Some studies on tuberculosis in camel By Manal, M. Yehya ... · PDF fileSome studies on tuberculosis in camel By Manal, M. Yehya* and Gobran, R. A.** ... mycobacterium tuberculosis

Egypt. J. Comp. Path. & Clinic. Path. Vol. 21 No. 4 (December) 2008; 58 - 74

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Some studies on tuberculosis in camel By

Manal, M. Yehya* and Gobran, R. A.** * Pathology Dept.; ** Bacteriology Dept.; Animal Health Research Insti-

tute, Dokki, Giza

SUMMARY

A total of 704 camels at different abattoirs were investigated in this study by different techniques for diagnosis of tuberculosis (T.B.).

These examined camels were divided into two groups, the first group with 569 camels which were kept in close contact with cattle and the second group with 135 camels were kept in close farm. Both groups were exam-ined for the presence of tubercles like lesions in different organs. In 1st group, tubercles granuloma could be detected in 25 camels mainly in lungs, lymph nodes and spleen. Eight camels of these group were re-ported as ELISA positive. By bacteriological examination of them, M. bovis could be isolated from 5 camels as well as typical histopathological lesions were observed which formed mainly of granulomatous reactions at different stages and milliary T. B. in 5 camels. On the other hand, in 2nd group 4 camels was positive (+ ve) for granuloma formation and one positive (+ve) for ELISA while were negative for bacteriological and histopathological examination for T.B.

We concluded that the incidence of camels infected with T.B. in Egypt is 0.7% and this incidence present among camels kept in close con-tact with cattle.

Referred byReferred by Prof. Dr. Ali A. El-Abeedy Professor of Mycoplasma, Animal Health

Research Institute, Dokki Prof. Dr. Afaf A. El-Ghawas Professor of Pathology, Animal Health Re-

search Institute, Dokki Prof. Dr. Gehan Hosny Professor of Pathology, Animal Health Re-

search Institute, Dokki

INTRODUCTION

C amels play important socio - economic roles within the

pastoral and agricultural systems in the arid and semiarid zones of Asia and Africa. The survival of millions of human being is de-pendent on the camel in such ar-eas, for meat, milk, hair production

and still as an important mean of draught and transport for large sec-tor of pastoral societies.

Tuberculosis is a disease that had already been diagnosed around the turn of the century in drome-daries in Egypt (Wernery and Kaaden, 2002).


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In tropical developing coun-tries where tuberculosis has re-ceived little attention, substantial economic losses can occur espe-cially in cattle. Tuberculosis as a zonosis, also plays an important role among nomadic people where milk and milk products are con-sumed raw (Seifert, 1992). This also true for camel milk (Don-chenko et al., 1975b) isolated M. bovis strains from 46 pooled milk samples from 712 lactating camel cows in Russia. Tuberculin tests were performed in these herds whereby 9.1% were reactive. Other than unheated camel milk, circus and zoo camels with active disease also present a danger to man (Dekker and Van Der Schaaf, 1962).

Tuberculosis persists as a costly zoonotic disease in numer-ous countries despite extensive eradication and control efforts, tu-berculosis in humans may result from exposure to any one of the tubercle bacilli included within the mycobacterium tuberculosis com-plex (i.e. M. tuberculosis, M. bo-vis, M. africanum, M. pinnipedii and M. microti). Mycobacterium bovis, unlike M. tuberculosis has a wide host range in the species most often isolated from tubercu-lous cattle and has several wild life maintenance hosts (Waters et al., 2006).

Duguid et al. (1983) reported

that the tubercle bacillus doesn't produce any toxin apart from the hyper sensitivity reaction which develops only in animals previ-ously infected with organism. The bacilli ingested by macrophages multiply slowly ingeneration time 6 to 12 h. depending on their being able to resist destruction by ly-sosomal enzymes. Macrophages died and disintegrated after laden with numerous bacilli and liber-ated bacilli continue to multiply extracellularly in tissue fluid or af-ter ingestion by other phagocytes. Termination of infection depended on the development of cell medi-ated immunity and a consequent production of activated macro-phages which have increased abil-ity to kill ingested bacilli.

