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Preventive Veterinary Medicine 174 (2020) 104817

Contents lists available at ScienceDirect

Preventive Veterinary Medicine


journal homepage: www.elsevier.com/locate/prevetmed

Canine parvovirus prevention and prevalence: Veterinarian perceptions and T


behaviors
M. Kelman*, V.R. Barrs, J.M. Norris, M.P. Ward
The University of Sydney, Sydney School of Veterinary Science, NSW 2006, Australia

A R T I C LE I N FO A B S T R A C T

Keywords: Canine Parvovirus (CPV) causes severe morbidity and mortality in dogs, particularly puppies, worldwide.
Canine parvovirus Although vaccination is highly efficacious in preventing disease, cases continue to occur and vaccination failures
CPV are well documented. Maternally derived antibody interference is the leading cause of vaccination failure and
Vaccination protocols age at vaccine administration is a significant risk factor for failure. However, no studies have been performed on
Titer testing
practicing veterinarians’ usage of and compliance with published vaccination guidelines and label re-
Veterinarian perceptions
Prevention
commendations. Likewise, there are no published studies of veterinarian perceptions on CPV occurrence and
mortality and its influence on case outcome. We report a study in which all Australian small companion animal
(canine and feline) veterinary hospitals were surveyed, yielding a response rate of 23.5% (534 unique veterinary
hospitals). Respondents overall perceived national CPV occurrence ten-times lower (median 2000 cases) than the
estimated national caseload (20,000 cases). Respondents from hospitals that did not diagnose CPV perceived
national occurrence twenty-times lower (median 1000 cases) than the estimated rate (p < 0.0001). Perceived
disease mortality (50%) was 2.74 times higher than that reported (18.2%). In addition, 26.7% of veterinarians
reported using serological titer testing to some degree, which some practitioners use in lieu of vaccination if a
titer is perceived to reflect sufficient immunity. Based on this study veterinarians appear to be aware of the
disease risk in their region but unaware of the burden of CPV disease nationally, and perceive mortality risk
higher than it actually is. This might lead to an overestimation of cost to treat, and over-recommendation of
euthanasia. Nearly half (48.7%) of respondents recommended final puppy vaccination earlier than guidelines
recommend, while 2.8% of respondents recommended a puppy re-vaccination interval longer than supported by
vaccine labels and guidelines. Both of these practices may put puppies at risk of CPV infection.

1. Introduction inappropriate vaccination timing can increase risk of exposure to dis-


ease; however, veterinarians’ vaccination usage patterns have not been
Canine parvovirus (CPV) is a single-stranded DNA virus within the previously investigated (Altman et al., 2017; Decaro et al., 2009, 2008).
genus Carnivore Protoparvovirus, and one of the most important patho- Currently, veterinarians vaccinate puppies on multiple occasions
genic viruses affecting dogs (Nandi et al., 2013). CPV is found world- according to a schedule (e.g. monthly) during the first months of a
wide and signs of infection range from asymptomatic to severe gas- puppy’s life. This is performed mostly to account for maternally derived
troenteritis, leucopenia, dehydration, lethargy, and death (Goddard and antibody (MDA) which protects the puppy against infection but also
Leisewitz, 2010). Puppies under 6 months of age are more commonly neutralizes vaccine virus, preventing effective development of acquired
clinically affected, however dogs of any age can succumb to disease immunity, if present at the time of vaccination (Decaro et al., 2005;
(Decaro et al., 2007; Decaro and Buonavoglia, 2012; Goddard and Pollock and Carmichael, 1982). Other factors can also interfere with
Leisewitz, 2010). Vaccination against CPV is routinely performed seroconversion (Altman et al., 2017; Roth and Spickler, 2010). MDA
worldwide and is the most effective method to control disease (Altman titer of a puppy is dependent on the titer of the bitch, volume of co-
et al., 2017; Nandi et al., 2013), yet cases continue to occur (Filipov lostrum consumed, and the time since birth (Decaro et al., 2004;
et al., 2016; Kelman et al., 2019; Mira et al., 2018; Miranda et al., 2015; Pollock and Carmichael, 1982). MDA titer decline occurs exponentially
Parker et al., 2017; Quino Quispe et al., 2018; Zhao et al., 2016). with a half-life of approximately 10–14 days (Mila et al., 2014; Pollock
Vaccination failures are well recognized in the literature and and Carmichael, 1982); shorter half-life findings are thought to be


Corresponding author at: PO Box 96, Peregian Beach QLD 4573, Australia.
E-mail address: kelmanscientific@gmail.com (M. Kelman).

