comparative anatomical, morphometric and histological studies of

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7 J.Anat.Soc. India 55 (1) Comparative Anatomical, Morphometric and Histological Studies of theTricuspid Valve-Complex in Human and Some Mammalian Hearts Mohamed A.B. Motabagani Department of Anatomy, College of Medicine, King Faisal University, Dammam, Saudi Arabia. Introduction : The human right atrioventricular (A V) valve is still described, by anatomists and clinicians, as tricuspid. The majority of the human tricuspid valves (62%) are reported to possess three well demarcated leaflets, some (30%) have two leaflets, and others (8%) are formed of four leaflets (Sutton et al. 1995). During conservative dissection of hearts in infants, Gerola et al. (2001) found that the cusps in the right A V valve were two to four in number and the finding of three cusps: anterior, posterior and septal was the commonest. In tricuspid valves with four cusps, the extra cusp was mentioned to be located anterolaterally. The structure of the leaflets of the human tricuspid valve has been infrequently verified in the literature (Harasaki et al. 1978; Lamers et al. 1995; Paelinck et al. 1998; Haroun et al. 1999 b). Anomalies of the tricuspid valve have been the target of several investigations. Congenital duplication of the human tricuspid valve with obstruction of the right ventricular outflow tract is determined by echo cardiography to be a rare heart anomaly (Bisognano et al. 1998). Accessory valve tissue is also a rare congenital cardiac anomaly that exists either alone or in association with other cardiac malformations as Fallot's tetralogy, transposition of the great vessels, ventricular septal defects, and coarctation of the aorta (Yoshimura et al. 2000). Ebstein's abnormality is the commonest anomaly of the tricuspid valve and it presents either alone or occasionally with other syndromes (Khan & Cohen, 1999). In Ebstein's malformation, the septal and posterior leaflets of the tricuspid valve are not attached to the valve annulus but displaced downwards leading to distal shift of the functional orifice into the right ventricle (Frescura et al. 2000). Accurate knowledge of the morphology and morphometry of the tricuspid valve is mandatory for differentiation between functional and organic tricuspid regurgitation (Grondin et al. 1967). Organic impairment of the tricuspid valve is reported to be encountered in 10-15% of rheumatic valve diseases (Gunied et al. 1989). Tricuspid valve regurgitation in man may result from severe annular dilatation of the valve without any organic or congenital disease affecting the valve leaflets (Aoyagi et al. 1999). A relation between the body weight as an extracardiac parameter and the diameter of the tricuspid valve as an intracardiac parameter was demonstrated, by Francalanci et al. (1998), in children aged one day to 14 years. Functional regurgitation through one or more of the cardiac valves could be also demonstrated in healthy young athletes and not in healthy sedentary individuals (Macchi et al. 2001). Severe tricuspid regurgitation may also result from a congenital cleft in the anterior leaflet of the valve associated with a patent foramen ovale (Motoyoshi et al. 2001, Okutan et al. 2002). Abstract : Ten postmortem hearts (five males and five females) of each of human, and Arabian camel, sheep and monkey have been utilized in this study for comparative gross examination, light microscopy and morphometric assessment of the different elements of the tricuspid valve-complex. The valve orifice was triangular and bordered by three leaflets in all species investigated. Clefts were identified in some human and animal leaflets. Supernumerary and perforated leaflets were not recognized. The total annular length of the tricuspid valve was insignificantly increased in camel but decreased in sheep and monkey, when compared to human. The human and animal tricuspid leaflets were similar in structure, and the lamina fibrosa of the animal leaflets looked thicker than the fibrous core of human leaflets. Characteristic fine folds of the human anterior leaflet, and of the camel and sheep leaflet parietalis were observed and their significance was proposed. The subendothelial elastic fibres and the wavy collagenous bundles noticed at the atrial aspect of the human tricuspid leaflets were functionally correlated. Blood vessels, but no muscle fibres, were identified in the basal parts of some human and animal leaflets. The structure of the chordae tendineae and papillary muscles was basically the same in all species. The wavy course of the chordal collagenous bundles imparts more extensibility to the chordae. A characteristic myotendineous transition was observed at the papillary apices in sheep and monkey. The present study reveals the similarities and dissimilarities between the human tricuspid valves and those of some mammals; this would be useful for further comparative investigations. This study also recommends the possibility of choice of any of these animal valve tissues for elaboration of tissue-engineered valve elements or the use of the whole of the biological prosthesis in human tricuspid valve replacement. Key words : comparative; tricuspid valve; man; camel; sheep; monkey; anatomy; morphometry; light microscopy. 1-23 (2006)

