Introduction

Pneumonia and other respiratory tract infections are of a common occurrence with a serious economic impact in the sheep industry. Pneumonic diseases are well known to be responsible for enormous capital losses due to substantial mortality in acute outbreaks, reduced growth in chronic infections and significant financial losses in drug costs and condemnations in abattoirs (Goodwin et al. 2005; Daniel et al. 2006). Authentic information on the prevalence of ovine pneumonia in the Al-Qassim region in the central parts of the Saudi Kingdom is currently lacking despite the presence a remarkably dense population of sheep flock in this area. However, circumstantial evidence of a wide prevalence of ovine pneumonia in the region is reflected by the large numbers of sick animals that are daily brought for treatment at the University Teaching Hospital and the official records of ovine lung condemnations at the local abattoir. A 6-month abattoir survey was conducted on ovine pneumonia a few years ago (Al-Sadrani 2010), and the results demonstrated the occurrence of various types of pneumonia in indigenous breeds of sheep slaughtered at the local abattoir. However, more detailed microscopic examination of the pneumonic lungs incidentally revealed the coexistence of some important pathological alterations indicative of certain specific pulmonary diseases that have not been previously recognized in the region. These finding are briefly described and discussed in the present communication.

Materials and methods

The materials of this report comprise 140 pneumonic ovine lung samples partially or totally condemned at the local abattoir of Buraydah City, Al Qassim Area, Kingdom of Saudi Arabia. The total number of lungs examined during the present study was 1425. The slaughtered sheep were local breeds, mostly male animals of an approximate average age of 2 years. The pneumonic lung samples were initially examined for visibly detectable gross lesions. A small portion of each lung showing pneumonic lesions was then fixed in 10 % buffered formalin solution for histopathological investigation. Tissue processing, sectioning and staining with haematoxylin and eosin (H&E) were carried out by routine procedures (Bancroft and Gamble 2007).

Results and discussion

Detailed microscopic examination of the pneumonic lung samples collected during the previously mentioned abattoir survey revealed the coexistence of certain significant pathological alterations indicative of the following diseases (Table 1):

Table 1 Incidental findings in pneumonic lungs of sheep slaughtered at the local abattoir
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  1. i

    Sheep pulmonary adenomatosis (SPA):

    Histopathological alterations indicative of sheep pulmonary adenomatosis (Jaagziekte) were detected in 8.6 % of the pneumonic lung samples (n = 12). Affected lungs revealed neoplastic proliferation of the alveolar epithelium forming numerous folds and papillary projections on the alveolar wall (Fig. 1). Most of alveoli were lined by cuboidal or short columnar cells and contained large numbers of foamy macrophages and mononuclear cells. These alterations were consistently reported as the most salient histopathological findings of the disease (Ali and Abdelsalam 1999; Cutlip and Young 1982; De las Heras et al. 2003).

    Fig. 1
    figure 1

    Sheep pulmonary adenomatosis: neoplastic proliferation of the alveolar epithelium forming numerous folds and papillary projections on the alveolar wall (H&E ×100)

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  2. ii

    Respiratory syncytial virus (RSV) infection:

    Histological evidence of respiratory syncytial virus infection was observed in a number of ovine lungs (n = 8; 5.7 %) which were initially diagnosed as acute fibrinous bronchopneumonia by gross inspection. Respiratory syncytial virus is a major cause of lower respiratory tract infections in human infants, cattle and sheep (Tripp 2004; Valarcher and Taylor 2007). It is classified as a pneumovirus within the Paramyxoviridae family (McIntosh and Chanock 1990). The name of the virus was based on its characteristic cytopathic effect in forming syncytial giant cells in infected lung tissue. The coexistence of RSV infection in the affected lungs in the present investigation was clearly indicated by the presence of numerous multinucleated syncytial giant cells randomly scattered on the lung parenchyma (Fig. 2). The syncytial cells were variable in size, relatively round or irregular in shape and contained several nuclei within the cytoplasm. Prominent vascular alterations comprising acute capillary congestion, thrombosis and intra-alveolar haemorrhages were also observed. The lung parenchyma showed extensive loss of airspaces due to massive infiltration of neutrophils and macrophages into the alveolar lumens. The inflammatory changes on the lung parenchyma were frequently accompanied by acute necrotizing bronchiolitis and massive destruction and desquamation of the bronchiolar epithelial. In addition, eosinophilic intracytoplasmic inclusion bodies were further detected in the bronchiolar epithelium (Fig. 3). Remarkable hyperplasia of the bronchial and bronchiolar epithelium was observed in less affected areas. The above-described histopathological alterations were similar to those previously reported for the natural and experimental infection with respiratory syncytial virus in cattle and sheep (Kimman et al. 1989; Bryson 1993; Ellis et al. 1996; Larsen 2000; Valarcher and Taylor 2007).

