(a) pathological, histochemical and immunohistochemical ... · (bbb) generally, in all liver and...

U. of K. Graduate College and Scientific Research. The 5th Annual Conference - Agricultural and Veterinary Research - February 2014, Khartoum, Sudan,

Conference Proceedings – Volume Two

328

(a) Pathological, Histochemical and Immunohistochemical Studies of

Lungs and Livers of Cattle and Sheep Infected with Hydatid Disease

(b) Sara Elgaili Ali Ibrahim1*

and Ahmed A. Gameel2

(c) 1 Faculty of Veterinary Medicine, University of Bahri, Sudan

(d) 2 Faculty of Veterinary Medicine, University of Khartoum, Shambat, Sudan

(e)

(f) ABSTRACT

(g)

(h) This work was carried out to study the pathological changes in the lungs and livers

with hydatid disease of slaughtered cattle and sheep. Lungs and livers of 521 cattle

and 675 sheep were examined. Infection rates of 4.8% and 1.8% were recorded in

cattle and sheep, respectively. The predilection sites in cattle were the lungs and the

livers, while in sheep cysts were only found in the livers. In cattle, lung and liver,

cysts were mostly of medium size (2–4 cm), but large cysts (> 4 cm) were, also,

observed, while most of sheep liver cysts were small in size (< 2 cm). The amount of

fluid from hydatid cyst of cattle ranged from 0.2 to 50 ml; only one cyst contained

600 ml. In sheep, the cyst contained small amounts of liquid with a maximum of 3

ml. The fertility rates of the cysts were 23.4% and 11.1% in cattle and sheep,

respectively. Cyst sections from infected lungs of cattle showed laminated

membranes surrounded by a zone of cellular infiltration of mainly lymphocytes,

plasma cells, macrophages and rarely neutrophils, eosinophils and giant cells and the

outermost fibrous tissue reaction. Calcification was, also, observed. The

neighbouring tissues showed atelectasis, emphysema, haemorrhage, congestion and

fibrosis. Sections from the second, third and fourth centimeters away from the cyst

walls showed similar but less pronounced pathological reactions. In liver cyst

sections, the pathological changes were almost similar to that observed in the lungs

with atrophy and necrosis of hepatocytes. Immunohistochemical studies revealed

that all slides stained with markers for CD³ and CD²º showed positive reaction for

CD³ and negative for CD²º. This finding suggests that the cellular reaction in the

hydatid cyst wall consists mainly of T-lymphocytes. In all liver and lung sections

from cattle and sheep stained with Masson’s trichrome stain, and fibrous tissues in

the hydatid cyst capsules or around blood vessels and air passages stained green.

The acellular laminated membranes and the protoscolices, also, stained green. In

hydatid cyst sections from cattle and sheep stained with Periodic Acid Scheff (PAS),

and laminated membranes, germinal layers and protoscolices took positive PAS

magenta colour. It is concluded that the presence of cyst in an infected organ causes

pathological changes in tissues around the cyst and further away from the cyst. It is,

also, concluded that T-lymphocytes (CD³ positive cells) appear to dominate the



329

mononuclear infiltrate as demonstrated by immunohistochemistry. This indicates

that T. lymphocytes play a role in immunological reaction against hydatid cyst.

(i) Key words: Hydatid disease; cattle; sheep; pathology; immunohistochemistry

(j) *Corresponding author: E-mail: [email protected]

(k) INTRODUCTION

(l) Hydatid disease is a worldwide zoonosis produced by the larval stage of the

Echinococcus tapeworm. The two main types of hydatid disease are caused by E.

granulosus and E. multilocularis (Pedrosa et al., 2000). The life cycle of E.

granulosus involves two hosts. The definitive host is usually a dog but may be some

other carnivores. The adult worm of the parasite lives in the proximal small bowel of

the definitive host, attached by hooklets to the mucosa. Eggs are released into the

host's intestine and excreted in the feces. Sheep are the most common intermediate

hosts. They ingest the ovum while grazing on contaminated ground. The ovum loses

its protective chitinous layer as it is digested in the duodenum. The released

hexacanth embryo, or oncosphere, passes through the intestinal wall into the portal

circulation and develops into a cyst within the liver. When the definitive host eats

the viscera of the intermediate host, the cycle is completed (Pumarola et a.l, 1990;

