more recent introduction of the pathogens or their respective vectors.
85
Arctic foxes in the Karrak Lake infrequently interact with domestic dogs and red foxes, whereas
86
high level exposure to goose fleas (Ceratophyllus vagabundus vagabundus) was recently
87
reported (Harriman, 2008; Harriman et al., 2011). Ticks from migratory birds could be another
88
mode of transmission.
89 90
In the northwestern Canadian Arctic, host and pathogen diversity are considered low as
91
compared to tropical and subtropical regions of the world. Therefore, Arctic animals, such as the
92
Arctic fox, might be susceptible to the direct or indirect consequences of human activities, such
93
as changes in environmental temperature resulting in the invasion of new pathogens to the biota
94
(Davidson et al., 2011). This study provided preliminary evidence that vector borne pathogens,
4 Page 4 of 8
95
not typically associated with the arctic ecosystem, existed at low levels in this Arctic fox
96
population. A comprehensive ecologic approach to delineate potential impacts of climate change
97
and human population dynamics on animal populations will be vital to the understanding of
98
infectious disease emergence in Arctic foxes and for the implementation of wildlife conservation
99
strategies. Future studies should also address vector exposure, pathogen transmission dynamics,
100
and changes in the geographic distribution of pathogens over time.
101 102
Acknowledgements:
103
The authors thank Tonya Lee for editorial assistance.
104 105
Conflict of Interest Statement:
106
The authors have not conflict of interests to disclose
107 108
Research Support:
109
This research was supported in part by Bayer Animal Health and the State of North Carolina.
5 Page 5 of 8
110
References
111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154
Angerbjörn, A., P. Hersteinsson, and M. Tannerfeldt. 2004. Arctic fox (Alopex lagopus). Canids: Foxes, Wolves, Jackals and Dogs - Status survey and conservation action plan. IUCN Gland:117-123. Compton, S.M., R.G. Maggi, and E.B. Breitschwerdt. 2012. Candidatus Mycoplasma haematoparvum and Mycoplasma haemocanis infections in dogs from the United States. Comp Immunol Microbiol Infect Dis. 35:557-562. Davidson, R., M. Simard, S.J. Kutz, C.M. Kapel, I.S. Hamnes, and L.J. Robertson. 2011. Arctic parasitology: why should we care? Trends in parasitology. 27:239-245. Duncan, A.W., R.G. Maggi, and E.B. Breitschwerdt. 2007. A combined approach for the enhanced detection and isolation of Bartonella species in dog blood samples: preenrichment liquid culture followed by PCR and subculture onto agar plates. J Microbiol Methods. 69:273-281. Egorov, I., A.S. Maramovich, S.M. Makeev, V.F. Cherniavskii, I.E. Trop, and L.D. Tugutov. 1996. [The epidemiological and epizootiological characteristics of leptospirosis in the Republic of Sakha (Yakutia)]. Meditsinskaia parazitologiia i parazitarnye bolezni:48-51. Elmore, S., L. Lalonde, G. Samelius, R. Alisauskas, A. Gajadhar, and E. Jenkins. 2013. Endoparasites in the feces of arctic foxes in a terrestrial ecosystem in Canada. International Journal for Parasitology: Parasites and Wildlife. 2:90-96. Fernandez-Aguilar, X., R. Mattsson, T. Meijer, E. Osterman-Lind, and D. Gavier-Widen. 2010. Pearsonema (syn Capillaria) plica associated cystitis in a Fennoscandian arctic fox (Vulpes lagopus: a case report. Acta veterinaria Scandinavica. 52:39. Gunnarsson, E., P. Hersteinsson, and S. Adalsteinsson. 1991. Prevalence and geographical distribution of the ear canker mite (Otodectes cynotis) among arctic foxes (Alopex lagopus) in Iceland. Journal of wildlife diseases. 27:105-109. Harriman, V.A., RT; Wobeser, GA. 2008. The case of the blood-covered egg: ectoparasite abundance in an arctic goose colony. Canadian Journal of Zoology. 86:959-965. Harriman, V.B., T.D. Galloway, R.T. Alisauskas, and G.A. Wobeser. 2011. Description of the larva of Ceratophyllus vagabundus vagabundus (Siphonaptera:Ceratophyllidae) from nests of Ross's and lesser snow geese in Nunavut, Canada. The Journal of parasitology. 97:218-220. Macdonald, E., K. Handeland, H. Blystad, M. Bergsaker, M. Fladberg, B. Gjerset, O. Nilsen, H. Os, S. Sandbu, E. Stokke, L. Vold, I. Orpetveit, H. Gaup Amot, and O. Tveiten. 