https://doi.org/10.1016/j.prevetmed.2019.104817
Received 22 August 2019; Received in revised form 19 October 2019; Accepted 25 October 2019
0167-5877/ © 2019 Elsevier B.V. All rights reserved.
M. Kelman, et al. Preventive Veterinary Medicine 174 (2020) 104817

explained by MDA-depletion due to viral replication and antibody se- add to 100%. The brand selections included all canine vaccine brands
questration (Macartney et al., 1988; Mila et al., 2014). Unless a titer- on the Australia market at the time of the survey: Canigen® (Virbac),
test is performed, MDA level at the time of vaccination is unknown. Canvac® (Zoetis), Companion® (MSD), Duramune® (Boehringer),
Depending on the puppy’s circumstances, an earlier start to vaccination, Nobivac® (MSD), Parvac® (Zoetis), Protech® (Boehringer). An option for
more frequent re-vaccination and later final vaccination can help re- “other” was provided but not selected by respondents. For most ques-
duce the risk of CPV infection. There are various guidelines published tions, a series of multi-choice answers were available for respondents to
by key opinion leaders (KOL), which provide recommendations for choose and they were also given the option to select “other” and to
vaccination protocols to protect against CPV disease (Australian instead provide their own answer.
Veterinary Association, 2018; British Small Animal Veterinary Veterinary hospital responses and CPV occurrence and mortality
Association, 2019; Day et al., 2016; Ford et al., 2017). Guidelines are perceptions were also grouped for statistical analysis by socioeconomic
published recommendations to assist practitioners in the use of vac- index (Index of Relative Socioeconomic Disadvantage, IRSD) and re-
cines, independent of registered use (off-label), where new scientific moteness (Remoteness Area, RA); provided by the Australian Bureau of
data dictate a different approach in the field that is better for the patient Statistics (ABS). IRSD is one of four Socio-Economic Indexes for Areas
(Thiry and Horzinek, 2007). The proportion of practitioners that follow (SEIFA) which ranks Australian postcodes according to census re-
guidelines or the variation in vaccination-usage patterns in different sponses of individuals living in that area, reflecting the relative dis-
circumstances has not been previously reported. advantage of an area based on the census questions relating to social
Veterinarians’ perceptions of CPV disease risk and case mortality and economic factors (Australian Bureau of Statistics, 2018). Data was
may differ depending on their experience with the disease. It is un- obtained as a data cube from the ABS (http://www.abs.gov.au/
known if these perceptions might play a role in altering case outcomes. AUSSTATS/abs@.nsf/DetailsPage/2033.0.55.0012016?
Veterinarians are an important source of information and advice for OpenDocument). RA assigns postcodes to one of five classes, to de-
clients on disease prognosis and can influence client decisions on monstrate the relative proximity to an urban center and relative access
treatment or euthanasia (Christiansen et al., 2015). How veterinarians’ to services. Data was obtained as a data cube from the ABS (http://
perceptions of CPV vary geographically, socioeconomically or due to www.abs.gov.au/AUSSTATS/abs@.nsf/DetailsPage/1270.0.55.
other factors has not been previously investigated. It has been de- 005July%202016?OpenDocument). Suburb data of all companion an-
monstrated that without treatment, euthanasia risk for CPV is corre- imal veterinary hospitals in Australia were obtained from our earlier
lated with socioeconomic disadvantage, and higher cost of treatment study (Kelman et al., 2019).
and veterinarian recommendations might play a role (Kelman et al.,
2019). 2.2. Data management and statistical analysis
The aims of this study were to: (1) document veterinarians’ per-
ceptions relating to CPV occurrence and mortality rate, (2) explore Only data from 2016 were analysed, and all data managed in
differences in preventive vaccination strategies utilized by veterinarians Microsoft® Excel for Mac version 16.16.10. Where respondents an-
and (3) determine where practitioner recommendations differ from swered open questions, their answers were interpreted and categorized
vaccine labels and KOL guidelines. manually into meaningful common groups for further analysis. Where a
respondent answered a question relating to vaccination timing with an
2. Materials and methods age range (for example, “between 12–14 weeks of age”) the latest first-
vaccination age or earliest final-vaccination age in the range was used
2.1. Data sources in the analysis. Where a range was advised for a vaccination interval,
the longest interval was used. Vaccine brands were categorized ac-
A national survey of Australian canine and feline veterinary hospi- cording to their length of advertised effective immunity (“annual” or
tals (including mobile clinics) was performed in 2017, to determine the “extended duration” e.g. 3 year duration of immunity) and according to
geographic distribution of CPV-related disease cases, financial impact the their CPV strain (CPV2 or CPV2b) (Altman et al., 2017). The
on pet owners, and veterinarians’ perceptions of CPV disease and pre- question on the usage of titer testing to determine vaccination interval
vention strategies. The results of case distribution, client impact, and elicited a range of descriptive responses presented in Supplementary
the survey design, have been previously reported (Kelman et al., 2019). Table 3, and where appropriate, “other” responses were re-categorized
For the current study, we report respondent perceptions of CPV oc- as “yes” or “no”. Socioeconomic deciles were converted into quintiles
currence and mortality, and strategies for disease prevention. for analysis. RA classes “Remote Australia” and “Very Remote Aus-
Respondents were asked a series of questions on personal demo- tralia” were combined as a single class for analysis due to insufficient
graphics (age category in years; year of graduation; university of gra- numbers of “Very Remote Australia” suburbs (three only). For corre-
duation), current and previous work-sector(s), veterinary hospital size lations, Remoteness Area codes (0,1,2,3) were used. All statistical
(number of full time veterinarians), state, postcode, and whether they analysis was performed using Statistix® version 10.0 (Analytical Soft-
performed any animal-shelter or council-pound-related work. They ware, Tallahassee, FL) and significance was p < 0.05 for all analyses.
were also asked their perception of CPV case numbers across Australia Descriptive statistics were generated for veterinarian perceptions of
and in their postcode in 2016, and their perception of CPV mortality CPV case number and mortality, and frequency distributions created for
rate in Australia (number of infected cases that die directly from the vaccination type usage and veterinarian perceptions. The relationship
disease, regardless of treatment or not, excluding euthanasia). between CPV case numbers and mortality versus IRSD score and RA was
Respondents were also asked questions about CPV vaccination proto- assessed by Spearman rank correlation statistics.
cols – at what age they recommend first and last puppy vaccination, the
frequency of puppy vaccinations, the age at which the first adult vac- 3. Results
cination is given, and how often they re-vaccinate adult dogs. They
were also asked if they made different recommendations in CPV out- 3.1. Demographics of respondents
break situations, for puppies or for adult dogs. Finally, respondents
were asked the percentage of each vaccine brand they use in their The most common age category of respondents was 31–40 years
practice and whether they use titer testing to determine whether to (147/569, 25.8%) and the least common was ≥61 (55/569, 9.7%).
proceed with vaccination against CPV. For vaccine brand percentage Respondents mostly graduated between 2000–2016 (258/569, 45.3%)
selection, respondents could choose a 10% increment between (and and most graduated from the University of Queensland (172/569,
including) 0% and 100%, as well as 5% or 95%. Total selections must 30.2%) or other Australian universities (319/569, 56.1%); 51/569