Lewall, 1998). Humans may become intermediate hosts through contact with a

definitive host (usually a domesticated dog) or ingestion of contaminated water or

vegetables. Many studies have been conducted on the epidemiology, pathology and

molecular aspects of the disease (Saad, 1984; Tola, 1987; Elsawi, 1994, Adam,

1997, 2004; Osman, 2007; Omer et al., 2010). However, updating information in

animals was undertaken to provide further information on the epidemiology,

pathology and immunohistochemistry of the disease in cattle and sheep in Sudan.

(m)MATERIALS AND METHODS

(n) Samples A total of 521 cattle and 675 sheep slaughtered in Alsabaloga and Alsalam

Abattoir during the period from October 2011 to February 2012 were examined for

the presence of hydatid cysts. All organs, especially lungs and liver, were carefully

examined, and organs with cysts were described in terms of number of cysts, their

sizes and sites, contents and fertility.

(o) Pathological examination Livers and lungs from cattle and sheep were carefully

examined for the presence of any cyst. Gross description of the cyst was based on

location, size and number of cysts per organ.

(p) Histopathological and histochemical examination part of the cyst wall together

with the neighbouring liver and lung tissue up to 5 cm away from cyst wall were

mailto:[email protected]



330

taken and fixed in 10% neutral formal saline for histopathological, histochemical

and immunohistochemical studies. Tissue samples were prepared in paraffin and

sections 4-6 µm thick were prepared. Sections for routine histopathology were

stained using haematoxylin &eosin (H&E), and for histochemical study were stained

using Periodic Acid Schiff stain (PAS) and Masson's trichrome stain (Drury and

Wallington, 1980).

(q)

(r) Immunohistochemical methods

(s) Three µm sections were cut and placed on clean immunohistochemical (IHC)

microscope slides (K8020, Flex, Dako, Denmark), prepared and stained using

markers for CD3 and CD20 according to the manufacturer procedures (Dako,

Denmark).

(t) RESULTS

(u) Infective rate

(v) Infective rates of 4.8% and 1.8% were recorded in cattle and sheep, respectively

(Table 1).

(w)

(x) Predilection site

(y) In cattle, the predilection sites were the lungs followed by livers, while in sheep

cysts were only found in livers (Table 1).

(z)

(aa) Cyst size

(bb) In cattle lungs and liver cysts were of mostly medium in size (2 – 4 cm), but

large cysts were, also, observed (> 4 cm) while most of sheep liver cysts were of

small size of < 2 cm (Table 2).

(cc)

(dd) Fluid amount

(ee) The amount of fluid from hydatid cysts of cattle ranged from 0.2- 50 ml

according to the size; only one cyst contained 600 ml. In sheep, cysts contained

small amounts of liquid, maximum of 3 ml.

(ff)

(gg) Fertility of cyst

(hh) The fertility test revealed 23.4% and 11.1% fertility rate in cattle and sheep,

respectively.

(ii)

(jj) Pathological findings



331

(kk) Gross description: most cysts were round in shape and of variable sizes.

They were either protruding from the surface or found deep in lung or liver

parenchyma (Figs. 1 and 2). The cyst had thick membrane, the cut surface of the cyst

manifested cavities lined by a smooth membrane which could easily be removed.

Some cysts were filled with a clear or turbid fluid, caseated (cheese like) material,

and others were calcified.

(ll)

(mm)

(nn) (a)

(oo)

(pp)

(qq) (b)



332

(rr) Fig (1) a) Sheep liver showing multiple partially embedded cysts with thick

membrane. b) cross section of hydatid cyst in bovine liver.

(ss)

(tt) (a)

(uu)

(vv) (b)

(ww) Fig (2) a) Cattle lung showing completely embedded single cyst. b) Cattle

liver showing multiple cyst, partially or completely embedded in the parenchyma.