    Fig. 2
    figure 2

    Respiratory syncytial virus infection: multinucleated syncytial giant cells randomly scattered on the lung parenchyma (H&E ×400)

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    Fig. 3
    figure 3

    Respiratory syncytial virus infection: intracytoplasmic inclusion body in the bronchiolar epithelium (arrow) (H&E ×400)

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  3. iii

    Ovine progressive pneumonia (maedi):

    Characteristic microscopic alterations of ovine progressive pneumonia were observed in 12.1 % of pneumonic lungs specimens in the present survey (n = 17). Ovine progressive pneumonia, also known as maedi or maedi-visna, is a slow viral infection of sheep and other small ruminants characterized by progressive lymphoid interstitial pneumonia with disseminated peribronchial lymphoid hyperplasia, lymphoid follicle formation and perivascular lymphocytic cuffing around the small arterioles (Georgsson and Pálsson 1971). The disease is caused by a non-oncogenic exogenous retrovirus belonging to the lentivirus subfamily (Narayan and Clements 1989; Pépin et al. 1998). In the present investigation, affected lungs showed chronic alveolitis with distortion of the alveolar spaces and considerable thickening of the alveolar septa and interstitial spaces. The alveolar septa were diffusely infiltrated with lymphocytes, macrophages, plasma cells and fibroblasts. In addition, there was a remarkable hyperplasia of the bronchial-associated lymphoid tissue (BALT). The proliferating lymphoid cells were forming prominent and well-defined lymphoid nodules within the vicinity of adjacent bronchi and bronchioles (Fig. 4). These previously described histological changes were similar to those consistently reported for the natural and experimental infection with maedi-visna virus in sheep and goats (Oliver et al. 1981; Hananeh and Barhoom 2009; Akkoc et al. 2011; Azizi et al. 2012).

    Fig. 4
    figure 4

    Ovine progressive pneumonia: peribronchial lymphoid hyperplasia with formation of prominent well-defined lymphoid nodules within the vicinity of adjacent bronchi and bronchioles (H&E ×100)

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  4. iv

    Verminous pneumonia:

    Various stages of an unidentified parasitic nematode, probably Muellerius capillaries, were incidentally detected in the alveolar spaces of some pneumonic lung samples (n = 9; 6.4 %). These cases were grossly diagnosed as granulomatous pneumonia. The parasitic larvae were present in cross and longitudinal sections surrounded by dense mixed cellular infiltrations of neutrophils, eosinophils, macrophages and lymphocytes (Fig. 5). Adult worms were also present in the lumen of the bronchi and bronchioles, inciting mild chronic catarrhal inflammations as indicated by accumulation of mucous exudate and inflammatory cells in the bronchial lumen. Mononuclear cellular infiltration was also observed in the lamina propria of the bronchial wall.

    Fig. 5
    figure 5

    Verminous pneumonia: presence of cross and longitudinal sections of parasitic larvae in the alveolar spaces surrounded by dense cellular infiltrations (H&E ×100)

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  5. v

    Pulmonary corpora amylacea:

    Pulmonary corpora amylacea (PCA) were detected in the lumen of intrapulmonary bronchi in several cases of fibrinous bronchopneumonia (n = 5; 3.6 %). They showed typical microscopic appearance of regularly spherical bodies composed of multiple concentric layers of a homogenous bluish- pinkish material with a centrally located spherical nucleus or nidus (Fig. 6). Corpora amylacea are spherical concentrically lamellated microscopic structures occasionally observed in some glandular tissues particularly the mammary glands (Arnold and Weber 1977; Brooker 1978; Claudon et al. 1998). They were also reported to occur in many other glandular and non-glandular tissues including the prostate gland, the lungs and the brain (Rocken et al. 1996). Pulmonary corpora amylacea have long been detected in pneumonic lungs of human patients (Michaels and Levene 1957; Hollander and Hutchins; 1978; Dobashi et al. 1989). Besides, they were also reported to occur in the alveolar spaces of ovine lungs with chronic non-progressive pneumonia (Lin et al. 1989) and acute bronchointerstitial pneumonia (Azizi et al. 2013). In the present investigation, pulmonary corpora amylacea were detected inside the bronchial lumen but not in the alveolar spaces of infected lungs. Although corpora amylacea are generally regarded as incidental findings in most glandular tissues, their presence however may probably indicate the occurrence of a previous injury or preexisting old lesions in which cellular debris and secretions have accumulated (Hollander and Hutchins 1978).

    Fig. 6
    figure 6

    Pulmonary corpora amylacea: the bronchial lumen contains spherical bodies composed of multiple concentrically lamellated layers of a homogenous bluish-pink material (H&E ×100)

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    The present results provided histological evidence of the coexistence of some very important specific respiratory diseases in sheep in the Al Qassim region, KSA. These included sheep pulmonary adenomatosis, ovine syncytial virus infection, ovine progressive pneumonia and verminous pneumonia. As a matter of fact, none of these diseases has previously been recognized, diagnosed or reported in Saudi Arabia. Therefore, further studies are essentially required to determine the actual prevalence and epidemiological status of these diseases in the Al Qassim region and in all other sheep-raising areas in the Saudi Kingdom.