Assessment of the Morphological Development of the Bursa of Fabricius in Turkey (Meleagris gallopavo

International Journal of Poultry Science 13 (x): xx-xx, 2014ISSN 1682-8356© Asian Network for Scientific Information, 2014

Corresponding Author: O. Nnadozie, Department of Veterinary Anatomy, Michael Okpara University of Agriculture, Umudike, AbiaState, Nigeria

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Assessment of the Morphological Development of the Bursa ofFabricius in Turkey (Meleagris gallopavo)

O. Nnadozie , D.N. Ezeasor , U.C. Nlebedum , E. Ikpegbu and I. Agbakwuru1 2 1 1 1

Department of Veterinary Anatomy, Michael Okpara University of Agriculture, Umudike, Abia State, Nigeria1

Department of Veterinary Anatomy, University of Nigeria, Nsukka2

Abstract: The post hatch (PH) development of the bursa of Fabricius in turkey (Meleagris gallopavo) wasstudied from day (D) 1 to D 140. The shape of the bursa varied significantly with age. Histologically, at D 1PH the bursa in transverse section consisted of high longitudinal mucosal folds whose cores comprisedround follicles organized on both sides of a common axis of connective tissue in a pinnate form. Thesefollicles were dominated by homogeneously distributed lymphocytes. By D 7, polyhedral follicles showed welldifferentiated cortex and medulla with specialized epithelial cells, the corticomedullary arch forming cells(CMAFC), aligned at the corticomedullary border. By D 14, interaction of follicles through the medulla with themodified epithelium was more elaborate. In the medulla of some follicles were pale stained figures thatcontained some reticular and pyknotic cells. Follicles appeared to increase in size and number up to D 63.By D 70, cellular density of follicles appeared reduced and the outline of the CMAFC was thrown into folds.Interfollicular spaces gradually increased with age and by D 140, follicles appeared less dense and themedulla and cortex were less obvious. There were proliferation of fibroblasts and apparent increase infibrous tissue infiltration of the bursal structures. Large interfollicular spaces occupied by connective tissueand follicles with reduced cortical dimensions dominated the plicae.

Key words: Bursa of fabricius, turkey (Meleagris gallopavo), morphology, development

INTRODUCTIONThe avian lymphoid system is structurally divided intotwo distinct components namely, the primary or centraland the secondary or peripheral components (Firth, MATERIALS AND METHODS1977). The primary or central component which One hundred apparently healthy day old turkey poults ofcomprises the bursa of Fabricius and the thymus glandis the primary site for the development of lymphocytes(Ratcliffe, 1989; Ciriaco et al., 2003) that are responsiblefor humoral and cell mediated immune responses,respectively (Silvestein, 2001). The bursa has beenfound to be well developed in sexually immature birds,but undergoes regression or involution at the onset ofsexual maturity (Glick et al., 1956; Payne, 1971). It hasas well been shown that in some breeds of chicken, thebursa of Fabricius had completely disappeared at theage of 196 days (Beach et al., 1934) and in the Pekinducks there was total loss of lymphoid follicles by day154 which left the bursa a fibrous sac (Hashimoto andSugimura, 1976), while in the guinea fowl even at theage of 224 days, the bursa had not completely involutedand was still functionally active (Onyeanusi et al., 1993).Although the development, gross and histologicalstructures of the bursa of Fabricius have been studied inmost avian species, there is still little information on thepost-hatch development of this organ in the turkey(Meleagris gallopavo). Hence, this research is aimed atstudying the age-related morphological changes

associated with the growth of the bursa of Fabricius fromday one post hatch to day 140 of age.

either sex were purchased from Green Hands Agro-VetFarms, Umuahia, Abia State, Nigeria. The birds werehoused and raised in a deep-liter pen in Michael OkparaUniversity of Agriculture, Umudike, Abia State and werefed commercially compounded feed (Topfeed ) and®

water was provided ad libitum. No medication of anykind including vaccination was given throughout thestudy period. The birds were divided into twenty groupsof five birds per group comprising day 1, 7, 14, 21, 28,35, 42, 49, 56, 63, 70, 77, 84, 91, 98, 112, 119, 126, 133and 140. Following the above schedule, five randomlyselected birds were euthanized by inhalationanaesthesia using chloroform soaked in cotton wool ina lid plastic container.The bursa of Fabricius, was collected by ventralabdominal dissection (Alboghobeish and Mayahi, 2003)and examined for gross features.