(xx)

(yy) Microscopic findings



333

(zz) In cattle lungs, sections of the first centimeter comprising the hydatid cyst

wall showed intact or disrupted laminated membrane moderate to broad fibrous

capsule. Some sections showed protoscolices, congestion, haemorrhage, fibrosis,

and heavy cellular infiltration composed of mononuclear cells mainly lymphocytes.

Hyperplasia of the bronchial and bronchiolar epithelium, atelectasis and emphysema

were seen in distant lung tissues. Fibrosis around bronchioles and blood vessels was

seen extending into the tissue parenchyma. Some sections showed calcification of

cyst wall, while others showed collapsed bronchioles. Cellular infiltration was

mainly seen in the fibrous capsule, and around blood vessels and bronchioles.

Sections of the second centimeter neighbouring the cyst, showed similar changes to

that of the first centimeter but emphysema was more pronounced. Few sections

showed slight fibrosis around bronchioles and few others showed interstitial

thickening, with presence of cellular infiltration in alveoli and airways. No

calcification was seen. Sections of the third centimeter away from cyst wall showed

congestion, haemorrhage with slight fibrosis mainly around bronchioles. Some

sections showed thickened interstitium with inflammatory cell infiltration. Sections

prepared from the fourth centimeter away from cyst wall, showed congestion,

haemorrhage, emphysema, atelectasis and cellular infiltration especially around

bronchioles.

(aaa) In sheep, liver sections prepared from the first centimeter neighbouring the

cyst wall showed congestion, haemorrhage, hepatocyte necrosis and atrophy

together with fibrosis and cellular infiltration of mainly lymphocytes and plasma

cells seen mostly in the inner side of the fibrous capsule which appeared broad.

Calcification was seen in the cyst wall. There was dilatation of sinusoids, and some

central veins. Fibrosis was, also, seen in the portal area. In the second centimeter,

most of the sections showed congestion, haemorrhage and hepatocyte necrosis.

Some sections showed fibrosis mainly in the portal areas, cellular infiltrate was seen

in sinusoids. No calcification was observed. In the third centimeter, most sections

showed similar changes to that in the second sections but the changes were less

pronounced.

(bbb) Generally, in all liver and lung sections from cattle and sheep, fibrous tissue

in the hydatid cyst capsules or around blood vessels and air passages stained green

with Masson’s trichrome. The acellular laminated membranes and the protoscolices

also took the green color. On the other hand, in the sections from cattle and sheep

stained with PAS, the laminated membranes, germinal layers and protoscolices took

positive PAS magenta colour (Figs. 3 to 6).

(ccc)



334

(ddd)

(eee) Figure (3) Cattle lung hydatid cyst showing continuous laminated membrane

(LM), fibrous tissue capsule(FC) and collapsed adjacent tissue (H&E X4).

(fff)

(ggg)

(hhh)

LM

FC



335

(iii)

(jjj)Figure (4) a) Sheep liver with hydatid cyst: showed portal fibrosis (star) (Masson’s

trichrome x10). b) cattle lung: showing fibrosis(star) (H&E x 10)

(kkk)

(lll)

(mmm)



336

(nnn)

(ooo) Fig(5) cattle lung tissue showing intact laminated membrane (arrow) X4, (a)

PAS stain, (b) Masson’s trichrome stain X4.

(ppp)

(qqq)

a b



337

(rrr)

(sss) Figure (6) Sheep liver showing broad fibrous capsule(FC), infiltration of

inflammatory cells (arrow), hepatocyte atrophy, degeneration and necrosis

(arrow)(x10).

(ttt)

(uuu) Immunohistochemical findings

(vvv) Slides stained with markers for CD3 and CD20 showed positive reaction for

CD3 and negative reaction for CD20. Positivity of CD3 varied according to the

animal species. High positivity was seen in cattle followed by sheep. The reaction

was observed mainly in cells in the cyst wall and cells infiltrating tissues

neighbouring the cyst wall. The reactions appeared as scattered brown stained cells

in the cyst wall and parenchyma in sections obtained from the two animal species.

