Cutaneous Mucinosis in a Strain of Brown–Egg Laying Chickens

Materials and Methods

Chickens

Twenty-six live brown egg–laying chickens aged between 43 and 46 weeks from a flock of 41 000 were submitted for necropsy to the California Animal Health and Food Safety Laboratory System (CAHFS)–San Bernardino branch. The brown egg–laying chicken is a strain of chicken originating from a cross between male Rhode Island Red (RIR) white variety and female RIR brown variety. The birds were humanely euthanized by use of carbon dioxide. The flock had a history of 20% egg production drop over a 10-week period starting at 33 weeks of age (Fig. 1), decreased feed consumption, weight loss, and feather loss on the head, neck, keel, and thigh. Other chickens of the same strain but different ages on the same premises but in different houses were not affected. No other clinical signs were noted in the flock. The birds were raised indoors and housed in cages (7 birds per cage; cage size: 7.31 × 6.09 m), with adequate ventilation and standard vaccination for layers. Feed and water were provided ad libitum. There was no history of pesticide application on the birds or in the house, and no mites or lice were found on the birds submitted for necropsy. For treatment, the birds were supplemented with vitamin A, biotin, and electrolytes, with no improvement.

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Figure 1.

Hen-day egg production in skin mucinosis–affected chickens compared with the expected standard of egg production in age-matched normal brown egg–laying chickens. Note the egg production drop starting at 33 weeks of age in the affected group. The hen production is the number of eggs produced per day/number of birds in the flock that day, expressed as a percentage.

Results

Gross Lesions

Postmortem examination revealed loss of feathers over 60% to 80% of the body and a scaly, dry skin with a slight green tinge and occasional petechiae scattered throughout the body but most prominent on the keel, crop, and anterior stifle. The dermis was mildly thickened (Fig. 2). The skin around the eyes, comb, and wattles was not affected. Most of the birds were out of production, as evidenced by inactive ovaries. No other gross lesions were observed.

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Figures 2–7. Skin; chicken, cutaneous mucinosis. Figure 2. Locally extensive feather loss. Figure 3. Accumulation of granular basophilic material in the dermis with formation of lakes in the superficial dermis. Hematoxylin and eosin (HE). Figure 4. Basophilic granular material within epithelial cells of feather follicles. Note the multifocal infiltration of lymphocytes and plasma cells. HE. Figure 5. Skin; chicken. Alcian blue–positive material, consistent with mucin, forming lakes in the superficial dermis. Alcian blue (pH 2.5). Figure 6. Skin; chicken. Diffuse accumulation of alcianophilic material within the dermis. Low number of lymphocytes and plasma cells infiltrate the perivascular space of small blood vessels. Alcian blue (pH 2.5). Figure 7. Skin; chicken. Periodic acid–Schiff (PAS)–negative reaction of the mucinous material. PAS.

Discussion

The histologic and histochemical results demonstrated unequivocally that a dermal mucinosis similar to that described in dogs might occur in brown egg–laying chickens. To our knowledge, this study represents the first report of this condition in an avian species. It is often difficult to visualize dermal mucin on HE-stained histologic slides, and only in severe cases of mucinosis are collagen bundles dissociated by a granular or wispy basophilic material. ²⁵ In the affected chickens, the alcianophilic reaction confirmed acid GAGs as the main components of the dermal deposits. Interestingly, the combs and wattles, which generally have large amounts of mucin in the dermis, were not affected in the chickens in this study. The reason for this is not known. The positive titers for MG and MS were considered not significant as other chickens on the same premises without skin lesions were also positive for MG and MS. In addition, MG and MS have not been known to cause any skin or feather conditions in chickens.

Although the precise cause of cutaneous mucinosis in these chickens cannot be determined, 2 possible mechanisms could be hypothesized: a primary hereditary mucinosis, in which mucin is the main histologic feature, or a secondary mucinosis due to inflammation.

The predominant occurrence of this condition in the submitted strain of chickens might suggest a genetic basis. Other birds on the premises, raised under similar conditions of management, environment, and diet but from different genetic sources, were not affected. Brown egg–laying chickens are bred under similar management conditions to other strains of chickens, therefore suggesting that management has no influence on the occurrence of cutaneous mucinosis in the brown egg–laying chickens. Furthermore, it is well known that the strain of brown egg layer chickens in this study has a genetic tendency to develop other diseases, such as amyloid arthropathy ¹⁹ and intestinal dilatation syndrome (IDS). ³⁶ However, potential genetic analyses are hindered in our cases by the lack of available tissue samples as well as readily available technology. Further genetic studies are necessary to confirm the genetic basis of skin mucinosis in the brown egg layer–type chickens and to ascertain the alterations responsible for this dysfunction.

Regarding inflammation as a putative trigger of dermal mucinosis, it is well known that cytokines may play an important role in the induction of GAG synthesis, specifically tumor necrosis factor α and β, interleukin (IL)–1, transforming growth factor (TGF) β, IL-6, and epidermal growth factor. ^4,5,20,22 Inflammatory cytokines released by lymphocytes, plasma cells, and heterophils in the submitted birds may be responsible for stimulating mucin production from dermal fibroblasts, producing a secondary dermal mucinosis. It is interesting that skin from 2 dermatitis-affected brown egg–laying chickens with mild to moderate accumulation of mucin confirms the association between inflammation and mucin production. Skin samples of the affected chickens in this study had similar mast cell density to the control skin, ruling out the pathophysiologic role of mast cells in the development of mucinosis, as demonstrated in humans. ^14,26

Interestingly, in the submitted birds, the severe and diffuse dermal mucinosis was associated with a moderate multifocal follicular mucinosis. Follicular mucinosis is an epithelial mucinosis, in which mucin infiltrates the outer root sheath of the follicles and sebaceous glands. ³⁴ Occasionally, the mucin leaks back into the dermis. ² Usually, this condition is associated with cutaneous epitheliotropic lymphoma, ^31,35 or otherwise a lymphocytic infiltrate is constantly present around the affected follicles and in the surrounding dermis. ⁸ Reed ²⁴ has speculated that T lymphocytes stimulate follicular keratinocytes to produce mucin. In the submitted chickens, a lymphocytic inflammatory infiltrate was noted around the affected epithelium. Based on this finding, we propose that the feather loss was due to a primary dermatitis with secondary dermal and follicular mucinosis.

One differential diagnosis for dermal mucin accumulation includes mucopolysaccharidoses, which are characterized by accumulation of glycosaminoglycans, such as dermatan and heparan sulfate, but these substances have different staining characteristics from hyaluronic acid. ²³

In conclusion, we have described a distinctive histopathologic form of dermal mucinosis in brown egg–laying type chickens. As further cases are reported, a clearer picture of cutaneous mucinosis in avian species may emerge. A dermal mucinosis by itself is only a consequence of an altered metabolism or catabolism of dermal GAGs, whatever its cause. Further studies are needed to elucidate the origin and pathogenesis of this unique dermatosis in birds.