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Page 1: Comparative Anatomical, Morphometric and Histological Studies of

7J.Anat.Soc. India 55 (1)

Comparative Anatomical, Morphometric and Histological Studies oftheTricuspid Valve-Complex in Human and Some Mammalian HeartsMohamed A.B. MotabaganiDepartment of Anatomy, College of Medicine, King Faisal University, Dammam, Saudi Arabia.

Introduction :The human right atrioventricular (A V) valve is still

described, by anatomists and clinicians, as tricuspid.The majority of the human tricuspid valves (62%) arereported to possess three well demarcated leaflets,some (30%) have two leaflets, and others (8%) areformed of four leaflets (Sutton et al. 1995). Duringconservative dissection of hearts in infants, Gerola etal. (2001) found that the cusps in the right A V valvewere two to four in number and the finding of threecusps: anterior, posterior and septal was thecommonest. In tricuspid valves with four cusps, theextra cusp was mentioned to be located anterolaterally.The structure of the leaflets of the human tricuspidvalve has been infrequently verified in the literature(Harasaki et al. 1978; Lamers et al. 1995; Paelinck etal. 1998; Haroun et al. 1999 b).

Anomalies of the tricuspid valve have been thetarget of several investigations. Congenital duplicationof the human tricuspid valve with obstruction of theright ventricular outflow tract is determined by echocardiography to be a rare heart anomaly (Bisognano etal. 1998). Accessory valve tissue is also a rarecongenital cardiac anomaly that exists either alone orin association with other cardiac malformations asFallot's tetralogy, transposition of the great vessels,ventricular septal defects, and coarctation of the aorta(Yoshimura et al. 2000). Ebstein's abnormality is thecommonest anomaly of the tricuspid valve and it

presents either alone or occasionally with othersyndromes (Khan & Cohen, 1999). In Ebstein'smalformation, the septal and posterior leaflets of thetricuspid valve are not attached to the valve annulusbut displaced downwards leading to distal shift of thefunctional orifice into the right ventricle (Frescura et al.2000).

Accurate knowledge of the morphology andmorphometry of the tricuspid valve is mandatory fordifferentiation between functional and organic tricuspidregurgitation (Grondin et al. 1967). Organic impairmentof the tricuspid valve is reported to be encountered in10-15% of rheumatic valve diseases (Gunied et al.1989). Tricuspid valve regurgitation in man may resultfrom severe annular dilatation of the valve without anyorganic or congenital disease affecting the valve leaflets(Aoyagi et al. 1999). A relation between the body weightas an extracardiac parameter and the diameter of thetricuspid valve as an intracardiac parameter wasdemonstrated, by Francalanci et al. (1998), in childrenaged one day to 14 years. Functional regurgitationthrough one or more of the cardiac valves could bealso demonstrated in healthy young athletes and notin healthy sedentary individuals (Macchi et al. 2001).

Severe tricuspid regurgitation may also result froma congenital cleft in the anterior leaflet of the valveassociated with a patent foramen ovale (Motoyoshi etal. 2001, Okutan et al. 2002).