(www)

(xxx)

FC

CC



338

(yyy) Figure (7) Cattle lung, hydatid cyst showing positive reaction for CD3

marker (x10)

(zzz)

(aaaa) (b)

Figure(8) Sheep liver showing (a) positive reaction for CD3 marker (x4). (b) Closer

view(x10).

U. of K. Graduate College and Scientific Research. The 5th Annual Conference - Agricultural and Veterinary Research - February 2014, Khartoum,

Sudan, Conference Proceedings – Volume Two

339

Table.1 Occurrence of hydatid cysts in slaughtered cattle and sheep

Table 2. Sizes of hydatid cysts from livers and lungs of cattle and sheep

Total

No. of

cysts

Lung Total

No. of

cysts

Liver

Small

< 2 cm

Medium

2-4 cm

Large Small Medium Large

27 2 21 4 19 4 12 3

DISCUSSION

In the present study, 521 cattle and 675 sheep were examined at meat inspection

for presence of hydatid cysts. Twenty five (4.8%) and 12 (1.8%) of the cattle and sheep,

respectively, were found infected with hydatid disease. This result agrees with the results

reported by Saad (1985), Njoroge et al. (2005), Osman (2007) and Mohammed (2010)

and is comparable with those reported by Tola (1987) found high infection rate in camels

(61.3%) followed by sheep (2.1%) and cattle (2.0%) and Abdul Latif (2009) who found

infection rate of 5.18% and 7.52% in cattle and sheep, respectively. Ould Ahmed Salem

et al. (2011), also, found that the infection rates were 5.5% and 6.5% in cattle and sheep,

respectively. The present findings, disagree with those of Torgerson et al. (2009) who

reported high infection rate in sheep (64%), Azlaf and Dakkak (2006) who reported

infection rate of 56% and 40% in cattle and sheep, respectively; and with those of Fromsa

and Jobre (2011) who reported 35.15% and 11.78% in cattle and sheep, respectively.

The frequency of cysts was about equal in livers and lungs of the surveyed cattle.

In sheep, cysts were only found in the livers and were small and infertile except two

Total No. (%) Organ affected No. of

animals

infected (%)

No. of

animals

slaughtered

Animal

species Liver No.

(%)

Lung No.

(%)

47(9.0) 19(40.4) 28(59.6) 25(4.8) 521 Cattle

18(2.7) 18(100) - 12(1.8) 675 Sheep



340

cysts. These findings partially agree with Tola (1987) and Abdul latif (2009) who found

that most cysts in cattle and sheep were in the lungs followed by livers. Acosta-Jamett et

al. (2010) showed that cattle had higher prevalence in livers compared to lungs in sheep

high prevalence was in livers. Elsawi (1994), also, reported that the liver is the

predilection site in sheep infected with hydatid cyst and this agrees with Osman (2007)

and Mohamadin and Abdelgadir (2011). No cysts were observed in this study in organs

other than the livers and lungs. Mohammed (2010), also, found that hydatid cysts

measured between 0.5- 10 cm in cattle and 0.9- 3 cm in sheep. Osman (2007) noticed that

most cyst size lie between 2-6 cm in cattle and less than 2 cm in sheep. Saad (1985)

found cysts measuring up to 9.5 cm in cattle while Tola (1987) encountered cysts with an

average size of 5 cm in cattle and sheep. Tola (1987) observed that fertile cysts were

most common in sheep (60.4%) while cysts from cattle were frequently calcified

(36.4%). The present results indicated the opposite; 23.4% cattle cysts were fertile with

brood capsule and protoscolices while only 2 cysts of sheep were fertile. Saad (1985)

found that fertility rate in cattle were 29%, while Mohammed (2010) found that 23.1%

and 8.3% of cysts from cattle and sheep, respectively were fertile. However, Osman

(2007) concluded that cattle hydtid cysts were more fertile than those of sheep.