Clinically tuberculosis di-vided into primary infection (Ghonfocus) which develops at the site of implantation of single air borne particle bearing one or few bacilli which mainly occur in lungs or some times occur in intestine as a result of ingestion of food con-taminated with M. bovis. From the primary lesion the bacilli are car-ried by lymphatic drainage to the regional lymph nodes which may be progressive enlarged and fol-lowed by caseation and calcifica-tion. Haematogenous spread oc-curs with implantation of bacilli in many organs leading to millary tu-berculosis. The post primary tuber-culosis developed in previously


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infected animal either as a result of endogenous reactivation of latent disease or exogenous reinfection in which one or more lung lesions progress to caseation and cavita-tion and involving the bronchial tree create a case of open tubercu-losis (Crofton et al., 1992).

The diagnosis of camelid tu-berculosis in living animals faces many difficulties. Non of the tests available can diagnose tuberculosis with certainly. Intradermal tuber-culin test, which is the classical di-agnostic test often gives non spe-cific reactions in camelids (Paling et al., 1988).

The aim of the present study was to determine the incidence of T.B. infection in camels as well as to compare between the bacterio-logical and histopathological tech-niques used for diagnosis of T.B. in camels..

MATERIAL AND METHODS

* Examined animals: This study performed on 704

camels at abattoirs. These camels were classified according to place which come from into 2 groups: 1st group: 569 camels belonged to

farmers who kept them in close contact with cattle and other animal species from different areas in Egypt.

2nd group: 135 camels which kept in closed farms from different localities in Egypt.

* Postmortem examination and samples collection:

Tissues with high infection expectation were collected from each examined animal both males and females, included lungs, spleen, the anterior and posterior mediastinal lymph nodes, left and right bronchial and left and right medial retropharyngeal lymph nodes (Table 1-A).

Each tissue specimen were divided into two parts, one part placed in sterile containers and submitted to the laboratory for bacteriological examination. The second part of these organs were fixed in 10% formalin and sub-jected to pathological examination. Other tissues with a low expecta-tion of infection (Table 1-B) were sliced in-situ and examined visu-ally. When lesion resembling tu-berculosis were found they were submitted for bacteriological ex-amination and histopathological examination up to a maximum of 3 lesions were examined from each animal (Corner et al., 1990). Se-rum samples for ELISA were col-lected from suspected animals.


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Table (1): Tissues examined for lesions of tuberculosis in animals.

A. Tissues collected for bacteriological exami-

nation

B. Tissues examined incision at the time of slaughter

Lung and spleen

Head

* Mandibular lymph node * Parotid lymph node * Lateral retropharyngeal lymph node * Tonsils

Medial retropharyngeal lymph nodes1. Thorax

* Tracheobronchial lymph nodes * Lungs

Mediastinal lymph no-des Abdomen

* liver and hepatic lymph node * spleen * Kidneys * mesenteric lymph nodes

Anterior and posterior tracheobronchial lymph nodes

Carcasses

* Caudal cervical lymph nodes * Subiliac lymph nodes * Medial iliac lymph nodes * Supramammary lymph nodes. * Politeal lymph nodes * Internal iliac lymph nodes * Gluteal lymph nodes * Lateral iliac lymph nodes

1. Includes left and right lymph nodes.

*Direct smears: Direct smears were made

from lesions for staining with Ziehl – Neelsen stain (Dwight and Yuan, 1999).

*Bacteriological examination of collected specimens (Marks, 1972):

All tissues submitted to the laboratory were examined bacte-riologically for Mycobacterium

species. The isolation of typical Mycobacterium species was used as the definitive test for the diag-nosis of camel tuberculosis, whether from animal with sus-pected tuberculous lesion or from tissues without visible lesions.

The collected tissue samples were dissected from fat and con-nective tissues and 2 gram portion of tissues from each specimen was


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gross lesions (tuberculous like le-sion in necropsid animal) could be detected in 25 camels only. By bacteriological examination of them. M. bovis could be isolated from 5 camels as well as typical histopathological lesion for T.B. was detected and 8 from this group of camels were recorded as ELISA positive. The impression smear of infected lung which stained by Ziehl Neleelsen showed the acid fast bacilli of T.B. (Fig. 1).

Regarding to 2nd group of camels (kept in closed farm) only four camels were positive for P/M examination and one camel was positive for ELISA while all cam-els gave negative results for bacte-riological and histopathological examination for T.B.