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M. Kelman, et al. Preventive Veterinary Medicine 174 (2020) 104817

Table 1 2260). Therefore, the highest and lowest quintiles were slightly over-
Personal demographics of veterinarian respondents in survey of Australian and under-represented, respectively. Hospitals from major cities were
veterinary practices regarding canine parvovirus occurrence, attitudes and the most common in the survey (314/534, 58.8%) with a decline in
preventative recommendations, 2017. representation the more remote the regions became. Hospitals from
Category Parameter No. of % areas designated “Remote Australia” were over-represented: 32.7% of
respondents all hospitals from this region responded (17/52) compared to all other
regions (range 23.0–24.4%). Slightly more hospitals did not see CPV
Age (years) 21 - 30 100 17.6
31 - 40 147 25.8
cases in 2016 compared to those that did (297 versus 237). Of the
41 - 50 130 22.8 hospitals that reported CPV cases, the majority had between 2 and 4.9
51 - 60 118 20.7 full-time-equivalent veterinary staff (48.0%, 123/256), and 32.8% (84/
61+ 55 9.7 256) reported performing some shelter-related or pound-related work
Didn't answer 19 3.3
(Table 2).
Total 569
Year of graduation 1958 - 1969 5 0.9
1970 - 1984 91 16.0
1985 - 1999 177 31.1 3.3. Veterinarians perceptions of canine parvovirus case numbers and
2000 - 2016 258 45.3
mortality
Didn't answer 38 6.7
Total 569
University of University of Queensland, 172 30.2 Veterinarian perceptions of annual national CPV caseload varied
Graduation QLD considerably (median 2000; range 10–2000,000; IQR 1000–5000).
University of Sydney, NSW 110 19.3 Respondents from hospitals that diagnosed CPV cases perceived the
Melbourne University, VIC 87 15.3
national CPV caseload 4.25 times higher than those whose hospitals
Murdoch University, WA 85 14.9
Other international 51 9.0 didn’t (median 4250, IQR 1000–10,000 versus median 1000, IQR
university 500–300; p < 0.0001). Perceptions of annual CPV caseload within the
Charles Sturt University, 20 3.5 respondent’s postcode also varied (median 10; range 0–5000; IQR
NSW 2–50) and there was a strong correlation between hospital caseload and
James Cook University, 12 2.1
QLD
respondent perception of local (in their postcode) caseload
University of Adelaide, SA 5 0.9 (rSP = 0.6638, p < 0.0001), and a moderate correlation with percep-
Didn't answer 27 4.7 tion of national caseload (rSP = 0.3587, p < 0.0001). Perceptions of
Total 569 national CPV mortality were more consistent: most respondents (272/
Current work sector Private Practice 530 93.1
569, 47.8%) suggested the median mortality value, 50% (range 5–90;
Shelter Sector 8 1.4
University 3 0.5 IQR 25–90), and there was no difference in CPV mortality rate per-
Corporate or industry 3 0.5 ceptions, regardless of hospital CPV caseload (p = 0.1422). There was a
Government 2 0.4 relatively normal distribution of CPV mortality estimates (Table 3).
Combined private/shelter 1 0.2
Other 3 0.5
Didn't answer 19 3.3
Total 569 3.4. Veterinarians standard recommendations for canine parvovirus
Previous work sector(s) Private Practice 429 75.4 vaccination
Private Practice and 23 4.0
Shelter Sector
The majority of veterinarians’ standard recommendation for first
Other (but not Shelter) 19 3.3
Private Practice and 15 2.6 puppy vaccination was at 6 weeks (422/569, 74.2%) or 8 weeks (141/
University 569, 24.8%) of age. Final puppy vaccination was most commonly re-
Shelter Sector 14 2.5 commended at 16 weeks (284/569, 49.9%) or 14 weeks (131/569,
Government 12 2.1 23.0%), though 10.9% (62/569) recommended 10 weeks of age. The
University 11 1.9
Other, including Shelter 10 1.8
most common vaccination interval was 4 weeks (484/568, 85.2%).
Sector Most respondents recommended first adult vaccination be given at 12
Private Practice and 6 1.1 months (542/568, 95.4%) and adult re-vaccination to be performed
Government either annually (286/569, 50.3%) or triennially (246/569, 43.2%).
Didn't answer 30 5.3
However, 6.5% of respondents (37/569) mentioned using other criteria
Total 569
before determining a re-vaccination interval, including antibody titer
testing (10/569, 1.8%) (Table 4).
(9.0%) graduated from a university outside of Australia. Most re-
spondents (530/569, 93.1%) worked in private practice at the time of
the survey, and the majority (429/539, 79.6%) had only worked pre- 3.5. Veterinarians recommendations during outbreaks, for canine
viously in private practice. Only 1.6% (9/569) currently worked in an parvovirus vaccination in puppies
animal shelter environment or a combination of private practice and
shelter, however 8.7% (47/539) had worked in a shelter environment Just over half the respondents (290/569, 51.0%) advised they
previously (Table 1). would make different recommendations during a CPV outbreak. The
most common change to vaccination protocols were different re-vac-
cination interval (168/290, 57.9%), different final puppy vaccination
3.2. Demographics of veterinary hospitals age (103/290, 35.5%) and different initial puppy vaccination age (54/
290, 18.6%). Of these changes, the most common recommendations
The most represented socioeconomic quintile in the survey was the were re-vaccination every 2 weeks (117/168, 69.6%), final puppy
highest (least disadvantaged; 28.8% of hospitals, 154/534). The least vaccination at 16 weeks (61/103, 59.2%) and first vaccination at 6
represented was the lowest (most disadvantaged; 12.9% of hospitals, weeks (28/54, 51.9%) (Table 5). A full analysis of responses is also
69/534). Nationally, 24.4% of veterinary hospitals populated the included in Supplementary Table 1.
highest quintile (552/2260) and 15.5% populated the lowest (351/

