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The Veterinary Journal 171 (2006) 566–569

TheVeterinary Journal

Short communication

Muco-cutaneous candidiasis in two pigs with postweaningmultisystemic wasting syndrome

Priscila Zlotowski a, Daniela B. Rozza a, Caroline A. Pescador a, David E. Barcellos b,Laerte Ferreiro c, Edna M.C. Sanches c, David Driemeier a,*

a Laboratory of Veterinary Pathology, College of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS),

Av. Bento Goncalves 9090, 91540-000 Porto Alegre, RS, Brazilb Department of Swine Medicine, College of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS),

Av. Bento Goncalves 9090, 91540-000 Porto Alegre, RS, Brazilc Laboratory of Veterinary Mycology, College of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS),

Av. Bento Goncalves 9090, 91540-000 Porto Alegre, RS, Brazil

Accepted 6 December 2004

Abstract

In two distinct commercial swine herds, poor weight gain and an increased number of animals showing wasting were observed

among nursery and growing pigs. Cases of postweaning multisystemic wasting syndrome (PMWS) and infection with Haemophilus

parasuis had been previously diagnosed in these herds. One growing wasted pig from each herd was necropsied and showed enlarged

lymph nodes. Pseudomembranous material adhered to the dorsum of the tongue, soft and hard palate in case 1, and in case 2, fibr-

inous material was seen as whitish plaques on the oesophageal surface with hyperkeratosis of the non-glandular stomach.

The main histological lesions in both cases were found in lymphoid tissues with a multifocal accentuated lymphohistiocytic infil-

trate, areas of lymphoid depletion and intracytoplasmic inclusions in histiocytic cells in lymph nodes and Payer�s patches. Focally,

extensive ulceration was found in the stratified pavement epithelium of the tongue with necrosis and necrosuppurative infiltrate in

case 1; in case 2, there was ulceration in the stomach with lymphohistiocytic infiltrate in the submucosa and ulceration in the mucosa

of the oesophagus associated with yeast cells and pseudo-hyphae. Candida albicans was isolated from the oral cavity lesions. Immu-

nohistochemistry of the lymph nodes was positive for porcine circovirus 2 (PCV2). The association between PMWS and mucocu-

taneous candidiasis reported here supports the potential immunosuppressive state of PMWS infected pigs.

� 2004 Elsevier Ltd. All rights reserved.

Keywords: Swine; PMWS; Immunosuppression; Mucocutaneous candidiasis

Postweaning multisystemic wasting syndrome

(PMWS) was first recognized in 1996 in Canada as

a new emerging disease causing wasting in post-weaning pigs. Since then, PMWS has been described

in pigs in Asia, North and South America and Europe

(Chae, 2004). The causative agent is porcine circovirus

2 (PCV2), a small non-enveloped DNA virus contain-

1090-0233/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.tvjl.2004.12.010

* Corresponding author. Tel.: +555133166107; fax: +555133166116.

E-mail address: davetpat@ufrgs.br (D. Driemeier).

ing a unique single-strand circular genome (Ellis and

Allan, 2000). Many studies have indicated that dis-

eases or syndromes associated with PCV2 affect pigherds worldwide (Ellis and Allan, 2000) and the most

frequent clinical signs are wasting or a failure to

thrive, enlarged lymph nodes, dyspnoea, pallor, jaun-

dice and diarrhoea (Harding, 2004). Enlargement of

lymph nodes (mainly inguinal, mesenteric and medias-

tinal) is the main macroscopic finding at necropsy.

Other gross lesions have included non-collapsed,

tan–mottled lungs, kidneys with multiple pale foci of

Fig. 1. Case 2: oesophagus. Fibrinous material longitudinally corru-

gated in the mucosal surface.

P. Zlotowski et al. / The Veterinary Journal 171 (2006) 566–569 567

variable diameter, reduction or increase in liver size,

with orange yellow discolorations (Segales et al.,

2004). The principal microscopic lesions are found in

lymphoid tissues and include a variable degree of lym-

phocytic depletion with loss of follicular architecture

combined with a multifocal to diffuse, slight to veryintense lymphohistiocytic multinucleated giant cell

infiltration (Chianini et al., 2003; Segales et al., 2004).