Different organs of slaugh-tered camels were examined as shown in table (1). The post mor-tem changes of examined organs mostly showed numerous milliary tubercles of the same widely scat-tered on the surface and deep in the lung parenchyma. In addition to large areas of the lung tissue ap-peared solid and caseated. Enlarge-ment of bronchomediastinal lymph nodes with the presence of white nodules 1 mm to 2 cm in diameter and prominent caseous spheroidal masses in the spleen. In sectioning a tubercle a gritty sensation and grating sound indicate the presence of calcareous material. Histopa-

thological examination of the lung revealed tuberculous pneumonia with large area caseated and ne-crosed alveoli with thickening of the pulmonary blood vessels and congested alveolar capillaries (Fig. 2) with severe hyperplasia of the bronchii (Fig. 3), thickening of the pleura with productive and prolif-erative response of fibrous tissues (Fig. 4). Typical characteristics of tuberculous lesions with caseous material in the central surrounded by aggregation of epithelioid cells and large number of lymphocytes with the tendency for fibrous tis-sues proliferation (Fig. 5), the caseated center undergo calcifica-tion with intense lymphocytic cell infiltration, fibrous connective tis-sues reaction and scanty langrhans giant cells were seen in the mar-ginal zone of old tubercles (Fig. 6). Old lesions of the lung where most of the lung parenchyma appeared fibrosed and bronchi surrounded with fibrous connective tissues with scanty lymphocytic infiltra-tion (Fig. 7). Sometimes lung ap-peared with different myriad tuber-cles 2-3 mm in diameter all of the same age and size named military tuberculosis with dilated alveoli and fibrosis of its wall with some necrotic and disintegrate cells in its lumen (Fig. 8).

Lymph nodes appeared with severe haemorrhage (Fig. 9) with the development of the typical fea-tures of granuloma began with


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homogenized with 2 ml of sterile distilled water in a sterile mortar containing sterile sand. Two ml of 4% H2SO4 were added to the mix-ture and incubated at 37 °C for 30 minutes. The mixture was diluted with 16 ml of sterile distilled water and centrifuged at 3000 rpm for 20 minutes. The supernatant fluid was poured off onto disinfected and the obtained sediment was inoculated into four lowensteinjensen slants (BioMerieux), then incubated at 37 °C for 8 weeks. The inoculated slants were examined daily over a week. Suspected colonies were subcultured and identified accord-ing to Chadwick (1981).

Enzyme Linked Immunoa-bsorbent Assay (ELISA) tech-nique:

ELISA for serological diagno-sis of tuberculosis in camels was performed as described by Rilacco et al. (1990). Microtitre plates were coated with bovine 50 µl PPD diluted in (10 µg/ml) carbon-ate bicarbonate buffer, (pH 9.6) and incubated for 20 h. at 4°C in humfied atmosphere. After wash-ing with PBS tween 20 (0.05% w/v) well were blacked with dried milk diluted in PBST (10% w.v). The blocking buffer tipped off and 100 µl/well of tested serum sam-ples diluted 1:50 were added and incubated at 37 °C for 60 minutes. After 3 washing with PBS (pH 7.4) containing 0.01% tween 20, 150 µl

of protein A horseradish peroxi-dase conjugate (1:1000) was added to each well and then incubated at 37 °C for 60 minutes. After wash-ing again working solution of ABTS substrate (100 µl/well) was added and incubate at 37 °C for 15 minutes.

The optical density recorded at 405 nm in Dynatech micro-ELISA reader. An ELISA reading that is equal to/or higher than dou-ble fold of the ELISA reading of negative control is considered positive.

Histopathological examinat-ion:

Post-mortem examination was carried out on the slaughtered cam-els. Tissues specimens were taken from the inspected tubercules and fixed in 10% neutral formalin. Processed routinely for embedding in paraffin and sectioned at 4-5 µ thick. Sections were stained with haematoxylin and eosin and exam-ined microscopically and for the detection of acid fast bacilli in tis-sues, sections were stained with Ziehl-Neelsen stain according to (Bancroft et al., 1996).

RESULTS

T he results of different tech-niques for diagnosis of tuber-

culosis in examined camel groups are summarized in table (2).

From 569 camels which kept in contact with cattle (1st group),


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clusters of neutrophils surrounded the invading bacilli (Fig. 10). This was replaced by whorl of lympho-cyes and macrophages that takes on a different appearance where the cells became reminiscent of epithelial cells with abundant eosi-nophilic cytoplasm that termed epithelioid cells (Fig. 11, 12) calci-fied tuberclus was also observed with aggregation of epithelioid cells and lymphocytes (Fig. 13).