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M. Kelman, et al. Preventive Veterinary Medicine 174 (2020) 104817

Table 2
Veterinary hospital demographics of veterinarian respondents in survey of Australian veterinary practices regarding canine parvovirus occurrence, attitudes and
preventative recommendations, 2017.
Category Parameter No. of % Total % Percentage representation of Estimated Australian %
respondents hospitals respondents population 2017a

State NSW 144 27.0 690 30.5 20.9


QLD 132 24.7 544 24.1 24.3
VIC 101 18.9 511 22.6 19.8
WA 75 14.0 237 10.5 31.6
SA 38 7.1 168 7.4 22.6
TAS 26 4.9 57 2.5 45.6
ACT 13 2.4 31 1.4 41.9
NT 5 0.9 22 1.0 22.7
Total 534 2260
Index of Relative Socioeconomic 1 69 12.9 351 15.5 19.7 20.0
Disadvantage (IRSD) quintile 2 100 18.7 449 19.9 22.3 20.0
3 116 21.7 479 21.2 24.2 20.0
4 95 17.8 429 19.0 22.1 20.0
5 154 28.8 552 24.4 27.9 20.0
Total 534 2260
Remoteness Area (RA) Major Cities of 314 58.8 1342 59.4 23.4 1.8(10)7 71.8
Australia
6
Inner Regional 135 25.3 587 26.0 23.0 4.5(10) 17.8
Australia
6
Outer Regional 68 12.7 279 12.3 24.4 2.0(10) 8.3
Australia
Remote Australia 17 3.2 52 2.3 32.7 5.0(10)5 2.0
Total 534 2260 2.5(10)7
Saw CPV cases in 2015 or 2016 Yes 237 44.4
No 297 55.6
Total 534
Size of hospital (number of < 1 3 1.2
veterinarians)b 1 - 1.9 65 25.4
2 - 4.9 123 48.0
5 - 9.9 53 20.7
10 - 19.9 9 3.5
20 + 3 1.2
Total 256
Performs any shelter or pound-related Yes 84 32.8
workb No 172 67.2
Total 256

a
Population Estimates by Remoteness Area (ASGS 2016), 2007–2017 - Revised (Released 31/8/2018), source: https://www.abs.gov.au/AUSSTATS/abs@.nsf/
DetailsPage/3218.02016-17?OpenDocument.
b
Canine parvovirus-reporting clinics only.

