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Article

An investigation of ear necrosis in pigs


Jeonghwa Park, Robert M. Friendship, Zvonimir Poljak, Josepha DeLay, Durda Slavic,
Catherine E. Dewey

Abstract — Porcine ear necrosis was investigated in 23 conveniently chosen farms, consisting of 14 case farms
and 9 control farms. Biopsies of lesions and oral swabs from pigs on 11 case farms were examined by histology
and bacterial culture. All farms were visited for observations and a survey on management, housing, and the pres-
ence of other clinical signs or behavioral vices. Histological examination revealed that the lesions began on the
surface and progressed to deeper layers, and that vascular damage did not appear to be the initiating cause.
Spirochetes were only rarely observed in histological examination and were not cultured from biopsies and oral
swabs. Staphylococcus aureus and Staphylococcus hyicus were cultured from 91% and 66% of samples, respectively.
Ear biting and a humid environment were associated with ear necrosis. On some farms large numbers of pigs were
affected and lesions were sometimes extensive. The condition appears to be an infectious disease beginning on the
surface of the skin; contributing environmental and management factors are likely.

Résumé — Enquête sur la nécrose des oreilles chez les porcs. La nécrose des oreilles porcines a fait l’objet d’une
enquête dans un échantillonnage de convenance de 23 fermes, composé de 14 fermes de cas et de 9 fermes témoins.
Les biopsies de lésions et des prélèvements oraux faits chez des porcs dans 11 fermes de cas ont été examinés par
histologie et culture bactérienne. Toutes les fermes ont été visitées pour recueillir des observations et effectuer un
examen de la gestion, du logement et de la présence d’autres signes cliniques ou vices de comportement. L’examen
histologique a révélé que les lésions commençaient sur la surface et progressaient vers des couches plus profondes
et que les dommages vasculaires ne semblaient pas être la cause initiale. Des spirochètes ont été rarement observés
à l’examen histologique et n’ont pas été cultivés dans les biopsies et les prélèvements oraux. Staphylococcus aureus
et Staphylococcus hyicus ont été cultivés dans 91 % et 66 % des échantillons, respectivement. Les morsures d’oreilles
et un environnement humide étaient associés à la nécrose des oreilles. Dans certaines fermes, un grand nombre de
porcs étaient affectés et les lésions étaient parfois importantes. L’affection semble être une maladie infectieuse qui
commence à la surface de la peau; des facteurs contributifs liés à l’environnement et à la gestion sont probables.
(Traduit par Isabelle Vallières)
Can Vet J 2013;54:491–495

Introduction ears (1). Little is understood regarding the risk factors that
influence severity and prevalence of ear necrosis. In general, ear
Ear necrosis is a common problem on Canadian pig farms and
necrosis is considered to have little effect on pig performance, at
several etiologies have been proposed but not confirmed. The
least when the lesions are only mild to moderate (2). However,
clinical manifestation of ear necrosis has been described as the
the unsightly visual appearance could interfere with the sale of
appearance of open wounds, crust, and bleeding on 1 or both
affected pigs, and raise welfare concerns.
The etiology of ear necrosis is unknown. Staphylococcus hyicus
Department of Population Medicine, Ontario Veterinary and Staphylococcus aureus have been suggested as potential
College, Guelph, Ontario (Park, Friendship, Poljak, Dewey), causative agents because of the similarity of histopathological
Animal Health Laboratory, University of Guelph, Guelph, lesions and bacterial cultural results between ear necrosis and
Ontario (DeLay, Slavic). exudative epidermitis (3–5). The pathogenesis of staphylococcal
Address all correspondence to Dr. Jeonghwa Park; e-mail: skin disease involves bacterial production of exfoliative toxins
jeonghwa@uoguelph.ca (ETs) which act as “molecular scissors” to cleave the epidermis
Use of this article is limited to a single copy for personal study. of mammalian skin (6). For a long time it was thought that
Anyone interested in obtaining reprints should contact the S. aureus ETs did not affect the epidermis of pigs (7); however,
CVMA office (hbroughton@cvma-acmv.org) for additional recent findings have demonstrated the targeting of desmoglein1
copies or permission to use this material elsewhere. in pig skin by S. aureus ETB and ETD (6). Spirochetes have

