Clinical aspects of an outbreak of papillomatous digital dermatitis in a dairy cattle herd

INTRODUCTION Papillomatous digital dermatitis (PDD) is an infectious and contagious disease of the skin of bovine digits, and during the past 20 years it has become an important cause of lameness in dairy cattle worldwide. The economic importance of papillomatous digital dermatitis is attributable to decreased milk yield, weight loss, impaired reproductive performance, increased numbers of culled cattle, and costs of treatment and control. Little is known about the cause and epidemiology of the disease. It is believed to be a multifactorial disease in which infectious agents are primarily involved. Some reports have focused on the role played by spirochaete organisms of the genus Treponema associated with PDD; these appear to be among the predominant organisms found invading the stratum spinosum and dermal papillae. A number of bacteria have been isolated from PDD lesions but none has been shown with certainty to play a role in the pathogenesis of the lesion. There is no evidence of viral involvement. The use of footh baths containing solutions of formaldehyde, copper sulphate or zinc sulphate is the most common treatment for cattle with PDD. PDD is responsive to either parenteral or topical antibiotic therapy, suggesting a bacterial role in the disease process. The present report concerns an infectious, acute and rapidly progressive outbreak of bovine papillomatous digital dermatitis in a dairy cattle herd in Israel.

The economic importance of papillomatous digital dermatitis is attributable to decreased milk yield, weight loss, impaired reproductive performance, increased numbers of culled cattle, and costs of treatment and control 16 .Little is known about the cause and epidemiology of the disease.It is believed to be a multifactorial disease in which infectious agents are primarily involved 4,10,13,14,19 .Some reports have focused on the role played by spirochaete organisms of the genus Treponema associated with PDD; these appear to be among the predominant organisms found invading the stratum spinosum and dermal papillae 4,14,17,[19][20][21] .
A number of bacteria have been isolated from PDD lesions but none has been shown with certainty to play a role in the pathogenesis of the lesion 4,8,13,22 .There is no evidence of viral involvement 15 .The use of footh baths containing solutions of formaldehyde, copper sulphate or zinc sulphate is the most common treatment for cattle with PDD 11,22 .PDD is responsive to either parenteral or topical antibiotic therapy, suggesting a bacterial role in the disease process 14,15 .
The present report concerns an infectious, acute and rapidly progressive outbreak of bovine papillomatous digital dermatitis in a dairy cattle herd in Israel.

CASE HISTORY
The disease was seen in a herd of 60 dairy cows in various stages of lactation.All age categories were affected, from 1st lactation to older cows; 12 (70.6 %) of the 17 affected animals were 2nd lactation and older cows, and only 5 (29.4 %) were 1st-calving cows.The hooves of the herd were routinely trimmed twice a year.
The cows were kept in a loose-housing system under continually wet conditions.The outbreak of PDD occurred in August.Lesions were evaluated in the milking parlour before initiation of treatment and again at 2-week intervals.Closer inspection of the affected limbs was performed after using a medium-pressure water hose, and the feet were cleaned.Gross lesions usually appeared in 3 forms: (1)  early lesions on the plantar aspect were circular and developed proliferative masses with projections on their surfaces (strawberry-like) (Fig. 1); these lesions were near or slightly proximal to the juncture of the bulbs of the heels.(2) Later, the lesion became more extensive, with a verrucose appearance (papillomatous-like), with superficial necrosis (Fig. 2) and a foul odour; the condition appeared to be restricted to the dermis, with no involvement of the subcutaneous tissues.
(3) Lesions in 2 cows developed at the dorsal aspect of the interdigital cleft, with interdigital hyperplasia; no swelling of the coronet was seen.Milk yield was reduced only in the lame cows, an average drop of 5 litres per cow per day (14 % of the daily milk production).
The lameness evaluation was performed by observing the cows individually as they walked at a normal pace in a vacant concrete alley.
Morbidity was high: 17/60 cows clinically examined were seen to be affected on the hind limbs only, 4 on both legs, 9 on the right and 4 on the left.Four cows showed varying degrees of lameness; they shifted weight from one foot to another and appeared uncomfortable when standing in the yards.
No pathogenic bacteria were identified when material scraped from lesion surfaces of 4 cows was stained with Gram's stain and examined microscopically.Aerobic and anaerobic cultures from the biopsies plated on ox-blood agar and on McConkey media also failed to yield pathogenic microorganisms.
Biopsies were taken from 4 affected cows, and parts were fixed in 10 % neutral buffered formalin and processed for histology.The histopathological changes were identical in biopsies taken from lesions of the affected cows: marked epidermal hyperplasia with hyperkeratosis, basal cells with prominent nucleoli, and acanthosis.Superficial epidermal necrosis was present and was associated with purulent inflammation (Figs 3, 4).Silverstaining, using the technique of Warthin-Starry, was performed on the tissue samples.Organisms similar to those described by Read et al. 14 were present deep in the lesion -a large number of filamentous to spiral organisms of the spirochaete group.We found that a 5 % formalin solution combined with 5 % sodium hydroxide in a foot bath (2 m long and 15 cm deep), used twice a week, resulted in a marked improvement of the condition after the 2nd treatment, and offers good control of the disease.Four weeks after the initiation of the treatment programme (a total of 8 treatments), all affected cows had completely recovered.The legs of the cows were washed clean of loose faeces and detritus before they entered the foot bath.The foot bath was cleaned weekly.The entire herd continued to receive the same treatment for 12 weeks.During the follow-up period of 1 year no new cases of digital dermatitis were recorded.
The 4 lame cattle were, in addition to the above treatment, treated parenterally with procaine penicillin (Renyamina, Israel) 22 000 IU/kg and metronidazole (Renyamina, Israel) 50 mg/kg for 3 consecutive days, which resulted in cessation of lameness and regression of lesions.