Abstract : Ten postmortem hearts (five males and five females) of each of human, and Arabian camel, sheep andmonkey have been utilized in this study for comparative gross examination, light microscopy and morphometric assessmentof the different elements of the tricuspid valve-complex. The valve orifice was triangular and bordered by three leaflets in allspecies investigated. Clefts were identified in some human and animal leaflets. Supernumerary and perforated leafletswere not recognized. The total annular length of the tricuspid valve was insignificantly increased in camel but decreased insheep and monkey, when compared to human. The human and animal tricuspid leaflets were similar in structure, and thelamina fibrosa of the animal leaflets looked thicker than the fibrous core of human leaflets. Characteristic fine folds of thehuman anterior leaflet, and of the camel and sheep leaflet parietalis were observed and their significance was proposed.The subendothelial elastic fibres and the wavy collagenous bundles noticed at the atrial aspect of the human tricuspidleaflets were functionally correlated. Blood vessels, but no muscle fibres, were identified in the basal parts of some humanand animal leaflets. The structure of the chordae tendineae and papillary muscles was basically the same in all species. Thewavy course of the chordal collagenous bundles imparts more extensibility to the chordae. A characteristic myotendineoustransition was observed at the papillary apices in sheep and monkey. The present study reveals the similarities anddissimilarities between the human tricuspid valves and those of some mammals; this would be useful for further comparativeinvestigations. This study also recommends the possibility of choice of any of these animal valve tissues for elaboration oftissue-engineered valve elements or the use of the whole of the biological prosthesis in human tricuspid valve replacement.

Key words : comparative; tricuspid valve; man; camel; sheep; monkey; anatomy; morphometry; light microscopy.

1-23 (2006)

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The chordae tendineae, according to theirattachment to the A V valves, are classified into types:free edge, marginal zone, basal, cleft and commissuralchordae (Silver et al. 1971~ Williams et al. 1995~Sinnatamby, 1999). The ultrastructure of the chordaetendineae of the normal human tricuspid valve wasreported by some authors (Lim, 1980~ Keller et al. 1999).Nigri et al. (2001) estimated the number of the humanchordae tendineae at their origin from the papillarymuscles of the right ventricle as follows: 1-11 from theanterior muscle, 1-8 from the posterior muscle, and 1-5 from the septal muscle.

The papillary muscles of the human right ventricleare described to be three in number. The anterior andposterior muscles were found in all autoptic specimensinvestigated by Nigri et al. (2001) while the septalpapillary muscle was absent in 21.5% of heartsexamined. Each of the reported anterior and posteriorpapillary muscles possessed 1-4 heads.

Comparative investigations of the tricuspid valve-complex in man and animals have proved to be usefulnot only for academic purposes but also for selectionof the appropriate valve tissue suitable for valvularbioprosthesis in man. Primary valve replacement ofthe tricuspid valve is preferred to valve repair inextensive tricuspid valve destruction as a result ofacute endocarditis (Lange et al. 1996). Few studiesdealing with the detailed anatomy, structure andmorphometry of the A V valve- complexes in animalsare available in the literature (Harasaki et al. 1975, Icardoet al. 1993, Munro et al. 1995, Hayashi et al. 1996,Haroun et al. 1999 a&b, Maish et al. 2003, Nozynski etal. 2003).

Aim of the WorkThe aim of the present work is to describe, in detail,

the morphology, morphometry and structure of thetricuspid valve in man and in some animals like Arabiancamel, sheep and monkey. This study will reveal theaspects of similarity and dissimilarity between thesespecies. The anatomical description of the rightatrioventricular valve in these animals will be of greathelp for academic comparative studies. The study willalso offer a valuable guidance for clinicians regardingthe possibility of utilization of any of these animal valvesas a bioprosthesis in human tricuspid valvereplacement.

Materials and MethodsA total of 40 apparently healthy adult hearts were

enrolled in this work; 10 hearts (five male and fivefemale) of each of the following species: human,

Arabian camel (Camelus Dromedarius), Arabian Naimisheep (Ovis Aries), and Arabian Baboon monkey (papioHamadryas). The human hearts were obtained from thepostmortem room, College of Medicine, King FaisalUniversity, Dammam, KSA and their ages ranged from35 to 55 years. The camel and sheep hearts wereretrieved from A1- Dammam Slaughter House, KSAimmediately after sacrifice. The Baboon monkeys (aged17-20 years and weighing 10-16 kg) were hunted fromthe Southern Province of Saudi Arabia, anaesthetizedand sacrificed by ether and thiopental, and their heartswere then excised. The sheep hearts were obtainedfrom animals aged 4-5 years and weighing 22-25 kgwhile the camels were aged 18-20 years and weighed300-350 kg.