Comparing E. granulosus infection in wallapies and sheep, Barnes et al. (2007) observed

that the development of hydatid cysts was more rapid and the onset of fertility occurred

earlier in wallapies than in sheep, and that degenerative changes were more frequent in

sheep cysts. This may partially explains why sheep cysts were small and less fertile than

cattle cysts investigated in the current study. The presence of cysts in the lungs and livers

is likely to be associated with tissue damage and functional disorders, and this has been

indicated by the histological changes observed in infected organs. In the current study,

the number of cysts encountered in the infected lungs and livers in the two animals

examined ranged between 1 to 3 cysts except one cattle liver which contained 15 cysts.

This finding agrees with Tola (1987) who reported that most infected organs contained 1-

2 cysts but multiple infection with more cysts/animal were, also, observed.

The structure of cyst wall comprised the laminated membrane with a thin inner most

germinal layer surrounded by a zone of mononuclear cells of mainly lymphocytes

(occasionally with neutrophil, eosinophil and giant cells) and fibrous tissue capsule.

Marked eosinophil infiltration reported by some authors (Sakamoto and Cebrera, 2003)

has not been observed here. Laminated membrane was in most cases disrupted and the

fibroplasias was variable being more pronounced in caseated and calcified cyst and in

case of sheep cyst. Saad (1985), Verma and Swammy (2009) reported that the fibrous

capsule response was dense and diffuse in fertile cysts. However, the laminated

membrane varied in thickness and in some sections was not clearly visible. Degenerated

laminated membranes were associated with heavy infiltration of inflammatory cells in the

inner side of the fibrous capsule. These features have been previously descriped (Hamid,

2012; Barnes et al, 2011; Kul and Yeldiz, 2010; Osman, 2007; Verma and swammy,



341

2009). Pathological changes have been observed in both liver and lung tissues around the

cyst wall; atelectasis, bronchiolar collapse and emphysema were seen in lung tissue, and

hepatocyte atrophy, degeneration and sinusoidal dilatation were observed in liver tissue.

In few sections from cattle brood capsules and protoscoleses were seen histologically.

Such changes has been previously noted in lungs and livers infected with hydatid disease

(Adam, 1997; Osman, 2007). Sections from lungs and livers prepared from sites up to

five cm away from cyst wall exhibited significant changes which were less expressed

further away from the cyst wall, and there were mainly attributed to the pressure effect

exerted by the hydatid cyst.

For Histochemistry, sections of hydatid cyst were stained using periodic acid Schiff

(PAS) and masson’s trichrome stains. The cyst wall consisted of three layers which are

inner most germinal layer, laminated layer and outer fibrous layer. PAS staining was

found to be superior in showing the laminated membrane and germinal layer where as

Masson’s trichrome was equally good in showing the laminated membrane and superior

in demonstrating the fibrous tissue capsule. These findings agree with that of Khalifa et

al. (2005) who concluded that the three layers of the cyst wall were better stained with

PAS, due to the presence of mucopolysaccharides and glycoproteins in laminated layer,

and also agree with Rashed et al, (2004) who used PAS and Masson’s trichrome stains

and found that the thickness of layers varied with each stain according to glycogen and

mucopolysaccharide content. In the present investigation, immunohistochemical studies

were performed in an attempt to characterize the lymphocyte infiltrate within liver and

lung tissues. The results showed that the inflammatory cells in all sections showed

positive reaction for CD3 markers but negative reaction for CD20 markers. The negative

reaction to CD20 markers indicates absence of B - lymphocytes as CD20 represent positive

B cells. On the other hand, CD3 represent positive T- lymphocytes and CD3 surface

marker is associated with the T cell receptors in both CD4 and CD8 cells. The number of

CD3 positive T cells is an approximation of the sum of CD4 and CD8 T cells (Keir et al.,

2002; Naji et al., 2007). This indicates that the cells infiltrating the hydatid cyst wall in

the sections examined belonged to the CD4, CD8 T lymphocytes which may play a role in

the immune response of animal hydatidosis as suggested in case of human infection

(Pearce et al., 1991).