DISCUSSION
The spirochaete-like organisms associated with the papillomatous digital dermatitis (PDD), which were found deep in the epidermis, in silver-stained tissue sections from 4 affected cows in the described outbreak, may apparently play an important role in the pathogenesis of PDD 2,9,14,15 .
Apart from spirochaete-like organisms other microorganisms that have been suspected to be involved in this condition are Fusobacterium necrophorum, Bacteroides spp. 22and Campylobacter faecalis 4 .The sudden onset and the rapid spread of the disease through the herd, the histological findings, and the response to treatment suggest an infectious aetiological agent.Until Koch's postulates can be fulfilled, the role of spirochaetes remains uncertain.
Bovine papillomatous digital dermatitis histologically resembles the human tropical disease 'yaws', a skin disease of the legs caused by the spirochaete Treponema pertenue (Treponema pallidum subspecies pertenue) 2,4,14,15,16,19 , which is also highly responsive to parenteral antibiotics.Invasiveness of the spirochaete has been demonstrated by a modified Steiner silver impregnation method for paraffin sections 14 .It seems that most reported outbreaks of PDD involve dairy herds of the Friesian and Holstein breeds and their crosses 24 .
Papillomatous digital dermatitis occurs most commonly on the hind limbs.Gross lesions in the reported herd appeared in 3 forms: demarcated red, raw granular areas (strawberry-like); yellow, grey or brown papillary proliferation (papillomatous-like), and interdigital proliferative dermatitis.
Morbidity of PDD in dairy herds in different countries varies widely, from 12 to 80 % 1,3,5,11,16,18 .In the recent outbreak the morbidity rate reached 28.3 %.The extensive outbreak of PDD followed the introduction of purchased heifers into the herd during the previous few months.Dairy herds for which replacement heifers were purchased, were more likely to be affected by PDD through the introduction of infected animals, than so-called 'closed herds' 11,18 .
Based on our cumulative data it appears that PDD prevalence has a seasonal pattern.Morbidity in the described herd and also on other dairy farms in Israel (unpublished data) is high mostly during the summer months (June-October).It seems that the housing of the cattle all year round in barns, in a region with a hot and humid climate, facilitates the spread of the infection through the herd.
Peterse 12 , Raven 13 , Greenough et al. 8 and Rodriguez-Lainz et al. 18 indicated that the predisposing conditions for PDD are a warm and wet environment for housed cattle -conditions that exist in countries with tropical and subtropical climates.There is general agreement that the condition occurs primarily while the cows are housed 1 .It seems that improved management and ventilation and dry bedding may reduce the prevalence of PDD in dairy cattle herds.
Treatment of the condition in the outbreak reported here consisted of cleaning the feet of cows on their way into the milking parlour, with a high-pressure water hose, and a foot bath twice a week in a solution of 5 % formalin and 5 % sodium hydroxide for 12 weeks.We recommend that all animals in the affected herd should be foot-bathed, with the affected cows being kept in the foot bath for at least 15 min, and parenteral treatment of the lame cows with procaine penicillin and metronidazole for 3 consecutive days.The described treatment and control programme proved to be successful in treatment and eradication of this apparently infectious disease from the affected herd.
It is to be hoped that due attention will be paid to such a potentially widespread infectious disease that causes economic losses in dairy cattle herds, and its spread by intensive animal trading, before it becomes endemic in many herds.