In each heart, the right atrium and ventricle wereincised along their right lateral walls, the walls werecarefully retracted, and the interior was thoroughlywashed with saline. The tricuspid valve was then openedby cutting through the annulus fibrosus and the anteriorleaflet of the human hearts or the angular leaflet of theanimal hearts. The tricuspid valve-complex wasexamined, photographed in situ, and then excised outof the heart to be morphologically studied and againphotographed. The presence of clefts, commissures,cusp scallops, and extra leaflet tissue was looked forand reported.

In each heart of each species group, themeasurements of the different components of thetricuspid valve-complex were determined before andafter excision of the valve using fine caliper, non-stretchable nylon thread and flexible metric ruler. Allmeasurements obtained were recorded, tabulated andsubjected to statistical analysis using SPSS programand Chi Square test for comparison. Thesemeasurements included:1- The total annular length of the valve.2- The annular length of each leaflet.3- The height of each leaflet, being measured from

the middle of its base at the annulus fibrosus tothe middle of its free edge. When scallops wereidentified in a leaflet, the sum and mean of theirheights were considered.

4- The annular length and height of each commissure.5- The length (and number) of the different types of

the chordae tendineae.In each species, two excised tricuspid valve-

complexes were chosen to get portions of theircomponents including annulus fibrosus, leaflets,chordae tendineae, tips of papillary muscles, and smallparts of adjacent atrial and ventricular walls. The excisedelements were fixed in 10 % formol saline, routinely

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processed for paraffin- blocks, sectioned at 7 µm,stained with haematoxylin and eosin, Masson'strichrome, as well as orcein stains, examined by thelight microscope and then photographed.

ResultsA. The Morphological studyAl. The tricuspid valve-complex in Man (Fig. 1) The

Leaflets and Commissures:Gross examination of the human tricuspid valve

showed that it possessed a triangular orifice boundedby the free margins of three leaflets: anterior, posteriorand septal.

The anterior leaflet was always ( 100% ) the largest,triangular and devoid of clefts. The posterior leaflet wasthe second in size and also triangular .It had either noclefts in two hearts (20% ) or a single cleft in theremaining human hearts (80%). When there was a cleft,the posterior leaflet was divided into a major scalloptowards the anteroposterior commissure and a minorscallop towards the posteroseptal commissure.

The septal leaflet of the human tricuspid valve wassemicircular along its free edge and always ( 100% )divided by a cleft into two unequal scallops of whichthe larger was located nearer to the anteroseptalcommissure .

Three commissures were observed to intervenebetween the three leaflets of the human tricuspid valve:anteroposterior, posteroseptal and anteroseptal. Theclefts and commissures were grossly identified by theattachment of the fan-shaped ramification of the cleftand commissural chordae tendineae. The anteroposteriorand posteroseptal commissures received commissuralchordae originating from the medial most apex of theanterior and posterior papillary muscles respectively.The anteroseptal commissure received chordae thatarose from one of the masses of the septal papillarymuscle or directly from the septal wall of the rightventricle.

The Papillary Muscles of the Right Ventricle:Inspection of the interior of the human right ventricle

revealed the presence of three papillary muscles:anterior, posterior and septal. The anterior papillarymuscle was always the largest in the form of a biapicalsingle-based conical belly. The base of the anteriormuscle was attached to the sternocostal wall of theright ventricle within its lower one-third.

The posterior papillary muscle of the humantricuspid valve-complex was the second muscle in sizeand also in the form of a biapical single belly. It arosefrom about the middle of the diaphragmatic wall of theright ventricle close to the interventricular septum. Mostof the chordae tendineae arose from the apices butfew from the sides of the anterior and posterior papillarymuscles. The chordae from the anterior papillary musclegot attached to the anterior and posterior leaflets aswell as to the anteroposterior commissure while thosearising from the posterior papillary muscle wereattached to the posterior and septal leaflets as well asto the posteroseptal commissure.

The septal papillary muscle was formed of smallconical masses, some uniapical and others biapical;all were tethered to the interventricular septum. Thechordae tendineae originated from the apices of thesemasses and from the septal wall of the ventricle aswell and they gained attachment to the septal andanterior leaflets, and the anteroseptal commissurebetween them.