3.6. Veterinarians recommendations for canine parvovirus vaccination in testing at some stage in their practice.
adult dogs during outbreaks
3.8. Veterinarians usage of vaccine types and strains
Only 24.4% (139/569) of respondents advised vaccinating adult
dogs differently in a CPV outbreak. Different re-vaccination timing was Vaccines classified as “annual re-vaccination” type were used by the
the main approach reported (59/139, 42.4%) with annual re-vaccina- majority of respondents with 47.3% (234/495) using only this vaccine
tion being the most common change (41/59, 69.5%). Of those who type. “Extended duration” (three-year) vaccines were used exclusively
advised another strategy, the most common was contacting clients to by 15.6% of respondents (100/495). The remainder used varying
recommend re-vaccination when pets were overdue (44/51, 86.3%) combinations of both vaccine types. From the vaccination usage index
(Supplementary Table 2). calculated, annual vaccination usage was approximately twice that of
the extended duration vaccines (66% versus 34%) (Table 7). Vaccines
3.7. Veterinarians use of titer testing strains were approximately equally distributed in usage by veterinar-
ians with 54.9% usage (calculated by index) of CPV2b strains versus
When questioned directly about antibody titer testing, only 10% 45.1% usage of CPV2 strain vaccines (Table 8).
(57/569) of respondents advised outright that they used this in their
veterinary practice, while 72.2% (411/569) did not (Table 6). The re- 4. Discussion
maining 17.8% (101/569) answered neither yes or no, but gave a de-
scriptive response providing further information. This information has Our study found significant variation between veterinarians’ per-
been included in Supplementary Table 3. Four “other” responses were ceptions of national CPV occurrence, mortality and their re-
re-categorized as yes (2) and no (2) for the analysis in Supplementary commendations for vaccination protocols. The perceived disease mor-
Table 3 while Table 6 left these responses as ‘other’. The most common tality, excluding euthanasia (50%), was 2.74 times higher than the
further clarification statements made were providing a titer test upon previously reported rate for CPV in Australia (18.2%) from a nationally-
client request (33/97, 34.0%), titer testing performed occasionally but operating disease surveillance system (Ling et al., 2012). This suggests
no reason given why (32/97, 33.0%), and it was performed if a client veterinarians’ perceptions of CPV prognosis is worse than actually oc-
requested or if vaccination was contraindicated (13/97, 7.2%). In total, curs which may lead to higher euthanasia recommendations than is
26.7% (152/569) of respondents indicated that they might use titer necessary. Higher treatment-cost estimates to clients may also result,

4
M. Kelman, et al. Preventive Veterinary Medicine 174 (2020) 104817

Table 3
Veterinarians perceptions of canine parvovirus (CPV) caseload and mortality in Australia, grouped by whether the respondent’s hospital saw CPV cases in 2015 or
2016 and by hospital CPV caseload.
Respondent perception Category Variable Descriptive statistics Kruskal-Wallis One-Way Spearman Rank
Analysis of Variance Correlation

N Min Max Median Interquartile Mean rank P value r P value


range

National CPV caseload, per Whether the hospital No 291 10 100000 1000 500 - 3000 231.3a < 0.0001
annum saw CPV in 2015 or Yes 278 10 2000000 4250 1000 - 10000 341.3a
2016
Hospital CPV 0 310 10 100000 1000 500 - 3000 229.6abcd
caseload in 2016 1-6 125 100 1500000 4000 1000 - 10000 333.1a 0.0275 0.3587 < 0.0001
7-15 54 250 1000000 4000 1000 - 6375 331.1b
16-40 49 300 100000 5000 2000 - 10000 383.8c
40+ 31 400 2000000 5000 2000 - 20000 408.7d
CPV caseload in their Whether the hospital No 291 0 1000 3.0 0 - 1000 191.3a < 0.0001
postcode, per annum saw CPV in 2015 or Yes 278 0 5000 42.5 10 - 5000 383.1a
2016
Hospital CPV 0 310 0 1000 4 0 - 10 194.4abcd < 0.0001 0.6638 < 0.0001
caseload in 2016 1-6 125 0 5000 15 10 - 50 330.4abcd
7-15 54 0 500 50 20 - 112.5 411.5b
16-40 49 0 1000 100 55 - 200 465.1c
40+ 31 5 5000 250 100 - 500 502.6d
CPV mortality rate Whether the hospital No 291 5 90 50 25 - 50 288.7 0.5254
percentage, nationally saw CPV in 2015 or Yes 278 5 90 50 25 - 50 281.1
2016
Hospital CPV 0 310 5 90 50 25 - 50 281.3 0.1422 0.0304 0.5003
caseload in 2016 1-6 125 5 90 50 25 - 50 285.8
7-15 54 10 90 50 25 - 50 287.3
16-40 49 10 90 50 50 - 75 328.4
40+ 31 5 75 50 25 - 50 246.9

indirectly influencing euthanasia rates. weeks of age.