2011. Public health implications of an outbreak of rabies in arctic foxes and reindeer in the Svalbard archipelago, Norway, September 2011. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 16. Maggi, R., A. Birkenheuer, B. Hegarty, J. Bradley, M. Levy, and E. Breitschwerdt. 2013a. Advantages and limitations of serological and molecular panels for the diagnosis of vector-borne infectious diseases in dogs. JAVMA. accepted for publication. Maggi, R.G., P.E. Mascarelli, N. Balakrishnan, C.M. Rohde, C.M. Kelly, L. Ramaiah, M.W. Leach, and E.B. Breitschwerdt. 2013b. 'Candidatus Mycoplasma haemomacaque' and Bartonella quintana bacteremia in cynomolgus monkeys. J Clin Microbiol. Maggi, R.G., P.E. Mascarelli, L.N. Havenga, V. Naidoo, and E.B. Breitschwerdt. 2013c. Coinfection with Anaplasma platys, Bartonella henselae and Candidatus Mycoplasma haematoparvum in a veterinarian. Parasit Vectors. 6:103. 6 Page 6 of 8
155 156 157 158 159 160 161 162 163 164 165 166 167
Nyberg, M., K. Kulonen, E. Neuvonen, C. Ek-Kommonen, M. Nuorgam, and B. Westerling. 1992. An epidemic of sylvatic rabies in Finland--descriptive epidemiology and results of oral vaccination. Acta veterinaria Scandinavica. 33:43-57. Perez Vera, C., P.P. Diniz, E.L. Pultorak, R.G. Maggi, and E.B. Breitschwerdt. 2013. An unmatched case controlled study of clinicopathologic abnormalities in dogs with Bartonella infection. Comp Immunol Microbiol Infect Dis. 36:481-487. Samelius, G., R.T. Alisauskas, K.A. Hobson, and S. Lariviere. 2007. Prolonging the arctic pulse: long-term exploitation of cached eggs by arctic foxes when lemmings are scarce. The Journal of animal ecology. 76:873-880. Skirnisson, K., M. Eydal, E. Gunnarsson, and P. Hersteinsson. 1993. Parasites of the arctic fox (Alopex lagopus) in Iceland. Journal of wildlife diseases. 29:440-446.
7 Page 7 of 8
168
Table 1: Vector-borne pathogens detected in blood from arctic foxes
Bartonella
Mycoplasma
Ehrlichia
Anaplasma
henselae*
haemocanis
canis
spp
Blood (n=20)
3
1
0
0
Blood clots (n=9)
0
0
1
1
Sample
*= Two B. henselae San Antonio 2, and one B. henselae Houston I. Note: Detection and identification of Bartonella, Mycoplasma, Ehrlichia , and Anaplasma species was performed by PCR amplification of the ITS region (Bartonella) and the 16SrRNA gene (using primers specific for Mycoplasma, Ehrlichia and Anaplasma) followed by sequence of positive amplicons (for species/strain identification) as described above.
169
8 Page 8 of 8
S0034-5288(14)00352-X http://dx.doi.org/doi: 10.1016/j.rvsc.2014.12.011 YRVSC 2787
To appear in:
Research in Veterinary Science
Received date: Accepted date:
27-8-2013 11-12-2014
Please cite this article as: Patricia E. Mascarelli, Stacey A. Elmore, Emily J. Jenkins, Ray T. Alisauskas, Mary Walsh, Edward B. Breitschwerdt, Ricardo G. Maggi, Vector-borne pathogens in arctic foxes, Vulpes lagopus, from Canada, Research in Veterinary Science (2014), http://dx.doi.org/doi: 10.1016/j.rvsc.2014.12.011. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
SHORT COMMUNICATION: Vector-borne pathogens in arctic foxes, Vulpes lagopus,
2
from Canada
3 4
Patricia E. Mascarelli1, Stacey A. Elmore2, Emily J. Jenkins2, Ray T. Alisauskas3; Mary Walsh1
5
Edward B. Breitschwerdt1, Ricardo G. Maggi*1
6 7
1
8
Translational Research College of Veterinary Medicine, North Carolina State University. North
9
Carolina, USA
Intracellular Pathogens Research Laboratory (IPRL), Center for Comparative Medicine and
10 11
2
12
Saskatoon, Saskatchewan, Canada S7N EB4
Department of Veterinary Microbiology, University of Saskatchewan, 52 Campus Drive,
13 14
3
15
5E2, Canada
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N
16 17
*Corresponding Author
18
Dr. Ricardo G. Maggi, College of Veterinary Medicine, North Carolina State University, 1060
19
William Moore Dr., Raleigh, NC 27606, Phone: 919-513-8273, Fax: 919-513-6336, e-mail:
20
[email protected]
21 22 23
1 Page 1 of 8
24 25 26 27 28 29 30 31 32
Highlights: We report three vector-borne pathogens in arctic foxes, Vulpes lagopus, from Canada. Bartonella henselae is the most prevalent pathogen found (3/28) Infection with E. canis, an Anaplasma spp., and M. haemocanis was found in single individuals. This is preliminary evidence of vector borne pathogens in foxes from the Canadian arctic ecosystem.