Histological investigation: Slices of the bursa of differentages were fixed in Bouin’s fluid and transferred to 70%alcohol after 24 h. The specimens were processed byplacing them in ascending grades of alcohol in the

Int. J. Poult. Sci., 13 (x): xx-xx, 2014

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following order, first 95% alcohol for 1 h and second their landmarks well established by strands of loose95% alcohol for 1¼ h, first absolute alcohol for 1½ h andsecond absolute alcohol for 2 h to ensure properdehydration of the tissues. It was then transferred tomixture of equal volumes of alcohol and xylene where itwas left overnight. It was later cleared in two changes ofxylene for 1 h each. It was then infiltrated for 1 h withmolten paraffin wax in the oven at 60°C. The tissueswere embedded in paraffin wax, trimmed and mountedon wooden chuck and then taken to the microtome forsectioning at 5 µm thickness. The sections were floatedin floating-out bath from where it was picked with cleanalbuminized slides. The slides were placed in a stainingdish and excess wax was removed by two changes ofxylene, hydrated by descending grades of alcohol in thefollowing order-absolute alcohol, 95% alcohol and 70%alcohol for 2 min each. The slides were taken to waterand then stained by filtered Ehrlich hematoxylin for 15min and then washed in water for 5 min, differentiated in1% acid alcohol for 3 sec and blued in running tap waterfor 10 min. It was then counter stained with filteredeosine for 2 min. Excess eosine was removed inascending grades of alcohol in the following order-75%alcohol, 95% alcohol and absolute alcohol for 2 mineach. It was then cleared in two changes of xylene andcover slipped with Depex mountant. The slides wereviewed under a light microscope and selected imageswere captured using moticam 2.0 digital cameraattached to a computer.

RESULTSThe shape of the bursa varied significantly with age.Between day 1 post hatch and day 14 of age, the bursawas tubular in shape with a short stalk, but became pearshaped at about day 28. From day 42 to day 140 it wasglobular in shape.Histologically, at day 1 post hatch, the four histologicallayers of the bursal wall were already formed. Themucosa lined by pseudo stratified columnar epitheliumhad formed between 8-12 primary folds of varyingdimensions whose cores were occupied by follicles atdifferent stages of development (Fig. 1). The follicleswere mostly round in shape and containedhomogeneously distributed lymphocytes, some reticularcells and mitotic figures (Fig. 2). Few of the follicles atthis stage had differentiated into a peripheral cortex anda central medulla and within the interfollicular spaceswere diffused accumulations of free lymphocytes,smooth muscle cells, fibroblasts and numerous bloodvessels (Fig. 3). The muscularis consisted of 3 to 4layers of circularly arranged smooth muscle fibers,surrounded by the serosa of loose connective tissuewhose mesothelium was composed of simplesquamous cells.By day 7 post hatch, the mucosal folds and follicles hadincreased in size with a marked increase in follicular celldensities. Most follicles were polyhedral in shape and

