Pathological Evaluation of Paratuberculosis in Naturally Infected Cattle
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Vet. Patho l. 15: 196 -207 (1978) Pathological Evaluation of Paratuberculosis in Naturally Infected Cattle C. D . BUERGELT , C. HALL, K. McENTEE and J. R . D UNCA N The Theriogeno logy Section, Department of La rge A nimal Medicine , Obstetrics and Surge ry, New Yo rk State College of Veterina ry Medicine, Cornell University, It haca, N .Y . Ab stract. T hirty-two of 51 cattle infected with Mycobacterium paratub erculosis had chro nic e nteriti s , chronic lymphangitis or me senteric lymphade no path y , or all three , at slaughte r. G ran ulom atous inflammatory lesion s were mi ld to ad va nced and predominantly involved the dista l small intestine . Rectal involvement was see n on ly in five ca tt le . Fourteen had microgranulom as in the liver . There were three cytologica l forms o f macrophage s: hist ioc ytic, po lygonal a nd e pithelio id . T he latt er two types had engulfed moderate numbe rs of acid-fast baci lli. T he histiocytic macro phages usua lly were packed with ac id-fast bacilli. Except in th e liver and occasionally its nodes , remote lesio ns of paratuberculosis were no t found in ot her organs. One animal had endocardial a nd ao rtic ca lcifications. Most cattle with signs of diarrhea had glo bule leu kocytes in or around mye nteric ganglio n ce lls . T he thymus of 3- to 8-year-o ld cattle wit h clinical signs frequently had mi ld to advanced involut ion . T he th ym us of sim ila rly aged infected anima ls without clin ica l signs, a nd of paratube rc ulos is-negative animals , had no t involuted. Paratube rc ulosis (Jo hne's disease) , a chro nic infectio us disease of do mes ticated and wild ruminants, has been recognized thro ugho ut the world since it first was described in 1895 . Its ca usative agent is Mycobacterium paratuberculosis, a faculta tive intracellular acid-fast bacterium . T he macroscopic and histologic lesion s of paratuberculosis basically remain confined to the intes tine , mesenteric and ileocaecallymph nodes [7] . A ltho ugh M . paratuberculosis has been cultured from a variety of othe r organs , microscopic lesions have been found only in th e liver [12] . M . paratuberculosis is ass umed to spread primarily via circulati ng macro phages. In the liver th ese macroph ages may become foca lly trapped in sin usoi ds and with lymphocytes may give rise to microgr anulomas. Early inves tiga tors of par atubercul osis emphas ized its similarity to leprosy [3 , 5 , 10] . Bo th diseases are cause d by acid-fas t bacte ria th at are diff icult to culture and have lon g gro wth periods . T he inflamm at ory response in both diseases is similar. Despite invo lvement of different organ syste ms, th e micro scopic lesion s are dom inated by macrophages an d Lan ghan s' gia nt cells . Le prosy has been classified int o two po lar forms - tubercul oid an d leprom at ou s 196 Pathology of Bovine Paratuberculosis 197 leprosy - wit h ma r ked hist ol ogical differe nces [I I] . In tuberculoi d leprosy , the dermal gra nulo ma is co m posed of a well de ve lope d populat ion of epithelioid macr ophages surrounded by dense co lle ctio ns o f small lym phocytes . M . le prae o rganis ms are se ldom fo und by standard me th o ds of examinatio n. T his is in contrast to the sit ua tio n in leproma tous lepro sy in whic h small lym ph ocytes are a bs e nt o r sca nty a nd im ma tur e macrophages a re packed with le pro sy bacilli. In accordance with t he morphologic find ings a re the o bservatio ns o f immuno logic im pa irm e nt in these patie nts [1 4 ]. We ha ve classifie d parat ubercu lous lesio ns in th e in test in al tr act a nd associate d lymph nodes, usin g as a model t he mo rph ol ogic sca le of lepro sy propo sed by Ridley a nd Jopling [II] . Materials and Met hod s Tissues fro m 32 Holstein cows (herd A) and fro m 19 Ang us cattle (herd B) , all infected with M . paratuberculosis, were collected at slaughter. Tissue specimens taken were from the duodenum, jejunum, ileum , ileocaecal valve , caecum , convoluted colon, terminal colo n-rectum (last 30 centimeters anterior to the an us) , mesente ric nodes, ileocaecal node, pharyngeal tonsil. heart , lung, kidney, liver, liver node , mammary gland, supra ma mmary node , thymus, spleen, bronchia l node , ad rena l and uterus. Major fetal orga ns and placental tissues were collected from infect ed pregnant cows. Tiss ues were fixed in 10% buffe red forma lin, embedded in paraffin and sectioned at 6 micrometers. Selected sections were stained with hematoxylin and eos in ( HE) and an acid-fast Zie hl-Neelsen stain. Results T he necropsy a nd mi cro scopic findings of Johnes disease, the rela tive numbers o f acid- fas t bacilli a nd degree o f th ymic in vo lu tion were as shown in tables I, II a nd V . Twenty-two of t he 32 cows in he rd A had gross changes cha racte rist ic of Johne 's di sease (table I) . There were co rr ugatio ns of the m ucosa of th e dista l small in testine a nd prominent mese nt e ric a nd subserosa I lym ph a tics in 17 cows . T we lve had la rge mese nte ric a nd ile ocaeca l lymp h no des . Six cows had loss o f skeletal muscle substance o r atrophy of body fa t or both . Ten ca tt le in he rd B had gross lesions with mucosal thi c kening . O f th ese , three had pro mi ne nt subserosal lym ph a tics a nd two had mesenteric lymp hade nopathy . T he body co nditio n o f two ca tt le was poo r. Extensive a lo pecia was di agnose d in two ot her cattle . One 5-year-old cow (no. 2) had e ndocardial a nd aortic ca lcifica tion s (ta ble II ) . Herd A Hi st o logic lesio ns co m patible wi t h those of pa ra tuberculosis we re graded as mild in nine co ws, mode rat e in 11 a nd ma rke d in 12 . In co ws wit h mi ld lesio ns (class I ) , in divid ual Lan gh an s' gia nt cells usu a lly were detected in th e lamin a propria of intestinal villi (fig . 1) o r scatt e red within th e pa racortical zo ne of mese nte ric nodes . Specific epithe lioid mac rophages were 198 Buergelt et al difficult to identify. Acid-fast baci lli indicative of M . paratuberculosis were see n in o nly on e cow . Co ws with moderate histologic lesion s (class 2) had severa l sma ll gro ups of macrophages or severa l indi vidual Lan ghans' giant cells or both in the lam ina propria of intestin al villi, in th e int estin al submucosa, in the subca ps ular sinus, or in th e par acortical zo ne of regional me senteric nod es. Small agg regates of macrophages were seen in the livers of two cow s. In three cows of cla ss 2 the number of macrophages to giant ce lls was equal; in four cows, macrophages exceede d giant cells; in four other co ws giant ce lls were the predominant ce ll type. Cow 3 had sma ll foci of mineralisation in so me giant cells. Many macrophages and giant ce lls had infiltrated the lamina propria and the submucos a of various seg ments of the small intestine in cows with advanced lesions (class 3) .T hese macro ph ages and giant ce lls also were in the stroma l tissue of the tunica muscularis and in the serosa . T he y filled the subm ucosal, subs erosal and mesenteric lym phatics and partially occluded the lumen. A substantial number of macrophages , giant cell s and lymphocytes surrounded the se lymphatics. T he intestinal villi were short and distorted. C rypta l glands were distended and filled with ne utrophils and mucoid substa nces. Villou s lact eals were prominent becau se of dilation and some contained a few inflammatory cells. Some lacteals had ruptured and fistulati on into the gut lumen had occurred. Peyer's patches were surrounde d by infla mma tory cells, but usuall y were not infiltrated by them . The submucosa was widen ed either by infiltrating inflamm a tory cells or tran sud at e . In 11 cows, the myenteric ga nglion cells of Meissner's plexus eithe r were surro unde d or infiltrated by a few globule leukocytes (fig. 2) . T he gra nulomato us infl ammatory respon se tended to exte nd to th e adjacent mesenteric nodes. A ffere nt lymphatics were distended and infiltrated by macro phages and giant ce lls. T he subcaps ular sinuses were filled with similar cell s. The lymphoid cells within th e par acortical zone largely were replaced by macrophages and giant ce lls .