33
Because of the relatively low biodiversity within arctic ecosystems, arctic foxes, Vulpes lagopus,
34
could serve as sentinels for the study of changes in the ecology of vector-borne zoonotic
35
pathogens. The objective of this study was to determine the molecular prevalence of 5 different
36
genera of vector borne pathogens (Anaplasma, Babesia, Bartonella, Ehrlichia, and Hemotropic
37
Mycoplasma spp.) using blood collected from 28 live-trapped arctic foxes from the region of
38
Karrak Lake, Nunavut, Canada. Bartonella henselae (n=3), Mycoplasma haemocanis (n=1),
39
Ehrlichia canis (n=1), and an Anaplasma sp. (n=1) DNA were PCR amplified and subsequently
40
identified by sequencing. This study provides preliminary evidence that vector borne pathogens,
41
not typically associated with the arctic ecosystem, exist at low levels in this arctic fox
42
population, and that vector exposure, pathogen transmission dynamics, and changes in the
43
geographic distribution of pathogens over time should be investigated in future studies.
Abstract
44 45
Keywords
46
Foxes; Canada; vector-borne; Bartonella; Mycoplasma; Ehrlichia; zoonosis
47
2 Page 2 of 8
48
SHORT COMMUNICATION
49 50
The relatively low biodiversity within arctic ecosystems could allow arctic foxes, Vulpes
51
lagopus, to serve as sentinels for the assessment of climate change on the emergence and ecology
52
of vector-borne zoonotic pathogens. In Europe, arctic fox numbers have declined due to
53
anthropogenic factors such as increased hunting pressure (Angerbjörn et al., 2004), the
54
emergence of zoonotic pathogens such as ear canker mites, the introduction of domestic cats,
55
dogs, and farmed foxes (Gunnarsson et al., 1991; Skirnisson et al., 1993), the introduction of
56
rabies derived from domestic dog importation (Macdonald et al., 2011; Nyberg et al., 1992),
57
leptospirosis introduced by cattle farming and farm-breed foxes (Egorov et al., 1996), and
58
bladderworms, also introduced via farm-breed foxes (Fernandez-Aguilar et al., 2010).
59
In North America, only the trophic interactions and intestinal parasite fauna of the arctic foxes of
60
the Canadian Arctic Tundra region have been described (Elmore et al., 2013; Samelius et al.,
61
2007). As a component of ongoing population and pathogen studies in the region of Karrak
62
Lake, Nunavut, Canada, blood samples from 28 arctic foxes were analyzed to determine the
63
molecular prevalence of 5 different genera of vector borne pathogens (Anaplasma, Babesia,
64
Bartonella, Ehrlichia, and Hemotropic Mycoplasma spp.) using DNA amplification. Briefly,
65
Bartonella testing was performed by PCR amplification of blood, and blood culture DNA
66
samples (using the BAPGM platform) as described previously (Duncan et al., 2007; Perez Vera
67
et al., 2013). Anaplasma, Babesia, Ehrlichia, and hemotropic Mycoplasma spp. infection in
68
blood samples was tested also by PCR amplification aiming at the 16SrRNA gene (Mycoplasma,
69
Ehrlichia, and Anaplasma) or the 18SrRNA gene (Babesia) (Compton et al., 2012; Maggi et al.,
70
2013a; Maggi et al., 2013b; Maggi et al., 2013c).