It has been suggested that PMWS may be related to

immunosuppression in pigs (Segales et al., 2001). Studies

performed in conventional pigs affected with PMWS

have described a decrease in circulating B-cells, loss of

lymphocytes in B-cells areas, and decreases in CD4+

and/or CD8+ T lymphocytes (Segales et al., 2001).The lack of response to antibiotic therapy, the existence

of a litter effect and the occurrence of other unusual dis-

ease syndromes or serious infections with ordinarily

non-pathogenic secondary organisms may reflect the

immunosuppressive features of PMWS (Segales and

Clark, 2002). This hypothesis is supported by typical

microscopic lymphoid damage in PMWS affected tissues

and the association of the disease with opportunisticpathogens commonly associated with immunosuppres-

sion, such as Aspergillus spp. (Segales et al., 2003), Chla-

mydia spp. (Carrasco et al., 2000), Pneumocystis carinii

(Clark, 1997) and Cryptosporidium parvum (Nunez et al.,

2003).

We describe here two cases of mucocutaneous candi-

diasis in PMWS affected pigs. The cases occurred in two

distinct industrial farms in the state of Rio Grande doSul, Brazil. The symptoms and clinical history were sim-

ilar, namely poor weight gain and increased wasting in

nursery and growing pigs. Cases of PMWS and infection

with Haemophilus parasuis and Pasteurella multocida

type D had been previously diagnosed in these herds.

Because of the bacterial infection the animals received

therapeutic medication with 200 ppm amoxicillin in the

food for 15 days. One growing pig from each herd, withpoor body condition was euthanased for diagnostic

purpose.

Necropsy was performed just after euthanasia and

several tissues were collected, fixed in 10% neutral buf-

fered formalin solution, sectioned at 5 lm thick and

stained with haematoxylin/eosin for histopathological

examination. To look for yeast cells and pseudohyphae,

histological slides of the tongue (case 1), oesophagusand stomach (case 2) were stained with Grocott and

PAS (periodic acid Schiff). Fragments of nasal turbin-

ates and tongue (case 1) were collected for bacteriologi-

cal and mycological culture, respectively. Samples

collected from the tongue were cultivated on Sabou-

raud�s dextrose agar with 0.5 g/L chloramphenicol at

37 �C for five days. For species identification we used fil-

amentation in equine serum and production of chlamy-dospores in corn meal agar (Sidrim and Moreira, 1999).

Bacteriological examination was by routine culture of

the material collected from the lesions (blood agar and

MacConkey agar), incubated at 37 �C aerobically and

anaerobically with evaluation at 24 and 48 h.

Immunohistochemical procedures were performed on

formalin fixed, paraffin-embedded sections of lymph

nodes which were digested in 0.005 g/10 mL proteaseXIV for 15 min at 37 �C. Polyclonal rabbit antibody

to PCV2 (Sorden et al., 1999) at 1/1000 dilution was

incubated for 1 h and then stained by the streptavidin-

biotin immunoperoxidase technique using diam-

inobenzidine as chromogen.

The main gross findings in both animals were enlarge-

ment of mesenteric and inguinal lymph nodes, and con-

solidation of the apical and middle lobes of the lungs.Cyanosis of the ears was noted as was a white pseudo-

membrane adhering to the dorsum of the tongue, soft

and hard palate and accentuated atrophy of the nasal

turbinates (case 1). Fibrinous material arranged as whit-

ish plaques on the oesophagus surface (Fig. 1) and

marked hyperkeratosis of the non-glandular mucosa of

the stomach were also noted (case 2).