Spleen appeared with thicken-ing of the splenic blood vessels

and haemocidrosis (Fig. 14) other lesions appeared to be slight, the same as in lungs and lymph nodes where the splenic parenchyma showed granulomatous reaction (Fig. 15) which undergo caseation and calcification with infiltration by mononuclear cells and prolif-eration of fibrous connective tissue (Fig. 16). For farther diagnosis of the tubercle bacilli, spleen stained with Ziehl-Neelsen stain where the bacilli appeared as red road shape with blue black ground (Fig. 17).

Table (2): Correlation between post-mortem, bacteriological and patho-logical examinations of examined camels.

Animal exam-ined

Num-ber

P/M ELISA Bacteriologi-cal examina-

tion

Pathological examination

No.

(a) % No.

(+ ve) % No. (b) % No.

(c) %

1st group (Camel in con-tact with cattle)

569 25 4.39e 8 32d 5 20d 5 20d

2nd group (Ca-me l kep t i n closed farm)

135 4 0.7e 1 25d 0 - 0 -

Total 704 29 18.4e 9 1.3e 5 0.7e 5 0.7e

(a): Presence of tubercles like lesions. (b) = 5 isolated microorganism identified as Mycobacterium bovis. (c) = 5 presence of the typical tubercles granuloma with langerhan's gaint

cells. (d) = % calculated according to No. of P/M positive camels. (e) = % calculated according No. of examined camels.


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Fig. (1): Impression smear of lung showing red acid fast bacilli with dark blue back ground (Ziehl Neel-son, X 650).

Fig. (2): Lung showing tuberculous pneumonia with large area of the alve-oli was caseated and necrosis with thickening of the wall of pulmonary blood vessels and congested alveolar capillaries (H & E X 200).

Fig. (3): Lung showed hyperplastic proliferation of epithelial lining the bronchi (H & E X 400).

Fig. (4): Lung showed thickening of the pleura with fibrous connective tis-sues proliferation (H & E X 200).

Fig. (5): Lung showed typical tubercles lesions with caseous material in the central surrounded by aggregation of epithelioid cells and lymphocytes (H & E X 200).


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Fig. (6): Lung showed calcified tu-bercle with mononuclear inflamma-tory cells with fibrous connective tissue reaction and scanty langhans giant cells in the marginal zone. (H & E X 400).

Fig. (7): Lung showed old lesion, where most of the parenchyma and bronchii appeared fibrosed and bronchi surrounded by fi-brous connective tissues with scanty lymphocytes (H & E X 400).

Fig. (8): Lung showed milliary tu-berculosis where the lung appeared with different myrried tubercles all the same age and size sometimes calcification and infiltration by mononuclear cells were observed (H & E X 200).

Fig. (9): Lymph node showed se-vere haemorrhage (H & E X 200).


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Fig. (10): Lymph node showed the beginning of the granuloma forma-tion where clusters of neutrophils surrounding the invading bacilli (H & E X 400).

Fig. (11): lymph node showed whorl of epithelioid cells in the central of garnuloma that replaced the eneutrophils (H & E X 200).

Fig. (12): Lymph node showed graunuloma with aggregation of epithelioid cells and lymphocytes (H & E X 400).

Fig. (13): Lymph node showed calcified tubercles surrounded with reminant of neutrophils, epi-thelioid cells and lymphocytes (H & E X 400).


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Fig. (14): Spleen showed thickening in the wall of splenic blood vessels and haemocidrosis (H & E X 400).

Fig. (15): Spleen showed granuloma in th esplenic paren-chyme (H & E X 200).

Fig. (16): Spleen showed old granu-loma with caseation, calcification and proliferation of fibrous connective tis-sues (H & E X 200).

Fig. (17): Spleen showed red rod shape tubercles bacilli (Ziehl-Neelsen X 400).


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DISCUSSION

T uberculosis is a chronic conta-gious disease caused by my-

cobacteria, which affects many vertebrate animals and particularly manifests itself in lungs and lymph nodes. The lesions are granulomas known as tubercles (Manefield and Timson, 1996).