Apart from smaller size of the heart and its valvesin females, no more magnificent morphological sex-differences were observed in the human tricuspid valve-complex.

Fig. 1: A photograph of the interior of the human right ventricle ofan adult male, showing a cleft (thick arrow) in the triangularposterior leaflet (PL) of the tricuspid valve dividing it into alarger scallop (1) towards the anteroposterior commissure(a pc) and a smaller scallop (2) towards the posteroseptalcommissure (psc). The septal leaflet (SL) is semicircularand divided by a cleft (thin arrow) into a smaller scallop (a)towards the posteroseptal commissure and a largerscallop (b) towards the anteroseptal commissure (asc).The anterior leaflet (AL) of the valve is divided by dissectioninto two parts. The anterior papillary muscle (APM) is formedof a biapical single conical belly cut at its base and thenlongitudinally split by dissection while the septal papillarymuscle (SPM) is formed of two conical masses: one isuniapical and the other is biapical, attached to theinterventricular septum (IVS). The posterior papillarymuscle (PPM) is seen attached to the diaphragmaticsurface of the ventricle. Note the septomarginal trabecula(SMT) and the fan-shaped branching of the commissuraland cleft chordae tendineae.

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A2. The tricuspid valve-complex in Camel (Figs. 2-4)The Leaflets and Commissures: The camel tricuspid

valve also had a triangular orifice bordered by the freemargins of three leaflets named: the "leaflet angularis",the "leaflet parietalis" and the "leaflet septalis",according to the nomenclature reported for otheranimals in the literature (Sisson & Grossman, 1975).

The leaflets angularis and parietalis of the cameltricuspid valve were triangular in outline while the leafletseptalis was semicircular along its free margin (Figs.2-4). The leaflet angularis looked to be the largest ofthe three leaflets in all camel hearts examined (100%)while the leaflet observed to be next in size was theleaflet septalis in six camel hearts (60% ) and the leafletparietalis in the remaining four hearts (40%). In all camelhearts investigated (100%), the leaflet angularis didnot show clefts.

The leaflet parietalis showed no clefts in two outof ten camel hearts examined (20%, Fig. 2), singlecleft in other two hearts (20%, Fig. 3), and double cleftsin the remaining six hearts (60%, Fig. 4). The singlecleft, when present, was located nearer to theparietoseptal commissure (Fig. 3). When there weredouble clefts, the leaflet parietalis was divided into threescallops of which the middle one was the largest (Fig.4).

The leaflet septalis of the camel tricuspid valveshowed either two clefts in seven hearts (70%) dividing

Fig. 2: A photograph of the tricuspid valve-complex of an adultfemale camel, showing two clefts (straight arrows) dividingthe semicircular leaflet septalis (LS) into three scallops(a,b&c) of which the middle one (b) is the smallest. Themuscle papillaris magnus (MPM) is a biapical mass beingsevered at its base (curved arrow) by dissection. Themuscle papillaris parvi (MPP) is a uniapical single bellyattached to the interventricular septum (IVS) at a moredistal level than that of the muscle papillaris subarteriosus(MPS). Note the septomarginal trabeculs (SMT), the leafletsangularis (LA) and parietalis (LP) devoid of clefts, thecommissures: anguloparietal ( apc ), parietoseptal (psc)and anguloseptal ( asc ), and the fan-shaped ramificationof the commissural and cleft chordae tendineae.

Fig.3: A photograph of the tricuspid valve-complex of an adultfemale camel, showing the biapical single-based musclepapillaris magnus (MPM) attached to the lateral wall of theright ventricle. The muscles papillaris parvi (MPP) andsubarteriosus (MPS) are attached to the interventricularseptum (IVS). The leaflet parietalis (LP) is divided by acleft (straight arrow) into two scallops (a&b) of which thesmaller (b) lies towards the parietoseptal commissure(psc). Note the septomarginal trabecula (SMT), the leafletsangularis (LA) and septalis (LS) devoid of clefts, and thefan-shaped commissural ( curved arrows) and cleftchordae tendineae.