A strong correlation between hospital caseload and perception of Nearly half (48.7%) of respondents recommended in non-outbreak
local caseload reflects that veterinarians are, in general, aware of the circumstances, final puppy vaccination earlier than 16 weeks of age,
risk of CPV in their regions. However, median perceived national CPV which is not considered best practice by KOL guidelines (Australian
caseload (2000 cases) was ten times lower than the estimated national Veterinary Association, 2018; Day et al., 2016) due to risk of MDA
caseload (20,000 cases) (Kelman et al., 2019), reflecting that veter- interference. It is worth noting that the current AVA policy was not
inarians may not be aware of the extent of CPV disease caseload, na- released until after our survey, so veterinarian recommendations may
tionally. Perception of national caseload was further reduced (median have changed since then to be more aligned with these guidelines. A
1000 cases) for respondents of hospitals that had no CPV cases present puppy re-vaccination interval of 5 or 6 weeks was recommended by
to them in 2016. Given that full-scale national disease reporting for 2.8% of respondents, which is an off-label vaccine usage not re-
companion animals has not occurred historically (Ward and Kelman, commended by any guidelines. This study did not examine whether
2011), this is not an unexpected finding. This lack of awareness could these vaccination usage patterns occurred in high-risk regions, which is
be an impediment to efforts to reduce disease cases through prevention another area for further research.
strategies and could be a significant risk factor for future outbreaks During a CPV outbreak, 51% of respondents advised they would
(Funk et al., 2009). While disease surveillance and communications for change their vaccination protocol, and the most cited changes brought
production animal species and zoonotic disease is supported by gov- respondents in alignment with WSAVA or AVA guidelines (2 week re-
ernment, for companion animals this falls on universities and not-for- vaccination interval, 16 week final puppy vaccination or 6 week first
profit animal welfare organizations, with limited funds (Australian vaccination). Only three vaccine brand labels (Canigen®, Virbac
Veterinary Association, 2019). Greater governance and financial sup- Australia; Canvac®, Zoetis Australia; Companion®, MSD Animal Health)
port for companion animals in this area could have a significant impact carried alternative recommendations for protocols in outbreak cir-
on disease control. cumstances. In one study, final puppy vaccination at 12 weeks resulted
An initial vaccination age of 6 to 8 weeks and re-vaccination every 2 in 8% of puppies failing to seroconvert (Friedrich and Truyen, 2000)
to 4 weeks are the recommendations of the World Small Animal and in another, 80% of vaccination failures occurred when final vac-
Veterinary Association (WSAVA) vaccination guidelines (Day et al., cination was given < 16 weeks of age (Altman et al., 2017). These
2016) and the Australian Veterinary Association’s (AVA) current vac- findings suggest that later vaccination should be implemented, espe-
cination policy (Australian Veterinary Association, 2018). The majority cially in higher-risk areas or during outbreaks.
of respondents supported these recommendations, which also aligns Almost all veterinarians (95.4%) recommended that the first ‘adult’
with the label statements of Australian commercial vaccines (http:// vaccination at 12 months of age; only 2.1% recommended the earlier ‘6-
www.infopest.com.au). However, an area where KOL guidelines dif- month adult vaccination’, which is a new feature of the 2016 WSAVA
fered from labels was the age for final puppy vaccination. Only one vaccination guidelines (Day et al., 2016). Adult re-vaccination was
vaccine brand label (Parvac®, Zoetis Australia) recommended final performed slightly more commonly annually (50.3%) than triennially
puppy vaccination at ≥16 weeks of age, in agreement with guidelines. (43.2%) and may reflect veterinarians’ concerns over CPV risk in their
However this is the only inactivated CPV vaccine in the Australian area. However, this issue was not analyzed in the current study and is
market and inactivated CPV vaccines may induce a lower immune re- an area for future research. The higher annual vaccine brand usage
sponse than attenuated vaccines (Day et al., 2016). The remainder of reported was likely due to use of this product for re-vaccination in
vaccines recommended final puppy vaccination at either 10 or 12 puppies. The effectiveness of annual versus triennial revaccination

5
M. Kelman, et al. Preventive Veterinary Medicine 174 (2020) 104817

Table 4 Table 5
Australian veterinarians standard (non-outbreak) recommendations for canine Australian veterinarians most reported alternative recommendations for canine
parvovirus vaccination protocols, 2017. parvovirus vaccination protocol in puppies during outbreak conditions, 2017.
Category Parameter No. of % Category Parameter No. of %
respondents respondents

Latest age for 1 st puppy 6 422 74.2 Different recommendations, in a CPV Yes 290 51.0
vaccination (weeks) 7 1 0.2 outbreak situation No 249 43.8
8 141 24.8 Never been in 25 4.4
10 5 0.9 an outbreak
Total 569 Didn't answer 5 0.9
Latest age for final puppy 10 62 10.9 Total 569
vaccination (weeks) 12 84 14.8 Different re-vaccination interval Every 1-2 weeks 1 0.6
14 131 23.0 Every 2 weeks 117 69.6
16 284 49.9 Every 2-3 weeks 8 4.8
20 2 0.4 Every 2-4 weeks 8 4.8
24 2 0.4 Every 3 weeks 17 10.1
Not Specified 4 0.7 Every 3-4 weeks 3 1.8
Total 569 Every 4 weeks 14 8.3
Interval between puppy 2 22 3.9 Total 168
vaccinations (weeks) 3 36 6.3 Different vaccination starting age 2 weeks 1 1.9
4 484 85.2 4 weeks 11 20.4
5 1 0.2 5 weeks 4 7.4
6 15 2.6 Before 6 weeks 4 7.4
Not Specified 10 1.8 6 weeks 28 51.9
Total 568 Before 8 weeks 3 5.6
Recommended age for 1 st adult 6 12 2.1 8 weeks 1 1.9
vaccination (months) 9 2 0.4 10 weeks 1 1.9
12 542 95.4 16 weeks 1 1.9
15 7 1.2 Total 54
36 2 0.4 Different vaccination finishing age 10 weeks 2 1.9
Not a specific age, 3 0.5 After 10 weeks 1 1.0
as required 12 weeks 10 9.7
Total 568 12-16 weeks 1 1.0
Adult Vac Interval (years) 1 286 50.3 14 weeks 11 10.7
3 246 43.2 14-16 weeks 5 4.9
Dependent on other 17 3.0 15 weeks 1 1.0
factors 16 weeks 61 59.2
Titre result 10 1.8 16-18 weeks 1 1.0
dependent 16-20 weeks 1 1.0
Client given choice 5 0.9 20 weeks 7 6.8
Other 5 0.9 6 months 2 1.9
Total 569 Total 103

