Veterinary Dermatology 2004, 15, 315 320

A herd level analysis of a Corynebacterium pseudotuberculosis

outbreak in a dairy cattle herd

Blackwell Publishing, Ltd.

ISRAEL YERUHAM*, SAMUEL FRIEDMAN, SAMUEL PERL, DANIEL ELAD,

YAIR BERKOVICH and YORAM KALGARD
*Hachaklait Gedera and the Koret School of Veterinary Medicine, the Hebrew University of Jerusalem,
PO Box 12, Rehovot 76100, Israel
National Service for Udder Health Caesarea, and the Koret School of Veterinary Medicine, The Hebrew
University of Jerusalem, PO Box 12, Rehovot 76100, Israel
The Kimron Veterinary Institute, Bet Dagan 50250, Israel and the Koret School of Veterinary Medicine, the
Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel
Hachaklait, KiryatAta 28201, Israel
Kibbutz Harduf 17930, Israel
(Received 27 August 2003; accepted 9 October 2003)

Abstract Corynebacterium pseudotuberculosis infection in an Israeli dairy cattle herd is described. The disease
was characterized by ulcerative granulomatous lesions, which occurred in an epidemic form. Thirty-two cows and
two heifers were affected, the ratio of the number affected to number at risk being 17.5 : 1 and 9.5 : 1, respectively.
The culling rate was 50% of the affected animals. Most of the affected animals were cows (91.2%), with one firstcalving cow (2.9%) and two heifers (5.9%) also affected. The infection occurred during the summer to autumn
months (AugustDecember), and lasted 118 days. The incubation period is about 2 months. The disease appeared
in two clinical forms cutaneous and mastitic or as a mixed form. C. pseudotuberculosis organisms that were
isolated from the ulcerative granulomatous lesions and from milk samples failed to reduce nitrate. A decrease in
milk production (4%) and an increase in the bulk-milk somatic cell count from a herd mean of 240 103 mL1
to 460 103 mL1 were noted during the morbidity period. The organism was isolated from milk samples of eight
animals (25%). Clinical, epizootiological and microbiological aspects of the infection are described.
Keywords: Corynebacterium pseudotuberculosis, dairy cattle, ulcerative granulomatous lesions.

I N TRO D U CT ION
Corynebacterium pseudotuberculosis is a Gram-positive,
pleomorphic, intracellular, nonmotile, facultative anaerobic
rod that grows well on blood agar, forming small, whitish,
opaque colonies. C. pseudotuberculosis has three major
characteristics that have been implicated in the expression of its pathogenicity and virulence: the high lipid
content in its cell wall; production of phospholipase D
exotoxin; and its intracellular ability to persist in macrophages.17 The protective nature of the cell capsule
enables the bacterium to persist in the environment for
extended periods under favourable conditions: damp,
shady areas and low temperatures.810 Two biotypes
of C. pseudotuberculosis have been reported: a nitratenegative form, most frequently isolated from sheep and
goats, and a nitrate-positive form that infects cattle and
horses.11 Other authors have reported that both types
may be isolated from cattle.1215 The source of natural
infection and the means of entry into the host are
not well documented for cattle, but the possible role of
arthropod vectors in transmission of the bacterium has

Correspondence: I. Yeruham, 4 Hagoren St., Gedera 70700, Israel.

Fax: +97288699083; E-mail: chkl1357@netivision.net.il
2004 European Society of Veterinary Dermatology

been studied.1620 Several clinical forms of the disease

have been described in cattle: pyogranulomatous
reactions, abscess formation, ulcerative lymphangitis
and mastitic and visceral forms.13,14,2124 Recently, an
additional form has been described: necrotic and
ulcerative dermatitis on the heel of the foot accompanied
by oedematous swelling and lameness.15 The present
paper describes the clinical and epidemiological aspects
of a C. pseudotuberculosis outbreak in an Israeli dairy
cattle herd and its economic importance.

M AT E R IA L S A N D M E T H O D S
Animals and management
Field observations were carried out in a dairy cattle
herd comprising 183 Israeli-Holstein dairy cows. The
herd also included female calves and heifers of various
ages. The cows were kept in a loose housing system in
large, completely covered open sheds. The lactating cows
were divided into two groups: first-lactation cows, and the
remainder. Dry cows and heifers were kept in separate
sheds. Thirty-eight pregnant heifers were introduced to
the herd 2 months prior to the disease outbreak, and
attached to the same age group. All clinical, reproduction,
milk production and management data were recorded
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I. Yeruham et al.

on computer by the herd manager and the attending

veterinarian, who visited the herd twice a week.