CVJ / VOL 54 / MAY 2013 491


also been considered as potential causative agents of ear necrosis to capture the margin of normal and lesional skin. A cotton
(8) and in 1 recent study spirochetes (genus Treponema) were swab was used to sample the mouth (especially around the
cultured and identified from ear necrosis lesions (9). gums) of the same pig and was placed in a tube with FAB
Clinical lesions of ear necrosis need to be differentiated from for culture of spirochetes. All samples were transported in an
secondary skin lesions developing occasionally at ear tips as insulated container and submitted on the day of collection by
a result of vasculitis associated with systemic diseases such as taking them directly to the Animal Health Laboratory (AHL),
salmonellosis and classical swine fever (10). An argument has University of Guelph, Guelph, Ontario. Bacterial culture was
A R T I C LE

been made that ear necrosis is the result of ischemic injury due performed and bacteria were identified as S. hyicus and S. aureus
to thrombosis of the small dermal capillaries in the tips of the by standard laboratory techniques including colony morphol-
ears as a result of immune-complex deposition, as occurs in ogy, hemolysis, Gram-stain, catalase reaction, and coagulase
porcine circovirus associated disease (PCVAD) (11), or due to reaction. Antimicrobial susceptibility testing with penicillin G,
mycotoxin-associated vasculopathy (10). ampicillin, ceftiofur, spectinomycin, sulphonamide, tetracycline,
Ear necrosis appears to be influenced by environmental tiamulin, and trimethoprim/­sulfamethoxazole was determined
and management factors. Purchased feed, fully slatted floor- by the disk diffusion method (Kirby-Bauer Procedure) defined
ing without straw, poor air quality and high humidity, and a by the Clinical and Laboratory Standards Institute (14). For
high stocking density of newly weaned pigs have been found to the purpose of analyzing the data, isolates classed as intermedi-
increase the risk of ear necrosis (12). Dry feed, early weaning, ate susceptibility were included with the bacteria identified as
poor housing conditions, fighting, feed and dirt on the tips of resistant.
ears, and concurrent mange have also been identified as possible Culture of spirochetes was performed following the method
risk factors (4,13). described by Pringle et al (9). Ear tissues and oral samples in
The objectives of this study were to: describe clinical and FAB were incubated for 24 to 48 h at 37°C in an anaerobic
histopathological lesions of ear necrosis; determine the presence chamber. One drop of the broth culture was added to a 0.22 mm
of potential pathogens, particularly Staphylococcus species and membrane filter placed on fastidious anaerobe agar with 10%
spirochetes; and determine herd-level risk factors of ear necrosis. horse blood. Following incubation of the agar plate at 37°C for
2 to 3 days in an anaerobic chamber, the bacterial growth under
Materials and methods the filter was examined by phase contrast microscopy.
A total of 23 conveniently selected farms were used in the study
(14 case farms and 9 control farms). To be included as a control Histopathological examination
farm, the farm owner or manager had to report that the farm Following 24 h fixation in 10% neutral buffered formalin,
had no history of clinical signs of ear necrosis, and the absence skin biopsies were processed for histologic examination. Where
of ear necrosis had to be confirmed by the researchers through sufficiently large, biopsies were bisected prior to processing,
an on-farm visit. All farms were visited between May 2010 and and all biopsies were processed in total. Serial tissue sections
April 2011, and the observations were conducted by the same (4 mm) from each biopsy were stained with hematoxylin and
individual on all farms. The research was approved by the animal eosin (H&E) and Warthin-Starry silver (WS) and were examined
care committee of the University of Guelph. using light microscopy by a single pathologist (JD).
Immunohistochemistry (IHC) for Treponema spp. was per-
Investigation of potential causative organisms formed on tissue sections from those cases in which spirochetes
Sampling for bacterial culture were identified by WS stain.
Material for diagnostic purposes was collected from 11 of
the 14 case farms. On each farm, 9 pigs were selected for Investigation of risk factors at farm level
testing by choosing 3 pigs from early, mid, and late stages of All 23 farms were visited and a questionnaire was administered to
clinical disease. Early-disease stage groups consisted of pigs the producers during a face-to-face interview. Information from
with small black scabs on their ears and were from pigs in the the questionnaire included: farm demographics, weaning age, pig
youngest affected age group. Mid-disease stage groups were flow, cleaning procedures, vaccination and medication regimens,
slightly older (1 or 2 wk) and generally exhibited lesions that feeding information, and source of pigs. In addition, observa-
had progressed to open wounds, thick scabs, and some loss tion notes for each disease-stage group were completed by the
of ear tissue. Late-disease stage groups were the oldest pigs, researchers after collecting samples during the visit to the farm.
which generally showed lesions that had resolved but bleeding Information collected through on-farm observation included: the
wounds and thick scabs were still common. Three wedge- prevalence of ear necrosis for each disease stage, a description of
shaped ear tissue biopsies and an oral swab were taken from the lesions, the presence of clinical signs other than ear necrosis
each pig. One biopsy sample was placed in a sterile plastic tube and the presence or absence of behavioral vices. A description of
for culture of S. hyicus and S. aureus. Another biopsy sample the facilities, noting the stocking density, type of flooring, feeder
was placed in a tube with fastidious anaerobe broth (FAB), and waterer type, and room temperature was recorded. A subjective
(LAB 71, Lab M, Heywood, Lancashire, UK) for culture of assessment of humidity and air quality in the pen was recorded.
spirochetes. A third biopsy sample was placed in a 100 mL On control farms, groups of pigs that were comparable to the age
jar containing 50 mL of 10% formalin solution for histologic of early, mid, and late disease stages for case farms were chosen for
examination. For the histology samples, an effort was made observation.