71 3 Page 3 of 8
72
Overall, Anaplasma, Bartonella, Ehrlichia, and hemotropic Mycoplasma spp. DNA was
73
successfully amplified and sequenced from individual Arctic foxes, whereas no Babesia DNA
74
was amplified from any sample (Table 1). Bartonella henselae was isolated from three of 28
75
foxes using an enrichment blood culture, whereas one fox each was infected with an Anaplasma
76
sp., Ehrlichia canis, and Mycoplasma haemocanis. DNA sequencing confirmed infection with B.
77
henselae SA2 in two foxes with 523/523 bp (100%) similarity to Genbank accession AF369529 ,
78
and B. henselae H1, with 494/494 bp (100%) similarity to Genbank accession NC_005956 in one
79
arctic fox. The E. canis DNA sequence shared 336/336 bp (100%) similarity to Genbank
80
accession NC_007354. The M. haemocanis DNA sequence had 100% (506/506 bp) similarity to
81
M. haemocanis (GenBank accession AY529641). To the author’s knowledge, prior studies have
82
not investigated any of these pathogens in Arctic foxes; therefore, it is not possible to determine
83
whether these vector borne infections have been present previously in Arctic foxes or whether
84
these organisms represent a more recent introduction of the pathogens or their respective vectors.
85
Arctic foxes in the Karrak Lake infrequently interact with domestic dogs and red foxes, whereas
86
high level exposure to goose fleas (Ceratophyllus vagabundus vagabundus) was recently
87
reported (Harriman, 2008; Harriman et al., 2011). Ticks from migratory birds could be another
88
mode of transmission.
89 90
In the northwestern Canadian Arctic, host and pathogen diversity are considered low as
91
compared to tropical and subtropical regions of the world. Therefore, Arctic animals, such as the
92
Arctic fox, might be susceptible to the direct or indirect consequences of human activities, such
93
as changes in environmental temperature resulting in the invasion of new pathogens to the biota
94
(Davidson et al., 2011). This study provided preliminary evidence that vector borne pathogens,
4 Page 4 of 8
95
not typically associated with the arctic ecosystem, existed at low levels in this Arctic fox
96
population. A comprehensive ecologic approach to delineate potential impacts of climate change
97
and human population dynamics on animal populations will be vital to the understanding of
98
infectious disease emergence in Arctic foxes and for the implementation of wildlife conservation
99
strategies. Future studies should also address vector exposure, pathogen transmission dynamics,
100
and changes in the geographic distribution of pathogens over time.
101 102
Acknowledgements:
103
The authors thank Tonya Lee for editorial assistance.
104 105
Conflict of Interest Statement:
106
The authors have not conflict of interests to disclose
107 108
Research Support:
109
This research was supported in part by Bayer Animal Health and the State of North Carolina.
5 Page 5 of 8
110
References
111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154
Angerbjörn, A., P. Hersteinsson, and M. Tannerfeldt. 2004. Arctic fox (Alopex lagopus). Canids: Foxes, Wolves, Jackals and Dogs - Status survey and conservation action plan. IUCN Gland:117-123. Compton, S.M., R.G. Maggi, and E.B. Breitschwerdt. 2012. Candidatus Mycoplasma haematoparvum and Mycoplasma haemocanis infections in dogs from the United States. Comp Immunol Microbiol Infect Dis. 35:557-562. Davidson, R., M. Simard, S.J. Kutz, C.M. Kapel, I.S. Hamnes, and L.J. Robertson. 2011. Arctic parasitology: why should we care? Trends in parasitology. 27:239-245. Duncan, A.W., R.G. Maggi, and E.B. Breitschwerdt. 2007. A combined approach for the enhanced detection and isolation of Bartonella species in dog blood samples: preenrichment liquid culture followed by PCR and subculture onto agar plates. J Microbiol Methods. 69:273-281. Egorov, I., A.S. Maramovich, S.M. Makeev, V.F. Cherniavskii, I.E. Trop, and L.D. Tugutov. 