Clinical, bacteriological and histological

examinations
All the clinical cases were recorded. The location, size
and appearance of any skin lesions were marked and
recorded regularly. During the disease period milk from
all the affected lactating cows was examined bacteriologically. Milk samples were taken by standard aseptic
techniques,25 refrigerated and processed the next day.
Once every month milk from individual cows and from
the bulk tanks was sampled and analysed for somatic
cell count by the Central Laboratory for Milk Recording of the Israeli Dairy Cattle Breeders Association. A
composite milk sample from all the lactating cows was
obtained at least annually and submitted for bacteriological examination. Confirmation of the clinical diagnosis of C. pseudotuberculosis infection was obtained
by culturing the aspirate content from the ulcerative
granulomatous lesions the content was thick, creamywhite and viscous. Samples were inoculated onto 5%
sheep-blood agar, nutrient agar and MacConkeys agar
(Difco Laboratories, Detroit, MI, USA) and incubated at
37 C. The colonies suspected to be C. pseudotuberculosis
were finally identified by the API-Coryne system (APIBioMerieux, La Balme les Grottes, France). Susceptibility tests of the isolated bacteria were also performed
using a standard method.26 Skin biopsies for histopathological examination were taken with a skin punch from
the lesions of five affected cows. They were fixed in 10%
neutral buffered formalin, embedded in paraffin wax,
sectioned at 56 m and stained with haematoxylin
and eosin.
The affected animals were isolated, showering was
prevented, and the skin lesions were locally treated with
Katran (phenol compounds) (Euro Farm, Stuttgart,
Germany).

R ESU LTS

Figure 1. Distribution of age groups in the herd affected with

C. pseudotuberculosis infection.

Figure 2. A cow with bleeding ulcerative-granulomatous lesion on

the forehead (a), neck (b), shoulder (c), tail base (d), and on the
hip (e), caused by C. pseudotuberculosis infection.

Clinical, epidemiological, bacteriological and

histological studies
The outbreak of C. pseudotuberculosis infection lasted
from 15 August to 10 December 2002. During the
study period ulcerative granulomatous lesions were
diagnosed in the following age groups: two heifers aged
1420 months (9.5% of the age-specific group), one
first-calving cow (2.4% of the age-specific group), six
second calving cows (13.3% of the age-specific group)
and 25 cows at third or more calving (31.2% of the
adult cows) (Fig. 1). The culling rate reached 50% of
the affected animals. The clinical signs included skin
lesions in the form of single or multiple ulcerative granulomatous lesions on the forehead, neck, shoulder, tail
base and hip (Fig. 2).
The cutaneous form of the disease appeared in all
the affected cattle, and the mastitic form in four cows
(12.5%); the organism was isolated from the milk of three

Figure 3. Granulomatous lesion with formation of giant cells (H&E,

100).

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Analysis of a Corynebacterium pseudotuberculosis outbreak

additional cows with skin lesions only (9.3%), and from
one first-calver with no apparent lesions (3.1%).
The regional lymph nodes were involved in all cases,
but generalized lymphadenitis and lymphangitis were
not observed.
Typically, the ulcerative granulomatous lesions reached
a diameter of 1520 cm; they usually exhibited a fibrous
tissue capsule in the subcutaneous tissues and were
fastened to the skin. Palpation of the lesions revealed
them to be doughy and they were oedematous and
painful. Some lesions had raised necrotic margins
and secreted either serosanguinous exudates or a bloodstained yellowish pus.
The lesions did not appear to cause systemic illness
in the affected cows. The infection occurred mostly
during the dry season, from August to December.
A definitive diagnosis was based on bacteriological
and histological examination. After 24 h of incubation,
nonhaemolytic, pinpoint-sized colonies appeared on
the blood and nutrient agar. After a further 24 h, the
colonies reached a diameter of about 1 mm, appeared
opalescent white and were surrounded by a narrow
zone of haemolysis. There was no growth on McConkeys
agar plates. The colonies consisted of Gram-positive
coryneform micro-organisms, indentified as C. pseudotuberculosis by means of the API-Coryne system (APIBioMerieux). C. pseudotuberculosis was isolated from
14 lesions. C. pseudotuberculosis organisms that were
isolated from milk samples were found not to be nitrate
reducers.
Histological examination of the lesion biopsies showed
a granulomatous reaction. There were numerous focal
neutrophilic infiltrations surrounded by epitheloid and
multinuclear giant cells in the subcutis (Fig. 3). Isolation
of the affected animals, local treatment with antiseptics
and fly control appeared to prevent the disease from
spreading to other animals in the herd.
The economic losses were attributed to high culling
rates (50% of the affected animals), to a decrease in average
monthly milk production of the whole herd by 4%
compared with the previous year, and to an increase in
the bulk-milk somatic cell count from a herd mean of
240 103 mL1 to a mean of 460 103 mL1 during the
morbidity period. The average somatic cell count of the
affected milking cows was 2600 103 mL1 (SE 431).
Haemograms of the affected animals revealed mild
to severe leukocytosis with left shift.