492 CVJ / VOL 54 / MAY 2013


Data management and statistical analysis Case farms
Information from survey questionnaires and observation notes
S. hyicus
for each stage were entered separately into Epi-data Software

Percent of isolates resistant


S. aureus
(EpiData Entry version 3; The EpiData Association, Odense M,
Denmark) and imported to Stata software (Stata Intercooled,
version 10; Stata Corporation, College Station, Texas, USA) for
further processing and analysis. Initially, data were checked for

A R T I C LE
accuracy, consistency, and missing values.
The average prevalence of ear necrosis in each stage group
was estimated as the number of pigs affected with ear necrosis
divided by total number of pigs in the pen.
Unconditional association between ear necrosis status of
farms and putative risk factors, obtained from the survey and
observation notes were evaluated using a chi-squared test or Antimicrobials
Mann-Whitney U-test, as appropriate (P , 0.05). Variables
Figure 1.  Antimicrobial resistance profiles of S. hyicus and
in the survey were measured at the farm level and the vari- S. aureus from clinical cases of ear necrosis.
ables in the observation notes were measured for each of the pen — penicillin G, amp — ampicillin, cef — ceftiofur, spec — spectinomycin,
tet — tetracycline, tia — tiamulin, sul — sulphonamide, trisul — trimethoprim-
3 stage groups at farm-level. These were then offered as sepa- sulfamethoxazole. Number of S. hyicus isolates is 63; number of
rate variables in a different stage group modeling. Initially, a S. aureus isolates is 87.
total of 16 variables was obtained from the survey and each of
21 variables obtained in early, mid, and late stage groups from
the observation notes were examined. Correlation analysis was Spirochetes
performed using the Spearman’s rank correlation statistic to Attempts to culture spirochetes from ear biopsies and oral swabs
identify collinearity among variables. Independent variables were unsuccessful. In WS-stained ear biopsies, spirochetes were
associated with the dependent variable at a 20% significance identified in 5 pigs (5.2%), including 4 pigs (11.1%, 4/36) from
level (P , 0.2) in unconditional screening were considered the early stage group and 1 pig (3.7%, 1/27) from the mid-stage
primary predictors of interest and were included in the multi- group. Spirochetes in 4 of 5 WS-positive biopsies were confirmed
variable main effects model. Then the presence or absence of as Treponema spp. by IHC. Spirochetes were clustered within
lesions of ear necrosis on the farm as the dependent variable crusts or pustules, or were located at margins of ulcerated foci in
was regressed on these primary predictors using multivariable the epidermis. In the spirochete-positive group, 3 pigs were posi-
logistic regression. Manual model building, which combined tive for S. hyicus, S. aureus, and spirochetes (3.1%, 3/96); 1 pig
forward selection, was employed in building a multivariable was positive for S. aureus and spirochetes (1%, 1/96); and 1 pig
model. Model fitting was evaluated by the Pearson Goodness of was positive only for spirochetes (1%, 1/96). Farm prevalence of
fit test. spirochetes was 36.4% (4/11).