interfollicular connective tissue septa that surroundedeach follicle. Points of interaction between the folliclesand the surface epithelium had become moreprominent. The follicles established direct contactsthrough their medulla with the modified follicleassociated epithelium (FAE). At the point of interactionthe cortex was lost and the FAE provided a directconnection between the follicular medulla and the bursallumen. Each follicle at this stage had differentiated intoa peripheral cortex and an inner medulla with the specialepithelial cells known as the cortico-medullary archforming cells (CMAFC), getting aligned at the cortico-medullary border (Fig. 4). The population of theaccumulated cells within the interfollicular spaces andsubepithelial regions had conspicuously reduced.Follicles consisted of denser populations oflymphocytes in the cortex with numerous scatteredepithelial reticular cells with visible nucleoli in themedulla. Plasma cells were equally observed within thelymphocyte population. Also in the medulla of somefollicles were pale stained bodies that contained somepyknotic cells and vacuolated reticular cells. Thisstructure resembled both in appearance andcomposition the irregular pale stained reticular structureof the thymus gland (Fig. 5).By day 14, plicae and follicles had further increased insize with apparent increase in cellular densities. Thecortex was obviously more densely populated withlymphocytes than the medulla and contained also fewhighly euchromatic cells with prominent nucleolisuspected to be the mesenchymal reticular cells. Thearchitecture of the corticomedullary arch forming cells(CMAFC) had equally become more obvious (Fig. 6). Thepseudo stratified columnar surface epithelium consistedof some large nucleated basal cells and in the laminapropria were diffused accumulations of lymphocytes,smooth muscle cells, fibroblasts and strands of looseconnective tissue fibers.Between days 21 and 28, there were no significantdifferences in development. The cortex still stained morebasophilic than the medulla and more blood vesselstraversed the axial connective tissue septa. More follicleshad acquired the eosinophilic reticular structure in theirmedulla. These reticular structures were composed notonly of reticular cells and vacuolated cells but also someaggregates of lymphocytes surrounded by reticular cells(Fig. 7). The follicular cell compositions among theseages were similar both in the cortex and medulla andcomprised mostly small lymphocytes.By day 35, there was further increase in follicle size andcell densities with the cortex still more denselypopulated than the medulla. Small lymphocytesremained predominant, but few giant unidentified cellswith polygonal nuclei were sparsely distributed in boththe cortex and medulla. In the medulla were also cells


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Fig. 1: Photomicrograph of a Transverse Section of the bursa of Fabricius at day 1 post hatch showing the mucosalfolds, P containing follicles, F1 and F2. ARROW: epithelium, BW: bursal wall. X100

Fig. 2: Transverse Section of bursa of Fabricius at day 1 post hatch showing a round follicle surrounded by connectivetissue, S. Note the homogenous distribution of cells in the follicle. RC: Reticular cell, LC: Lymphocyte, MF:Mitotic figure, EPITH: Epithelium. X1000

with deeply basophilic nuclei that were surrounded by columnar epithelium showed apical brush borders,clear cytoplasm suspected to be vacuolated while in the subepithelial regions or more precisely thedegenerating lymphocytes. The pseudo stratified lamina propria were still accumulations of lymphoid


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Fig. 3: Section of bursa of Fabricius at day 1 showing the extra follicular region. Note the lymphocyte, LC: Fibroblast,FB: Reticular cell, RC: Smooth muscle cell, SMC and the blood vessels, BV. X1000

Fig. 4: Section of the bursa at day 7 showing a follicle bounded by the interfollicular septum, IFS. Note the interactionof the follicle with the follicle associated epithelium, FAE and the orientation of the corticomedullary archforming cells (arrow). S: Reticular Structure, C: Cortex, M: Medulla. X400

tissue. The eosinophilic body of the medulla was still There were no significant variations in developmentalcomposed of whorls of reticular cells with prominent changes observed for days 42 and 49. Within thesenucleoli. ages, the follicular cell densities seemed to be uniform,


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Fig. 5: Section of a bursal follicle at day 7 showing the pale stained structure, RS in the medulla. Note the RC:Reticular cells, PKC: Pyknotic cell and VC: Vacuolated cell, within the structure. LC: lymphocyte, C: cortex, M:medulla. X1000

Fig. 6: Section of a bursal follicle at day 14 showing the cortex, C and medulla, M. Note the apparent corticomedullaryarch forming cell (arrow) and the mesenchymal reticular cell, MRC in the cortex. ML: muscle layer. X1000

although the outline of the corticomedullary border heterochromatic lymphocytes, while the medullaremained clearly defined. The follicular cell composition eosinophilic body remained dominated by whorls ofconsisted of dense populations of various sized reticular cells.