D ISCU SSION
Corynebacterium pseudotuberculosis infection is one of
the most commonly diagnosed infectious diseases in
cattle in Israel.1315,23,24 In the present case, the disease
occurred in two clinical forms: cutaneous and mastitic.
The visceral form reported in a previous paper13 was
not observed in the present study.
The inflammatory process and local oedematous
swelling around the lesions are attributed partly to the
organisms, putative virulence factors, but mainly to

317

the direct effect of phospholipase D exotoxin in the

surrounding blood vessels and lymphatics.7,20
Corynebacterium pseudotuberculosis infection probably spreads among Israeli dairy cattle herds through
the introduction of infected animals into an infectionfree herd, as possibly occurred in the present case,
and spreads within the herd through the movement
of infected animals from one barn to another or
via mechanical transmission by houseflies18,19 or other
Diptera.20 Sheep flocks and goats herds grazing in the
neighbourhood to this dairy cattle herd may also have
served as a source of the infection. The time span
between the introduction of the new heifers and the
occurrence of the disease matches the incubation
period of the disease in cattle, namely 2 months, which
is shorter than the incubation period reported in sheep.27
Movement of the disease between cattle groups was
118 days. The fact that the outbreak occurred mainly
during the summer to autumn months (August to
December) may be related to the large population of
houseflies and other Diptera, which play an important
role in harbouring and disseminating C. pseudotuberculosis in dairy herds in Israel.19,20
An additional predisposing factor is wet skin,28
which results from the Israeli practice of showering lactating cattle in the waiting yard three to five times daily
during the summer months, to cool them and to reduce
their heat stress. The resulting excessive wetting of the
coat may have damaged the epidermis and sebaceous
film.29 Moreover, under these conditions, the disease
may have been transmitted directly.
The potential of C. pseudotuberculosis to survive
outside the host, and the close contact between animals when they gather near the water trough and in the
waiting yard, are considered to be the most important
factors in the spread of this organism. C. pseudotuberculosis has been shown to survive for prolonged periods in a contaminated environment under favourable
conditions.8 The eradication of endemic C. pseudotuberculosis infection is near impossible because of the
longevity of the organism on infected premises,8,9 despite
its sensitivity to ultraviolet light and therefore to direct
sunlight.
The potential for environmental contamination from
a single ulcerative-granulomatous lesion is very high,
and the ability of the organism to survive in soil and on
fomites ensures its continuing presence.8,10 Infected
milk dripping from a dairy cow may also contaminate
the environment and infect other cows in the herd.
As a result of the primary infection in the animal, the
bacteria may become disseminated.30 It appears that
geographical and climatic conditions, seasonally
fluctuating incidence, a contaminated environment,
age and possibly also breed of the affected animals, are
potential risk factors for the epidemic occurrence of
the disease, and they may also have an important role
in its epizootiology.
The cutaneous form of the disease occurred at various sites, usually subcutaneous or within lymph nodes;
the mastitic form is apparently less common.13 It seems

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I. Yeruham et al.

that the severe cases tend to involve mixed forms, either

cutaneous and visceral, or cutaneous and mastitic.13 In
the present study the visceral form of the disease was
not detected.
Presumptive diagnosis of C. pseudotuberculosis infection can be made by consideration of the ulcerative
dermatitis. A definitive diagnosis of C. pseudotuberculosis infection is based on isolation of the organism
from the skin lesions, and on histological examination
of skin biopsies. Due to our previous experience only
local treatment was applied, and it appeared to be
effective.
The development of a pyogranuloma is associated
with limited bacterial dissemination, as described by
Pepin et al.,30 whose results illustrate the dual role of
granulomas in chronic bacterial disease.31 On the one
hand, an infectious granuloma can be considered as a
mechanism of defence, which limits bacterial dissemination to critical sites and stimulates the development
of an effective immune reaction.32,33 On the other hand,
it can be considered as the expression of an immunopathological process, because of the tissue damage
and excessive fibrosis associated with the persistence of
viable bacteria.34 All the strains of C. pseudotuberculosis
that were isolated from the ulcerative granulomatous
lesions and from all milk samples failed to reduce
nitrate, and this failure is characteristic of the ovine
and caprine strains;11,12 earlier reports have made
similar observations.13,23
The disease can also spread via infected milk, and it
forms a public health hazard when unpasteurized milk
or milk products are consumed by humans.35 Human
infection may also occur as result of continued close contact with infected animals. The distribution patterns
of ulcerative granulomatous lesions suggest a relationship between the age of the animals and prevalence of
the disease; young cattle appeared to be less susceptible
to the ulcerative granulomatous form than older cows.
Although lymphadenitis has been diagnosed serologically in sheep,10,36 to the best of the authors knowledge no such method has been developed for cattle.
Serodiagnosis, however, would be very useful in certifying herds as free from C. pseudotuberculosis. Epidemic
C. pseudotuberculosis infection in cattle is a severe
condition, with significant economic consequences, as
pointed out in the present and in previous reports.13,18,24
The drop in milk production and the substantial rise in
the herd average of SCC were caused by loss of milk
yield and dramatic rise in SCC of the infected cows.
All forms of the infection severely affect the animals
health and milk production, and a better understanding of
the epizootiology and of the clinical aspects of the disease
should be applied to preventive management schemes.