Results Histological examination


Investigation of potential causative organisms Biopsies from the majority of affected pigs demonstrated crust-
Staphylococcal culture ing erosive to ulcerative pinnal dermatitis with variably severe
A total of 96 pigs were selected from 11 case farms (mean: neutrophilic dermatitis and large numbers of bacterial cocci in
8.7 pigs/farm). The recovery rate of S. hyicus from ear tissue crusts. Lesions in affected pigs consistently involved epidermis,
biopsies was 66% and the recovery rate of S. aureus from ear and were typically more severe in epidermis than in underlying
tissue biopsies was 91%. There was no significant difference dermis. Superficial dermal inflammation was dominated by neu-
in the recovery rates (Wald X 2 P = 0.36). Both S. aureus and trophils, with fewer lymphocytes and histocytes. In a few cases,
S. hyicus were recovered from 58.3% of pigs, whereas S. aureus vasculitis or overt thrombosis was evident (6/96) and vascular
was recovered alone from 32.3% of the pigs and S. hyicus was lesions were associated with foci of epidermal ulceration and
recovered alone from 7.3% of the pigs. At the farm level, the dermal necrosis/inflammation. Dermal granulation tissue and
recovery rate was 90.9% (10/11) and 100% (11/11) for S. hyicus fibrosis, indicative of lesion chronicity, were present in 25/96
and S. aureus, respectively, based on at least 1 positive isolate (26%) cases.
from a farm. The recovery rates of S. hyicus were 76.9%, 66.7%,
66.7%, in early, mid, and late stages, respectively. The recovery Risk factors at the farm level
rates of S. aureus were 82%, 93.3%, and 90%, in early, mid, The average prevalence rates of ear necrosis on case farms were:
and late stages, respectively. Antimicrobial resistance profiles 31.6% [standard deviation (SD): 32.8], 44.2% (SD: 36.1), and
of S. hyicus and S. aureus isolates are presented in Figure 1. 54.8% (SD: 38.1)] for early, mid, and late stages, respectively.
The most common resistance pattern of S. hyicus isolates The average ages of each disease stage group on case and control
was penicillin G-ampicillin-ceftiofur (27.8%), and the most farms are presented in Table 1. The degree of severity varied
common resistance pattern of S. aureus isolates was penicillin between farm and within farm. The most severe lesions resulted
G-ampicillin-ceftiofur-tetracycline (20.4%). in the loss of as much as one-third of the ear.

CVJ / VOL 54 / MAY 2013 493


Table 1.  The average ages of pigs showing clinical signs of early, Table 2.  Descriptive statistics of variables in survey questionnaires
mid, and late stage ear necrosis on case farms (n = 14) and the found to be unconditionally associated with ear necrosis status of
ages of pigs on control farms (n = 9) that were used in the study the farm (P , 0.2)
Early Mid Late Early-Lateb Variables Case mean (SD) Control mean (SD) P-value
Case (wk) 6.6 (3–12)a 7.7 (5–13) 10 (5–16) 3.7 Minimum weaning 16.9 (1.15) 27 (1.72) 0.05
Control (wk) 5.7 (3–12) 8.4 (6–12) 14 (8–20) 8.6   age (days)
a Range.
Average weaning 20.7 (0.99) 28.6 (3.31) 0.06
  age (days)
A R T I C LE

b The mean of age-difference from early to late stage.