CM

VC

PKC

RS

RC


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Fig. 7: Section of the bursa of Fabricius at day 28 showing the reticular structure, S in the medulla. Note the clustersof lymphocytes, LC surrounded by reticular cells (arrow) and the vacuolated cell: VC. X1000

Fig. 8: Transverse Section of the bursal follicle at day 56 showing the eosinophilic reticular structure, S of the medulla.Note the interaction of this structure with the follicle associated epithelium, FAE. X400

By day 56, follicles were separated from one another by eosinophilic reticular structure in the medulla hadfine connective tissue septa and seemed to comprise increased in dimension and in some follicles, itsuniform distribution of cells with inapparent outline of association with the follicle associated epithelium (FAE)corticomedullary border at low magnification. The was clearly defined (Fig. 8).

M

C

EPITH

FAE

S


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Fig. 9: Section of the bursa at day 70 showing part of a follicle. Note the folded outline of the corticomedullary borderand the accumulated cortical cells (arrow) along it. C: Cortex, M: Medulla, EPITH: Epithelium. X400

Fig. 10: Transverse Section of the bursa at day 98 showing the nature of the follicles. Note the extent of invaginationof the cortex, C into the medulla, M and the accumulated adipose tissue, AT in the submucosa. Observe alsothe loose cell density along the interfollicular septa. X100

At day 70, each follicle still showed defined cortex and in most follicles had invaginated into the medulla,medulla, but the outline of the cortico-medullary border thereby giving an increased appearance of thebecame irregular and was thrown into folds. The cortex dimension of the cortex. There was accumulation of


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Fig. 11: Section of the bursa at day 112 showing the follicles. Note the inapparent corticomedullary border (arrow) andthe fibroblast invaded interfollicular connective tissue septa, IFS. C: Cortex, M: Medulla, FB: Fibroblast. X400

Fig. 12: Transverse Section of the bursa at day 140 showing the follicles, F. Note the extent of invasion of the folliclesby connective tissue and the mass of adipose tissue, AT. IFS: Interfollicular sperm, BV: Blood vessel. X40

cortical cells along the axis of the cortico-medullary predominant, although the cortex showed widerborder, which resulted in thickened appearance of intercellular spaces (Fig. 9).the profile of the cortico-medullary arch forming By day 98, there was further in-folding of the cortexcells. Within each follicle small lymphocytes were still into the medulla such that opposite surfaces of the


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Fig. 13: Section of the bursa at day 140 showing part of a follicle. Note the profile of the cortex, C and medulla, M andthe nature of the blood vessels, BV. ARROW: corticomedullary arch forming cell; CT: connective tissue. X400

corticomedullary borders were in close proximity at fibrous tissue infiltration of the bursal structures. Greatersome points in the medulla. The peripheral zones of the proportion of the cortex had been taken over bycortex showed clearer outline along the interfollicular connective tissue due to the invasion of the interfollicularregions due to the existence of wide intercellular regions by fibroblast. Adipose tissue accumulations inspaces, while the septa consisted of thicker bundles of the submucosa had as well prominently increased inconnective tissue fibers. There was also adipose tissue mass (Fig. 12). The subepithelial regions also showedinfiltration in the submucosa. The cortico-medullary arch increased network of connective tissue fibers withforming cells still lined the borders, but showed reduced numerous fibroblast. Although follicular cell densitycortical cell accumulation (Fig. 10). remained reasonable in most follicles, some showedBy day 112, distinction between the cortex and medulla depletion in cell population due to invasion andwas inapparent in most follicles. Also the outline of the displacement of the cortical structures by connectivecortico-medullary arch forming cells was inapparent and tissue. The cortico-medullary arch forming cells stillthe interfollicular septa consisted of thick bundles of lined the corticomedullary borders and the infolding ofconnective tissue fibers with many fibroblasts (Fig. 11). the cortex remained prominent. The cortex in someFollicles remained populated with predominantly small follicles remained apparently the invaginated portion andlymphocytes with some plasma cells, mitotic figures the blood vessels within the interfollicular septaand reticular cells. appeared fibrotic (Fig. 13).By day 133, each follicle showed prominent cortical andmedullary zones with well defined, but still irregularlyoriented cortico-medullary border. The medulla stainedpale while the cortex remained invaginated into themedulla. Adipose tissue infiltration had spread todifferent regions along the common axis of the plicaeand the blood vessels showed thick walls. Thethickness of the bursal wall had obviously increased andconsisted of several layers of circular smooth musclefibers.At day 140, follicles appeared less dense and themedulla and cortex were less obvious. There wereproliferation of fibroblasts and apparent increase in