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Rsum Cet article dcrit une infection par Corynebacterium pseudotuberculosis dans un troupeau laitier en
Isral. La maladie tait caractrise par des lsions granulomateuses et ulcratives, qui sont apparues de faon
pidmique. Trente-deux vaches et deux gnisses ont t atteintes avec un ration animaux malades/animaux risque de 17.5:1 et 9.5:1 respectivement. La plupart des animaux affects taient des multipares (91.2%); une primipare (2.9%) et deux gnisses (5.9%). La morbidit est apparue pendant les mois dt/automne (aot-dcembre),
et lpisode a dur 118 jours. La priode dincubation est denviron 2 mois. La maladie est apparue sous deux
formes cliniques: cutane et mammaire ou mixte. Les C. pseudotuberculosis isols des lsions granulomateuses
ulcres et des chantillons de lait ne rduisaient pas les nitrates. Une diminution de la production de lait (4%)
et une augmentation des comptages cellulaires dans le lait dune moyenne de 240 103/ml une moyenne de 460
103/ml ont t notes pendant lpisode. Les microorganismes ont t retrouvs dans le lait pour huit animaux
(25%). Les aspects cliniques, pizootiques et microbiologiques de cette infections sont dcrits.
Resumen Se describe la infeccin por Corynebacterium pseudotuberculosis en un rebao de vacas de leche de
Israel. La enfermedad se caracterizaba por unas lesiones granulomatosas ulcerativas que se producan de forma
epidmica. Se afectaron treinta y dos vacas y dos novillas con un ndice de nmero afectado sobre nmero bajo
riesgo de 17.5:1 y 9.5:1 respectivamente. El ndice de sacrificio fue del 50% de los animales afectados. La mayora
de animales afectados fueron vacas adultas (91.2%); una vaca con un solo parto (2.9%) y dos novillas (5.9%).
La morbilidad se produjo durante los meses de verano-otoo (AgostoDiciembre), y dur 118 das. El perodo
de incubacin es de aproximadamente 2 meses. La enfermedad apareca en dos formas clnicas cutnea y masttica o mixta. Los organismos de C. pseudotuberculosis aislados de las lesiones granulomatosas ulcerativas y
de las muestras de leche no redujeron el nitrato. Durante el periodo de morbilidad se detectaron una disminucin
en la produccin de leche (4%) y un incremento en el recuento de clulas somticas en un rebao, de una mediana
de 240 103/ml a una de 460 103/ml. El organismo fue aislado de muestras de leche de ocho animales (25%).
Se describen los aspectos clnicos, epizootiolgicos y microbiolgicos de la infeccin.
Zusammenfassung Es wird eine Corynebacterium pseudotuberculosis-Infektion bei einer Rinderherde in Israel
beschrieben. Die Erkrankung zeichnete sich durch ulzerativ-granulomatse, epidemisch auftretende Lsionen
aus. Zweiunddreiig Khe und zwei Frsen waren befallen, wobei das Verhltnis der Anzahl der befallenen Tiere
zu der Anzahl der gefhrdeten Tiere 17,5:1 beziehungsweise 9,5:1 war. Die Ttungsrate lag bei den befallenen
Tieren bei 50%. Die befallenen Tiere waren zumeist Khe (91,2%), eine Erstkalbin (2,9%) und zwei Frsen (5,9%).
Die Morbiditt zeigte sich whrend der Sommer-Herbstmonate (August Dezember) und dauerte 118 Tage. Die
Inkubationszeit ist ungefhr 2 Monate. Die Erkrankung trat in 2 klinischen Formen auf Haut-oder Euterform
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I. Yeruham et al.
oder in einer gemischten Form. C. pseudotuberculosis-Organismen konnten von den ulzerativ-granulomatsen
Lsionen und aus Milchproben mit negativen Nitratproben isoliert werden. Whrend des Morbidittszeitraumes
konnte ein Abfall der Milchproduktion (4%) und ein Anstieg der Anzahl der somatischen Zellen in der Milch
von einem Herdendurchschnitt von 240 103/ml zu einem Durchschnitt von 460 103/m festgestellt werden. Die
Organismen wurden aus Milchproben von acht Tieren (25%) isoliert. Klinische, epidemiologische und mikrobiologische Aspekte der Infektion werden beschrieben.

2004 European Society of Veterinary Dermatology, Veterinary Dermatology, 15, 315 320