Microscopically, in both cases, lymphoid tissuesshowed multifocal accentuated lymphohistiocytic infil-

trates with areas of moderate lymphoid depletion and

sharply, demarcated spherical, intracytoplasmic inclu-

sions in histiocytic cells in lymph nodes and Payer�spatches. In the lungs, hyperplasia of the lymphoid tissue

around the bronchi and bronchioles with mononuclear

and polymorphonuclear cells inside, and thickening of

the alveolar septa were also present. Mild lymphohistio-cytic inflammatory infiltration was found in the portal

zones of the liver and submucosal multifocal lymphoh-

istiocytic inflammatory infiltrates were in the colon.

In the stratified pavement epithelium of the tongue,

focally extensive ulceration, necrosis and necrosuppura-

tive infiltrate associated with yeast cells and pseudo-

hyphae could be observed. In the nasal turbinates atro-

phia of the spongiform bone with lymphohistiocytic

Fig. 3. Lymph node. PCV2 antigen-positive cells containing intracy-

toplasmic granules consistent with inclusion bodies. Immunohisto-

chemistry, 40·.

568 P. Zlotowski et al. / The Veterinary Journal 171 (2006) 566–569

infiltrate in the lamina propria was noted. The ear had

purulent dermatitis in association with large amounts

of bacteria (case 1). The stomach showed focally exten-

sive ulceration, hydropic degeneration of the cells on the

non-glandular epithelium with lymphohistiocytic infil-

trate in the submucosa. Focally extensive ulcerationwas also seen in the mucosa of the oesophagus. These

lesions were associated with yeast cells and pseudo-

hyphae (case 2) (Fig. 2). Yeasts of Candida albicans were

isolated from lesions in the oral cavity. P. multocida type

D was isolated from fragments of the nasal cornet (case

1). Immunohistochemical examination of both cases

revealed a moderate number of stained histiocytic cells

in the lymph nodes (Fig. 3).Candida albicans occurs in small numbers on the skin

and in the oral cavity, stomach and intestines of normal

pigs. However, when immune defences are compromised

it appears to colonise debilitated skin surfaces and le-

sions on other mucous surfaces. Using broader spectrum

antimicrobials for a long period of time could predis-

pose the growth of this yeast (Taylor, 1999) by inhibit-

ing the competitive microflora leading to invasion ofmucous surfaces and penetration of pseudohyphae of

the superficial layers of the epithelium (Chandler et al.,

1980). Chronic gastroenteritis, gastric ulceration and

cutaneous and oropharyngeal infections can occur in

piglets of 7–14 days of age (Taylor, 1999). Lymphocyte

cell-mediated immunity (CMI) is an important host de-

fence against fungi and is probably the principal protec-

tion at the mucosal and epidermal surface (Forsyth andMathews, 2002). During the induction of CMI, C. albi-

cans antigens are presented to T cells and stimulate their

proliferation with the synthesis of cytokines, which en-

hance the candidacidal functions of the phagocytic cells

(Newman and Holly, 2001). A decrease in circulating B-

cells, loss of lymphocytes in B-cell areas, and a decrease

in CD4+ and/or CD8+ T lymphocytes as observed in

Fig. 2. Case 2: oesophagus. Necrosis and necrosuppurative infiltrate

associated with yeast cells and pseudo-hyphae. PAS, obj. 40·.

PCV2 infected animals (Segales et al., 2001) could facil-itate infection with C. albicans because of the participa-

tion of these cells in the host defences against this yeast.

The lesions in the lymphoid tissues and lungs, ob-

served in this study were similar to those previously

reported in PMWS affected pigs (Chae, 2004; Segales

et al., 2004). Clinical signs, macroscopic and micro-

scopic findings and the presence of PCV2 in histiocytic

cells support the diagnosis of PMWS due to PCV2infection. The presence of oral, oesophageal and gastric

lesions associated with yeasts and pseudo-hyphae in

these lesions in growing pigs suggest a failure in the

immune response of the hosts. With the worldwide

spread of PMWS, opportunistic agents as C. albicans

may be increasing in swine herds. This is the first known

report describing the association between C. albicans

and PMWS.

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