DISCUSSIONThe anatomical position of the bursa of Fabricius inturkey was similar to those described for chicken(Akter et al., 2006), guinea fowl (Onyeanusi et al., 1993),duck (Glick, 1963) and goose (Jolly, 1915). The shape ofthe bursa varied slightly with age in turkey, but in theadult, the globular shaped bursa as was also describedby Jolly (1915) related much closely to the oval to roundshaped bursa in the chicken (Glick, 1963). In the Pekinduck, the bursa of Fabricius was elongated (Glick,1963), cylindrical in the goose (Jolly, 1915) but varied inshape among adults in guinea fowl. In one group, the


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bursa was reported to appear as an oval sac or had a medulla within a connective tissue envelop. Gulmez andpointed cranial blind end with a bulging mid section inanother group (Onyeanusi et al., 1993).Histological investigations revealed that the bursa ofFabricius in turkey appeared structurally similar to thosedescribed for most avian species. The bursal wall wasmade up of 4 layers. The innermost layer, the mucosawhich was thrown into folds was lined by predominantlypseudo stratified columnar epithelium without gobletcells as reported in broiler chicken (Akter et al., 2006)and White Pekin duck (Indu et al., 2005), but in contrastto the pseudo stratified columnar epithelium with gobletcells in the guinea fowl (Onyeanusi et al., 1993) andgoose (Gulmez and Aslan, 1999). Payal et al. (2010)observed an age variation in form of the bursalepithelium in Vanaraja and Cari breeds of chicken.According to them, the epithelium was simple columnarin chicks and layers, while pseudo stratified columnar ingrowers. The epithelium in turkey as reported in otheravian species comprised both the interfollicularepithelium (IFE) of pseudo stratification and the moremodified follicle associated epithelium (FAE). There wasalso a basal layer of cuboidal cells in the surfaceepithelium as was found in chicken, whose function isunknown but could be a predestined interfollicularepithelial cells (IFEC), since the surface epithelium doesnot proliferate and no epithelial stem cell has beenidentified (Olah and Vervelde, 2008). Although in one ofhis reports, Hodges (1974) stated that there were threedefinitive types of surface epithelial cells in the chicken,which included some oval, round nucleated cells withP.A.S positive cytoplasmic granules suspected to bethese basal cells, but their functions were not as wellmentioned.Variations were also recorded in the number andstructure of the mucosal folds of the bursa. In the turkey,there were 8-12 primary folds that projected into thebursal lumen. Ackerman and Knouff (1959) observed11-13 such folds in chicken, while Onyeanusi et al.(1993) recorded about 12-13 folds in the guinea fowl. Inthe White Pekin duck, Indu et al. (2005) observed 2 largewell developed folds on the ventral aspect and about 5-6smaller folds all round the circumference, while in thegoose, there were about 11-12 folds (Gulmez and Aslan,1999). The immunological significance of the structureand number of these mucosal folds has not been clearlydefined, but there could be a correlation betweenimmune competence of the bursa of Fabricius and thenumber of folds associated with it; since the functionalunits (follicles) of the bursa are located within these fold,hence the higher the number of folds the greater thenumber of follicles and the immune competent cells.The structural architecture of the bursal follicles in turkeywas similar to those already described for most studiedavian species (Honjo and Hirota, 1993; Onyeanusi et al.,1993). It comprised a lymphocyte dominated stroma thatwas differentiated into a peripheral cortex and central