Fig. 4: A photograph of the tricuspid valve-complex of an adultmale camel, showing two clefts (thick arrows) dividing thetriangular leaflet parietalis (LP) into three scallops (1,2&3)of which the middle one (2) is the largest. Another cleft(thin arrow) divides the semicircular leaflet septalis (LS)into a smaller scallop (a) towards the parietoseptalcommisure (psc) and a larger one (b) towards theanguloseptal commissure (asc). The leaflet angularis (LA)and the biapical single-based muscle papillaris magnus(MPM) are divided by dissection. The muscle papillarisparvi (MPP) is a biapical single conical belly attached toabout the middle of the interventricular septum (IVS). Themuscle papillaris subarteriosus (MPS) is formed of smallmuscular knobs tethered to the interventricular septumwithin its upper one- third. Note the septomarginal trabecula(SMT) and the fan-shaped ramification of the commissuraland cleft chordae tendineae.

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No evident morphological features were observedas sex-related differences in the tricuspid valve-complex of the camel heart.

A3. The tricuspid valve-complex in Sheep (Figs. 5&6)The Leaflets and Commissures: The orifice of the

sheep tricuspid valve was nearly triangular having threeleaflets named in the same way as those of the cameltricuspid valve but they looked smaller and thinner. Theleaflets angularis and parietalis were triangular in shape,nearly of the same size, and devoid of clefts while theleaflet septalis was always (100%) the largest,semicircular along its central margin, and showing clefts(Figs. 5&6).

The leaflet septalis showed one cleft in each of allsheep hearts examined (100%). The cleft was nearerto either the anguloseptal commissure in three hearts(30%, Fig. 5) or the parietoseptal commissure in theremaining sheep hearts (70%, Fig. 6).

Three commissures were observed to intervenebetween the three leaflets of the sheep valve. Thecommissures and clefts were also identified by the fan-shaped branching chordae tendineae. Theanguloparietal, parietoseptal and anguloseptalcommissures received their chordae from the apicesof the muscles papillaris magnus, parvi andsubarteriosus respectively (Figs. 5&6).

the leaflet into three scallops of which the middle oneis the smallest (Fig. 2) or one cleft nearer to theparietoseptal commissure in two hearts (20%, Fig. 4).In one camel heart (10%), the leaflet septalispossessed no clefts (Fig. 3).

Three commissures were interposed as a junctionaltissue between the leaflets of the camel tricuspid valve:anguloparietal, parietoseptal and anguloseptalcommissures (Figs. 2-4). The commissures and cleftswere identified by the fan- shaped mode of branchingof the commissural and cleft chordae tendineae. Theanguloparietal and parietoseptal commissures receivedcommissural chordae tendineae arising from themedialmost apices of the muscles papillaris magnusand parvi respectively (Figs. 2-4). The anguloseptalcommissure gained commissural cordae tendineaeoriginating from the apex of one of the masses of themuscle papillaris subarteriosus and/or from the septalwall of the ventricle in addition (Figs. 2-4).

The Papillary Muscles of the Right Ventricle: Threepapillary muscles were identified in the camel rightventricle and they were named according to the reportednomenclature for animals (Nickel et al. 1981): themuscle papillaris magnus, the muscle papillaris parviand the muscle papillaris subarteriosus (Figs. 2-4).

The muscle papillaris magnus, the largest andlongest, was always demonstrated as a biapical singlebelly attached to about the middle of the right lateralwall of the ventricle. Chordae tendineae arose mostlyfrom the apices and to a lesser extent from one side ofthe muscle (Figs. 2-4). These chordae gainedattachment into the leaflets angularis and parietalis,and the anguloparietal commissure in between (Fig. 4).

The muscle papillaris parvi, being smaller andshorter than the former, was observed as either auniapical (20%, Fig. 2) or a biapical (80%, Fig.4) singleconical belly attached, by its base, to the interventricularseptum variably below the parietoseptal commissure(Figs. 2-4). The chordae arose from the apices and sidesof the muscle to be attached to the leaflet parietalis,leaflet septalis and parietoseptal commissure (Figs. 2-4).

The muscle papillaris subarteriosus was thesmallest in the form of multiple small and short musclemasses attached to the interventricular septum belowthe anguloseptal commissure and at a more proximallevel than that of the muscle papillaris parvi (Figs. 2&4).The chordae arose from both the apices of thesemuscle masses and the interventricular septum to beinserted into the leaflet septalis, leaflet angularis andanguloseptal commissure (Figs. 2-4).