Number of sows 871.1 (287.07) 357.4 (121.15) 0.2
  on farm
Zinc level in feed
The variables in survey questionnaires, which were found to   (ppm) 191.3 (41.7) 1009.8 (465.7) 0.2
be unconditionally associated with ear necrosis status of the farm Downtime after 1.9 (0.32) 1.1 (0.4) 0.2
under P , 0.2, are presented in Table 2. Based on observation   washing (days)
notes, the variables in early, mid, and late stage groups, which SD — standard deviation.
were unconditionally associated with ear necrosis status of the
farm under P , 0.2, are presented in Table 3. In the multivari- Table 3.  Descriptive statistics of variables unconditionally
able model of observation notes, the variables of perception of associated (P , 0.2) with pigs showing clinical signs of early,
mid, and late stage ear necrosis based on observations
high humidity and the presence of ear biting were significantly
associated with the presence of ear necrosis (Table 4). No evi- Variables Compared with P-value
dence of a confounding effect was found within the variables in High humidity in the pen Moderate and low humidity 0.01
the final model. Similarly, no statistically significant interaction   in the pen
Presence of ear biting 0.01
effects were identified (P . 0.05). Visual assessment of residuals Presence of tail biting 0.01
was performed and this identified an outlier, but no coefficient Low availability of drinkers 0.01
changes were shown without the outlier.   per pig
Presence of scratches 0.06
In the final multivariable model using results of the survey, Low availability of feeders 0.06
no variables were significantly associated with the presence of   per pig
ear necrosis under the 5% significance level. Concrete solid floor Half slatted and wholly slatted 0.07
Low availability of space 0.09
From the survey, the source of semen and genetic composi-   per pig (ft2)
tion of piglets, the breeds of sows and replacement gilts showed Bowl drinker Bowl 1 nipple and nipple 0.12
a wide variety in both case and control farms. Small purebred  drinker
High temperature (°C) 0.15
breeders and a number of multinational genetic supply compa-
nies contributed to supply semen and replacement gilts to both
case and control farms. In addition, there was no difference in lesions may have been too subtle to be recognized when pigs
the types of farm between case and control farms. were chosen for sampling or at the time of the visit there were
no pigs available at the very earliest stage.
Discussion In the current study, the staphylococcal isolates showed a high
The low prevalence of spirochetes found by histological exami- degree of resistance to some of the commonly used antibiotics,
nation and the lack of spirochetes identified by culture in the suggesting that bacterial resistance might lead to poor response
current study is similar to the findings of Richardson et al (3), to antibiotic treatment.
who also observed spirochetes in only a small number of affected The low prevalence of vascular lesions in biopsies from the
animals. It is possible that spirochetes were present but we were study suggests that ear necrosis does not represent a manifesta-
not able to culture them. However, if spirochetes were the pri- tion of PCVAD (11); the vascular lesions appear to have devel-
mary agent, one would expect their presence to be more promi- oped secondarily to epidermal inflammation. In addition, the
nent in histological examination using silver staining techniques. case farms were not associated with other clinical signs such as
The evidence from this study suggests that these organisms are depression, respiratory disease, or enteric disease that could be
more likely secondary invaders rather than primary pathogens. indicative of infections with PCV2 or other systemic diseases.
In contrast, both S. aureus and S. hyicus were frequently iso- As well, the advent of widespread PCV2 vaccination and sig-
lated from samples of the ear lesions. However these organisms nificant reduction in PCVAD has not eliminated or reduced
can be commonly isolated from the skin of pigs. In order to the occurrence of ear necrosis in the case herds. The results are
determine whether these organisms play a role in the etiology consistent with the study by Lang et al (16) who investigated
of ear necrosis it will be necessary to confirm that these isolates the role of PCV2 and couldn’t detect virus in the lesions when
can produce exfoliative toxins (ETs) and to conduct challenge using PCV2 in-situ hybridization testing. Mycotoxins were not
studies to reproduce the disease. Histological examination investigated but the histological description of the lesions and
showed lesions similar to the lesions of exudative epidermitis the lack of other clinical signs associated with mycotoxicosis
such as severe epidermal inflammation with erosion, ulceration, tend to rule out their involvement.
and crust with relatively mild dermal inflammation through all Ear biting was strongly associated with the presence of ear
stages of the disease (15). Our attempt to find early changes of necrosis in the study. Trauma from ear biting has been suggested
gross vesiculation (3) was unsuccessful; possibly, the very early to be the triggering factor in allowing infectious agents to invade

494 CVJ / VOL 54 / MAY 2013


Table 4.  Herd level factors associated with ear necrosis in the sary to investigate the isolates from cases of ear necrosis and
final multivariable logistic regression model based on observational determine the presence of exfoliative toxins. Ear necrosis is
data (P , 0.05)
in all likelihood a disease that requires multiple contributing
Variable OR OR (95% CI) P-valuea factors. A study involving large numbers of case and control
Presence of ear biting 22.34 1.09–459.49 0.04 farms is required to thoroughly investigate management and
High humidity level (versus low) 52.63 2.81–1000 0.01 environmental factors but in this small study high humidity,
Number of observations: 24 early weaning, and the presence of ear biting appeared to be
AUCb: 0.90

A R T I C LE
AICc: 22.61 BICd: 26.14 associated with the condition.
OR — odds ratio.
a Wald test was used to determine statistical differences.
b AUC — area under the ROC (receiver operating characteristic) curve.
Acknowledgments
c AIC — Akaike’s Information Criteria. The research was funded by Ontario Pork, the Animal Health
d BIC — Bayesian Information Criteria.
Strategic Investment Fund, Ontario Ministry of Agriculture,
Pearson X 2 goodness-of-fit test, P , 0.001.
Food and Rural Affairs, and the University of Guelph. We are
very appreciative of the farmers who participated and Bryan
the skin and cause necrosis (17) rather than being the serious Bloomfield for technical assistance. CVJ
sequela of ear necrosis. However, bloody ear lesions are likely
to attract penmates whose chewing could result in the severity
of the lesions (18). Therefore, further research on whether ear
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