Aslan (1999) reported that some bursal follicles in thegoose were in direct contact with the bursal epitheliumwhile others were completely surrounded by connectivetissue. Similar observation was made in this study inturkey, but Olah and Velverde (2008) stated that eachbursal follicle is attached to the epithelium through thefollicle associated epithelium (FAE), so the number offollicle associated epithelial attachments is identical tothe number of follicles. Therefore, the observation thatsome follicles were completely surrounded byconnective tissue may have resulted from the plain ofsectioning which might have excluded the points ofattachment of these follicles with the epithelium.Development of bursal follicles seemed relatively slowin turkey and chicken compared to the guinea fowl. Atday 1 post hatch in turkey, follicle formation is still inprogress. Most regions of the plicae still containeddiffused accumulations of lymphocytes that were not yetincorporated into follicles and only few of the alreadyformed follicles had differentiated into cortex andmedulla. Similar findings were made in chicken wherethe first cortical cells appeared around hatching and thecortex only fully developed by day 14 post hatch (Pikeet al., 2004; Ratcliffe, 2006). But in guinea fowl, by day 1post hatch the plicae were filled with follicles (Onyeanusiet al., 1993), although no mention on the extent ofdevelopment of these follicles was made. Speciesvariation rather than incubation period could be thereason for the disparity in development since the turkeyshares almost the same incubation period with theguinea fowl.The eosinophilic structure in the medulla that wascomposed of whorls of reticular cells, somedegenerated cell, vacuolated cells and few lymphocytesin some cases in the turkey had also been described insome other species. In the guinea fowl, Onyeanusi et al.(1993) described it as a collection of reticular epithelialcells with the total exclusion of lymphocytes andmacrophages, while Gulmez and Aslan (1999)described it as a group of some healthy reticular cellswith P.A.S. positive stained cells with degenerated nucleiwhose cytoplasm were totally or locally vacuolated in thegoose. This structure was observed as early as day 7post hatch in turkey, but was first mentioned in guineafowl at about day 77. Though the significance of thisstructure had not been established, its anatomicalpeculiarity to the diffused form of the Hassall’scorpuscles of the thymus gland raised the opinion thatit may be involved in the turnover of epithelial reticularcells as proposed for the Hassall’s corpuscle.Invagination of the cortex into the medulla or moreprecisely the folding of the cortico-medullary border andthe accumulation of cortical cells along this border asobserved from day 70 suggested a possibleconservative measure for cortical structures, since therewas gradual displacement of the cortex by connectivetissue in later ages.


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Involution characteristics in bursa of Fabricius became Gulmez, N. and S. Aslan, 1999. Histological andevidenced after day 133 in turkey and by day 140 it wasvery pronounced. In comparison, involution of the bursastarted a little earlier in turkey than in guinea fowl whereit started at day 154 (Onyeanusi and Onyeanusi, 1990),but later when compared with the period of involution inmost breeds of chicken.Although the cortex had lost a reasonable proportion ofits structures to connective tissues in most follicles byday 140 in the turkey, the population of follicularlymphocytes was still high. Investigations showed thatin some breeds of chicken, the bursa of Fabricius hadcompletely disappeared at the age of 196 days (Beachet al., 1934) and in the Pekin ducks there was total lossof lymphoid follicles by day 154 which left the bursa afibrous sac (Hashimoto and Sugimura, 1976), while inthe guinea fowl even at the age of 224 days, the bursahad not completely involuted and was still functionallyactive (Onyeanusi et al., 1993).Although the period of investigation in this study did notgo beyond 140 days, the bursa in turkey had obviouslystarted involuting by this age but still very activeconsidering the amount of cell in the follicles; but furtherinvestigation beyond day 140 is needed to ascertain thefate of the bursa of Fabricius in much older turkey.

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Assessment of the Morphological Development of the Bursa of Fabricius in Turkey (Meleagris gallopavo

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