REFERENCES

Abdul Latif, A. (2009). Genotyping of Echinococcus granulosus in Punjab. PhD thesis.

University of the Punjab, Quaid-E-Azam, Lahore.

Acosta-jamett, G.,Cleaveland, S., Cunningham, A.A., deC.Bronsvoort, B. M. and Craig,

C. (2010). Echinococcus. granulosus infection in humans and livestock in the

Coquimbo region, North-central Chile. Veterinary Parasitology. 169: 102-110.



342

Adam, A. (1997). Some epidemiological indicators of the Echinococcosis/ Hydatidosis

infection in dogs, cattle, camels, and man in nyala town, Southern Darfur state,

M. T. A. H, Thesis. University of Khartoum.

Adam, A. (2004). Some epidemiological aspects of Echinococcus granulosus and isolate

characterization in animals in Darfur region, PhD, thesis. University of

Khartoum.

Amer, H. A; Nibal, A. H; Dalal, S. M; Hassan, H. M.(2007). Pathological and serological

studies on cystic echinococcosis in naturally infected camel calves. veterinary

medical journal giza. 55(1): 115-129.

Azlaf, R. and Dakkak, A. (2006). Epidemiological studies of the cystic Echinococcosis in

Morocco. Veterinary Parasitology. 137: 83-93.

Barnes, T. S., Hinds, L. A., Jenkins, D. J., Bielefeldt-Ohmann, H., Lightowlers, M. W.

and Coleman. G. T. (2011). Comparative Pathology of Pulmonary Hydatid Cysts

in Macropods and Sheep. Journal of Comparative Pathology. 144:113-122.

Drury, R. A. B. and Willington, E. A. (1980). Carleton’s histological technique. Fifth

Edition. Oxford University press. London.

Elsawi, A. S. A. (1994). Natural and experimental infection of sheep and goats with

hydatidosis. M. V. Sc, Thesis. University of Khartoum.

Fromsa, A. and Jobre, Y. (2011). Infection prevalence of hydatidosis (Echinococcus

granulosus, Batch, 1786) Asynthesis report of previous reports in domestic

animals in Ethiopia. Ethiopian Veteterinary Journal. 15(2): 11-33.

Hamid, M. H. A. (2012). Pathological studies on hepatic lesions of camel (camelus

dromedaries) slaughtered at Tambool abattoir, Sudan. M. V. M, Thesis.

University of Khartoum.

Keir, H. E., Rosenberg, M. G., Sandberg, J. K., Jordan, K. A., Wiznia, A., Nixon, D. F.,

Stoddart, C. A. and Mc Cune, J. M. (2002). Generation of CD3

CD8 low

T

lymphocytes in the HIV type 1- infected thymus. Journal for Immunology.

169(5): 2788 – 2796.

Khalifa, R. M. A., abdel-rahman, S. M., Monib, M. S. M and Yones, D. A. (2005).

Characteristics of hydatid cyst of camel strain of Echinococcus granulosus in

Assiut. Elminia Medicine Bulletine. 16(1): 202-214.

Kul, O.and Yildiz, K. (2010). Multivesicular cysts in cattle: Characterisation of unusual

hydatid cyst morphology caused by Echinococcus granulosus. Veterinary

Parasitology. 170: 162–166.



343

Lewall, D. B. (1998). Hydatid disease: biology, pathology, imaging and classification.

Clinical Radiology. 52:863-874.

Mohamadin, S. A.and Abdelgadir. A. E. (2011). Study on hydatid cyst infection in

Slaughterhouses in Khartoum state, Sudan. Archives of Applied Science

Research. 3(6):18-23.

Mohammed, N. A. A. (2010). Experimental Hydatidosis in the Sudan: transmission and

natural infection. PhD, Thesis. University of Khartoum.

Naji, A., Le Rond, S., Durrbach, A., Radonne, I. K., Creput, C., Daouya, M., Caumartin,

J., le Maoult, J., Carosella, E. D. and Roues-Freiss, N. (2007). CD3+

Cd4 low

and

CD3+

CD8 low are induced by HLA-G novel periplural blood suppressor T cell

subsets involved in transplant acceptance. Blood.10(12):3969-3948.