1996. [The epidemiological and epizootiological characteristics of leptospirosis in the Republic of Sakha (Yakutia)]. Meditsinskaia parazitologiia i parazitarnye bolezni:48-51. Elmore, S., L. Lalonde, G. Samelius, R. Alisauskas, A. Gajadhar, and E. Jenkins. 2013. Endoparasites in the feces of arctic foxes in a terrestrial ecosystem in Canada. International Journal for Parasitology: Parasites and Wildlife. 2:90-96. Fernandez-Aguilar, X., R. Mattsson, T. Meijer, E. Osterman-Lind, and D. Gavier-Widen. 2010. Pearsonema (syn Capillaria) plica associated cystitis in a Fennoscandian arctic fox (Vulpes lagopus: a case report. Acta veterinaria Scandinavica. 52:39. Gunnarsson, E., P. Hersteinsson, and S. Adalsteinsson. 1991. Prevalence and geographical distribution of the ear canker mite (Otodectes cynotis) among arctic foxes (Alopex lagopus) in Iceland. Journal of wildlife diseases. 27:105-109. Harriman, V.A., RT; Wobeser, GA. 2008. The case of the blood-covered egg: ectoparasite abundance in an arctic goose colony. Canadian Journal of Zoology. 86:959-965. Harriman, V.B., T.D. Galloway, R.T. Alisauskas, and G.A. Wobeser. 2011. Description of the larva of Ceratophyllus vagabundus vagabundus (Siphonaptera:Ceratophyllidae) from nests of Ross's and lesser snow geese in Nunavut, Canada. The Journal of parasitology. 97:218-220. Macdonald, E., K. Handeland, H. Blystad, M. Bergsaker, M. Fladberg, B. Gjerset, O. Nilsen, H. Os, S. Sandbu, E. Stokke, L. Vold, I. Orpetveit, H. Gaup Amot, and O. Tveiten. 2011. Public health implications of an outbreak of rabies in arctic foxes and reindeer in the Svalbard archipelago, Norway, September 2011. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 16. Maggi, R., A. Birkenheuer, B. Hegarty, J. Bradley, M. Levy, and E. Breitschwerdt. 2013a. Advantages and limitations of serological and molecular panels for the diagnosis of vector-borne infectious diseases in dogs. JAVMA. accepted for publication. Maggi, R.G., P.E. Mascarelli, N. Balakrishnan, C.M. Rohde, C.M. Kelly, L. Ramaiah, M.W. Leach, and E.B. Breitschwerdt. 2013b. 'Candidatus Mycoplasma haemomacaque' and Bartonella quintana bacteremia in cynomolgus monkeys. J Clin Microbiol. Maggi, R.G., P.E. Mascarelli, L.N. Havenga, V. Naidoo, and E.B. Breitschwerdt. 2013c. Coinfection with Anaplasma platys, Bartonella henselae and Candidatus Mycoplasma haematoparvum in a veterinarian. Parasit Vectors. 6:103. 6 Page 6 of 8
155 156 157 158 159 160 161 162 163 164 165 166 167
Nyberg, M., K. Kulonen, E. Neuvonen, C. Ek-Kommonen, M. Nuorgam, and B. Westerling. 1992. An epidemic of sylvatic rabies in Finland--descriptive epidemiology and results of oral vaccination. Acta veterinaria Scandinavica. 33:43-57. Perez Vera, C., P.P. Diniz, E.L. Pultorak, R.G. Maggi, and E.B. Breitschwerdt. 2013. An unmatched case controlled study of clinicopathologic abnormalities in dogs with Bartonella infection. Comp Immunol Microbiol Infect Dis. 36:481-487. Samelius, G., R.T. Alisauskas, K.A. Hobson, and S. Lariviere. 2007. Prolonging the arctic pulse: long-term exploitation of cached eggs by arctic foxes when lemmings are scarce. The Journal of animal ecology. 76:873-880. Skirnisson, K., M. Eydal, E. Gunnarsson, and P. Hersteinsson. 1993. Parasites of the arctic fox (Alopex lagopus) in Iceland. Journal of wildlife diseases. 29:440-446.
7 Page 7 of 8
168
Table 1: Vector-borne pathogens detected in blood from arctic foxes
Bartonella
Mycoplasma
Ehrlichia
Anaplasma
henselae*
haemocanis
canis
spp
Blood (n=20)
3
1
0
0
Blood clots (n=9)
0
0
1
1
Sample
*= Two B. henselae San Antonio 2, and one B. henselae Houston I. Note: Detection and identification of Bartonella, Mycoplasma, Ehrlichia , and Anaplasma species was performed by PCR amplification of the ITS region (Bartonella) and the 16SrRNA gene (using primers specific for Mycoplasma, Ehrlichia and Anaplasma) followed by sequence of positive amplicons (for species/strain identification) as described above.
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