From the result illustrated in table (2). It is clear that 5 animals from 569 camels kept in close con-tact with cattle were positive for tuberculosis while all examined camels kept in closed farm (group 2) were negative for tuberculosis with incidence of 0.7% and 100% bovine type, these were agreed with Refai (1993) who reported the incidence of tuberculosis in camels in Egypt by 0.3% to 4% and mostly of bovine type. The ELISA-PPD using protein labeled with horseradish peroxidase conju-gate as a substitute for the specific anticamel IgG conjugate, can be applied in the detection of antitu-berculosis antibodies in camels. ELISA could detect 9 cases as positive (1.3 %) but by comparison with bacteriological finding only 5 camels were positive from which M. bovis were isolated. The other false positive cases may be attrib-uted to non specific antibodies due to other microorganism. These re-sults coincided with El-Sergany et al. (1991) who failed to isolate Mycobacterium organisms from ELISA positive animals but the

isolated organisms were Coryne-bacterium, Staphylococci, Citro-bacter species and E. coli.

These positive animals by post mortem inspection and histo-pathological examination revealed typical tubercles granulomas mai-nly in lungs, lymph nodes and spleens with tubercules pneumonia and hyperplastic proliferation of cells lining bronchi which may be attributed to the irritation action of the microorganism thus the histo-pathological scores were generally positively correlated with CFU counts (Dormans et al., 2004).

In the early stages of active tuberculosis most tubercle bacilli are taken with macrophages that destroy them by various lysosomal enzymes and reactive oxygen in-termediates ROI (Rook and Blo-om, 1994). There are 3 strategies by which mycobacteria survive within macrophages. First, they inhibit fusion of the phagosome to the lysosomes. Second, they neu-tralize ROI by means of cell wall lipids including peptidoglycolipids and lipoarabinomannan and by se-creting the enzyme super oxide disminase. Third, they escape from the phagosome and replicate in the cytoplasm of the cell (McDo-nough et al., 1993). When tubercle bacilli enter macrophages and not destroyed, they replicated and kill the cell and local area of inflam-mation is established by attract


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more phagocytes to the site of in-fection. Some bacilli transported within phagocytes to regional lymph nodes where they are en-gulfed by antigen presenting cells (APC) and the epitopes from my-cobacteria presented on the cell surface formed (CD4 + helper T cells which undergo activation and produce cytokins including inter-feron Y (IFN-Y) that activates macrophages and draw more of these cells to the lesion arranged in compact palisade, resemble epithe-lial cells termed epithelioid cells that may fuse together to form multinucleated giant cells which are the characteristic of the granu-lomas of tuberculosis. This acti-vated macrophages produce a cy-tokine termed tumor necrosis fac-tor (TNFα) which plays a key role in protective immunity by main-taining the integrity of the granu-loma and haematogenous spread occurs with implantation of bacilli in many organs leading to millary tuberculosis (Collier et al., 1998).

It is highly likely that the en-tire granuloma is much more capa-ble of destroying tubercle bacilli than isolated macrophages. This palisade of metabolically active macrophages consumes oxygen diffusing into the granuloma so that the center became anoxic and undergoes necrosis termed casea-tion. This anoxia and free fatty ac-ids provide an environment highly unfavorable to the bacilli many of

which die and the granulome be-come inactive, fibroblasts sur-rounded them and may be calcified (Dannenberg, 1993). Our histopa-thological finding were in agree-ment with Wernery et al. (2007); Kinne et al. (2006) and Oev-ermann et al. (2004). All results agree with Gatt and Mack (1963) who reported that in Egypt, Tuber-culosis didn't occur in nomadic camels but in those belonging to farmers who kept them in close contact with cattle. The mode of transmission of tuberculosis is un-known in camelids but it is pre-sumed similar to that in cattle. In cattle it is mainly horizontal. It is believed that camelids suffering from pulmonary tuberculosis infect healthy animals via aerosols. The alimentary, congenital, veneral and cutaneous routes that may occur in cattle have not been described in camelid. Kogramanov et al. (1971) found that the Ixodes tick Hyalomma asiaticum can transmit M. tuberculosis to camels. In this concern Donchenko et al. (1975a) reported that tuberculosis is rare among camels kept under nomadic condition. The disease occurs more frequently when camels are kept in close quarters with other animals or in close contact with cattle.

It is concluded that the inci-

dence of camels infected by T.B is 0.7% in Egypt. The infected cam-els were reared with cattle or be-side cattle farms. The isolated


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strain was M. bovis. The ELISA technique is most efficiency in the diagnosis of T.B as well as the histopathological examination.

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Some studies on tuberculosis in camel By Manal, M. Yehya ... · PDF fileSome studies on tuberculosis in camel By Manal, M. Yehya* and Gobran, R. A.** ... mycobacterium tuberculosis