Njoroge, E. M., Mbithi, P. M., Gathuma, J. M. Wachira, T. M., Gathura, P. M.,

Magambo, J. K. and Zeyhle, E. (2005). A study of cystic Echinococcosis in

slaughtered animals in three selected areas of northern Turkana, Kenya.

Veterinary Parasitology. 104: 85-91.

Omer, R. A., Dinkel, A., Romig, T., Mackenstedt, U., Elnahas, A. A., Aradaib, I.E.,

Ahmed, M.E., Elmalik , K.H. and Adam , A. (2010). A molecular survey of

cystic echinococcosis in Sudan. Veterinary Parasitology. 169: 340–346.

Osman, A. M. A. (2007). Pathological and biochemical study on hydatid disease in

camels, cattle and sheep. M. V. M, thesis. University of Khartoum.

Ould Ahmed Salem, C. B., Schneegans, F., Chollet, J. Y. and et Jemli, M. H. (2011).

Epidemiological studies on Echinococcosis and characterization of human and

livestock hydatid cysts in Mauritania. Iranian Journal of Parasitology. 6(1): 49-

57.

Pearce, E. J., Caspar, P., Grzych, J. M., Lewis, F. A. and Sher, A. (1991).

Downregulation of Th1 cytokine production accompanies induction of Th2

responses by a parasitic helminth, Schistosoma mansoni. Journal of

Experimental Medicine. 173:159-166.

Pedrosa, I., Saíz, A., Arrazola, J., Ferreirós, J.and Pedrosa, C. S. (2000). Hydatid

Disease: Radiologic and Pathologic Features and Complications. Radio Graphic.

20:795-817.

Pumarola A, Rodriguez-Torres A, García-Rodriguez JA, Piédrola-Angulo G.( 1990).

Microbiología y parasitología médica 2nd ed. Barcelona, Spain: Salvat..

Rashed, A. A., Omer , H. M., Fouad, M. A and Al Shareef , A. M. (2004). The effect of

severe cystic hydatidosis on the liver of a Najdi sheep with special reference to

http://radiographics.rsna.org/search?author1=Iv%C3%A1n+Pedrosa&sortspec=date&submit=Submit

http://radiographics.rsna.org/search?author1=Antonio+Sa%C3%ADz&sortspec=date&submit=Submit

http://radiographics.rsna.org/search?author1=Juan+Arrazola&sortspec=date&submit=Submit

http://radiographics.rsna.org/search?author1=Joaqu%C3%ADn+Ferreir%C3%B3s&sortspec=date&submit=Submit

http://radiographics.rsna.org/search?author1=C%C3%A9sar+S.+Pedrosa&sortspec=date&submit=Submit



344

the cyst histology and histochemistry. Journal of Egyptian Society of

Parasitology. 34(1):297-304.

Saad, M. B. (1985). Hydatidosis/ Echinococcosis in the Sudan with emphasis on

epidemiology, experimental transmission and histopathology. PhD, Thesis.


Sakamoto, T. and Cabrera, P. A. (2003). Immunohistochemical observations on cellular

response in unilocular hydatid lesions and lymph nodes of cattle. Acta Tropica.

85 (2):271-279.

Tola, H. M. (1987). On the sero-epidemiology of hydatid disease. M. Sc, Thesis.


Torgerson, P. R., Ziadinov, I., Aknazarov, D., Nurgaziev, R. and Deplazes, P. (2009).

Modelling the age variation of larval protoscolices of Echinococcus Granulosus

in sheep. International Journal for Parasitology. 39: 1031- 1035.

Verma, Y. and Swamy, M. (2009). Prevalence and pathology of hydatidosis in buffalo

liver. Buffalo Bulletin. 28(4) p. 207-211.

http://journals2.scholarsportal.info/search-advanced.xqy?q=Perla%20A.%20Cabrera&field=AU




(a) pathological, histochemical and immunohistochemical ... · (bbb) generally, in all liver and...

Documents