strategies for preventing disease has never been compared. While ser- Table 6
ological studies support that many dogs will have CPV titers considered Australian veterinarians reported usage of titer testing, 2017.
protective against disease for greater than 1 year, some will not (Moore Parameter No. of respondents %
and Glickman, 2004; Roth and Spickler, 2010) and opinions remain
divided whether reduced adult re-vaccination frequency poses an in- Yes - do use 57 10.0
creased risk for disease, particularly in outbreak conditions. No - don't use 411 72.2
Other 101 17.8
Our study identified that vaccine strain usage in Australia was ap- Total 569
proximately equal between CPV2 and CPV2b at the time of the survey.
It has been suggested that vaccine strain may be a risk-factor for vac-
cination failure and that newer CPV variants may be less protected by socioeconomic disadvantage, remoteness or perceptions around CPV
the ‘original’ CPV2 strain vaccines (Cavalli et al., 2008; Decaro et al., are factors involved in veterinarians decisions for CPV prevention and
2009; Pratelli et al., 2001), however recent Australian research de- treatment. This will be followed up in a subsequent study.
monstrated no difference in failure rates between the two commercially
available strains (Altman et al., 2017). The reported disease occurrence
rate of wild CPV strains in Australia, CPV2a and CPV2b, was 54% and 5. Conclusions
46% respectively between 2007 and 2016 (Clark et al., 2018), although
3 cases of CPV2c have also been reported from Adelaide in 2015 Raising veterinarians’ awareness on CPV mortality rates, case oc-
(Woolford et al., 2017). Ongoing monitoring of vaccine strain usage and currence outside their immediate area, and KOL vaccination guidelines
vaccination failures will help determine if vaccine strain is a risk factor could result in improvements to prevention and treatment strategies
for vaccination failure. that reduce risk of future CPV outbreaks and reduce case fatality rates.
One limitation of this study was the slightly skewed populations Even though this study was limited to Australia, it is likely that similar
when grouped by state, IRSD and RA, and estimations of case numbers findings would be reflected internationally.
provided by 70% of respondents which might affect some results.
However, age distribution in our study approximated that of a national
veterinary workforce study from the previous year (Australian Declaration of competing interest
Veterinary Association, 2016) and our study was broadly representative
nationally when analyzed at the electoral division level (Kelman et al., The authors have no conflicts of interest to report.
2019). Further analysis is needed to examine whether demographics,

6
M. Kelman, et al. Preventive Veterinary Medicine 174 (2020) 104817

Table 7 Australian Veterinary Association, 2018. Vaccination of Dogs and Cats - AVA Policy 2018
Veterinarians reported usage of vaccine types - annual or 3 year duration of [WWW Document]. Vaccination of Dogs and Cats. (accessed 8.25.18). https://www.
immunity (DOI) vaccines, 2017. ava.com.au/node/112438.
Australian Veterinary Association, 2016. Australian Veterinary Workforce Survey 2016.
Vaccine usage Vaccine usage indexa British Small Animal Veterinary Association, 2019. Vaccination Guidance for Boarding
Establishments and Local Authorities.
Annual % 3 year DOI % Frequency % Frequency Annual 3 year DOI Cavalli, A., Martella, V., Desario, C., Camero, M., Bellacicco, A.L., Palo, P.D., Decaro, N.,
Elia, G., Buonavoglia, C., 2008. Evaluation of the antigenic relationships among ca-
0 100 77 15.6 0.0 1555.6 nine parvovirus type 2 variants. Clin. Vaccine Immunol. 15, 534–539. https://doi.
org/10.1128/CVI.00444-07.
5 95 11 2.2 11.1 211.1
Christiansen, S.B., Kristensen, A.T., Lassen, J., Sandøe, P., 2015. Veterinarians’ role in
10 90 13 2.6 26.3 236.4
clients’ decision-making regarding seriously ill companion animal patients. Acta Vet.
20 80 23 4.6 92.9 371.7 Scand. 58, 30. https://doi.org/10.1186/s13028-016-0211-x.
30 70 19 3.8 115.2 268.7 Clark, N.J., Seddon, J.M., Kyaw-Tanner, M., Al-Alawneh, J., Harper, G., McDonagh, P.,
40 60 13 2.6 105.1 157.6 Meers, J., 2018. Emergence of canine parvovirus subtype 2b (CPV-2b) infections in
45 55 1 0.2 9.1 11.1 Australian dogs. Infect. Genet. Evol. 58, 50–55. https://doi.org/10.1016/j.meegid.
50 50 31 6.3 313.1 313.1 2017.12.013.
60 40 15 3.0 181.8 121.2 Day, M.J., Horzinek, M.C., Schultz, R.D., 2016. Guidelines for the vaccination of dogs and
70 30 9 1.8 127.3 54.5 cats. J. Small Anim. Pract. 57, E1–E45.
80 20 5 1.0 80.8 20.2 Decaro, N., Buonavoglia, C., 2012. Canine parvovirus—a review of epidemiological and
90 10 20 4.0 363.6 40.4 diagnostic aspects, with emphasis on type 2c. Vet. Microbiol. 155, 1–12. https://doi.
95 5 24 4.8 460.6 24.2 org/10.1016/j.vetmic.2011.09.007.
100 0 234 47.3 4727.3 0.0 Decaro, N., Campolo, M., Desario, C., Elia, G., Martella, V., Lorusso, E., Buonavoglia, C.,
2005. Maternally-derived antibodies in pups and protection from canine parvovirus
Total 495 6614.1 3385.9
infection. Biologicals 33, 261–267. https://doi.org/10.1016/j.biologicals.2005.06.
Percentage 66.1% 33.9%
004.
a
Decaro, N., Cirone, F., Desario, C., Elia, G., Lorusso, E., Colaianni, M.L., Martella, V.,
Vaccine usage index calculated by multiplying vaccine usage percentage Buonavoglia, C., 2009. Severe parvovirus in a 12-year-old dog that had been re-
with frequency of hospitals reporting this usage. peatedly vaccinated. Vet. Rec. 164, 593–595. https://doi.org/10.1136/vr.164.19.
593.
Decaro, N., Desario, C., Campolo, M., Cavalli, A., Ricci, D., Martella, V., Tempesta, M.,
Table 8 Buonavoglia, C., 2004. Evaluation of lactogenic immunity to canine parvovirus in
Veterinarians reported usage of vaccine strain – CPV2 or CPV2b vaccines, 2017. pups. New Microbiol. 27, 375.
Decaro, N., Desario, C., Elia, G., Campolo, M., Lorusso, A., Mari, V., Martella, V.,
Vaccine usage CPV2 CPV2b Vaccine usage indexa Buonavoglia, C., 2007. Occurrence of severe gastroenteritis in pups after canine
parvovirus vaccine administration: a clinical and laboratory diagnostic dilemma.
(%) Frequency % Frequency % CPV2 CPV2b Vaccine 25, 1161–1166. https://doi.org/10.1016/j.vaccine.2006.10.020.
Decaro, N., Desario, C., Elia, G., Martella, V., Mari, V., Lavazza, A., Nardi, M.,
5 9 2.2 9 2.2 11.0 11.0 Buonavoglia, C., 2008. Evidence for immunisation failure in vaccinated adult dogs
10 11 2.7 6 1.5 26.9 14.7 infected with canine parvovirus type 2c. Microbiologica-Quarterly Journal of
20 6 1.5 6 1.5 29.3 29.3 Microbiological Sciences 31, 125–130.
30 6 1.5 2 0.5 44.0 14.7 Filipov, C., Desario, C., Patouchas, O., Eftimov, P., Gruichev, G., Manov, V., Filipov, G.,
40 4 1.0 1 0.2 39.1 9.8 Buonavoglia, C., Decaro, N., 2016. A ten-year molecular survey on parvoviruses in-
50 10 2.4 10 2.4 122.2 122.2 fecting carnivores in Bulgaria. Transbound. Emerg. Dis. 63, 460–464. https://doi.
60 1 0.2 3 0.7 14.7 44.0 org/10.1111/tbed.12285.
70 2 0.5 1 0.2 34.2 17.1 Ford, R.B., Larson, L.J., Schultz, R.D., Welborn, L.V., 2017. 2017 AAHA canine vacci-
nation guidelines. J. Am. Anim. Hosp. Assoc. 53, 243–251.
80 1 0.2 6 1.5 19.6 117.4
Friedrich, K., Truyen, U., 2000. Untersuchung der wirksamkeit von parvovirusimpfstoffen
90 5 1.2 6 1.5 110.0 132.0
und der effektivaitat zweier impfschemata. Praktischer Tierarzt 81, 988–994.
95 6 1.5 11 2.7 139.4 255.5
Funk, S., Gilad, E., Watkins, C., Jansen, V.A.A., 2009. The spread of awareness and its
100 9 2.2 9 2.2 220.0 220.0 impact on epidemic outbreaks. Proc. Natl. Acad. Sci. 106, 6872–6877. https://doi.
Total 190 46.5 219 53.5 810.5 987.8 org/10.1073/pnas.0810762106.
Percentage 45.1% 54.9% Goddard, A., Leisewitz, A.L., 2010. Canine parvovirus. Vet. Clin. North Am. Small Anim.
Pract. 40, 1041–1053. https://doi.org/10.1016/j.cvsm.2010.07.007.
a
Vaccine usage index calculated by multiplying vaccine usage percentage Kelman, M., Ward, M.P., Barrs, V.R., Norris, J.M., 2019. The geographic distribution and
with frequency of hospitals reporting this usage. financial impact of canine parvovirus in Australia. Transbound. Emerg. Dis. 66,
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Ling, M., Norris, J.M., Kelman, M., Ward, M.P., 2012. Risk factors for death from canine
Acknowledgements parvoviral-related disease in Australia. Vet. Microbiol. 158, 280–290. https://doi.
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Macartney, L., Thompson, H., McCandlish, I.A., Cornwell, H.J., 1988. Canine parvovirus:
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interaction between passive immunity and virulent challenge. Vet. Rec. 122,
the survey and the veterinary students and non‐veterinary volunteers 573–576. https://doi.org/10.1136/vr.122.24.573.
who helped to contact hospitals to seek their involvement. The research Mila, H., Grellet, A., Desario, C., Feugier, A., Decaro, N., Buonavoglia, C., Chastant-
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in this paper was completed in partial fulfilment for the requirements of
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a PhD degree at The University of Sydney by the lead author. 2014.57.
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