Fig. 5: A photograph of the interior of the right half of the heart ofan adult male sheep, showing the triangular leafletsangularis (LA) and parietalis (LP) of the tricuspid valvedevoid of clefts. The leaflet septalis (LS) is the largest,semicircular and divided by a cleft (straight arrow) into alarger scallop (a) towards the parietoseptal commissure(psc) and a smaller one (b) towards the anguloseptalcommissure (asc). The biapical muscle papillaris magnus(MPM) is cut at its base (curved arrow) then longitudinallybisected. The muscle papillaris parvi (MPP) appears as abiapical single belly attached to the interventricular septum(IVS) at a more distal level than that of the muscle papillarissubarteriosus. Note the septomarginal trabecula (SMT)and the fan-shaped commissural and cleft chordaetendineae.

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The Papillary Muscles of the Right Ventricle: Thethree papillary muscles of the sheep right ventricle werenamed in the same way like those of the camel. Themuscle papillaris magnus was constantly ( 100% ) inthe form of a biapical single conical belly attached tothe middle one- third of the ventral wall of the rightventricle and sending its chordae to the leaflets angularisand parietalis, and the anguloparietal commissure aswell (Figs. 5&6).

The muscle papillaris parvi was also a biapicalsingle belly attached to the septal wall of the ventricledistal to the parietoseptal commissure. It sent itschordae to the leaflets parietalis and septalis, and theparietoseptal commissure in between (Figs. 5&6).

The muscle papillaris subarteriosus was thesmallest in the form of multiple short muscular knobstethered to the interventricular septum distal to theanguloseptal commissure but more proximal than theseptal attachment of the parvi muscle (Figs. 5&6). The

chordae arose from the pointed apices of these knobsand from the septum itself to be received into theanguloseptal commissure and the leaflet tissue on eachside.

The morphology of the tricuspid valve-complex ofthe sheep heart was the same in both sexes.

A4. The tricuspid valve-complex in Monkey (Fig. 7)The Leaflets and Commissures: The monkey

tricuspid valve had a triangular orifice guarded bymarkedly thin three leaflets. The leaflet angularis wasthe largest while the parietalis was the smallest. Theleaflets angularis and parietalis were triangular in shapewhile the leaflet septalis was semicircular. The leafletsangularis and septalis showed no clefts.

The leaflet parietalis of the monkey heart showedeither no clefts in three hearts (30%) or a single cleft inseven hearts (70%). The cleft divided this leaflet into amajor scallop towards the anguloparietal commissureand a minor scallop towards the parietoseptalcommissure.

Fig. 6 : A photograph of the interior of the right half of the heart ofan adult female sheep, showing the biapical andlongitudinally bisected muscle papillaris magnus (MPM),the biapical muscle papillaris parvi (MPP), and the musclepapillaris subarteriosus as small muscular knobs ( curvedarrows) tethered to the interventricular septum (IVS). Theleaflet septalis (LS) is semicircular and it shows a cleft(straight arrow) that divides it into a smaller scallop (a)towards the parietoseptal commissure (psc) and a largerscallop (b) towards the anguloseptal commissure (asc).Note the leaflet parietalis (LP), the two dissected parts ofthe leaflet angularis (LA), and the septomarginal trabecula(SMT).

Fig. 7: A photograph of the interior of the right half of the heart ofan adult male monkey, showing the annulus fibrosus (AF)of the tricuspid valve divided by dissection at the triangularleaflet angularis (LA) and also at the semicircular leafletseptalis (LS) near the anguloseptal commissure (asc).The leaflet parietalis (LP) is also triangular in shapeexhibiting a cleft (arrow) that divides it into a larger scallop(a) towards the anguloparietal commissure (a pc) and asmaller scallop (b) towards the parietoseptal commissure(psc). The uniapical single-bellied muscle papillaris magnus(MPM) is attached to the ventral wall of the right ventricle.The muscle papillaris parvi (MPP) is composed of atriapical muscle mass attached to the distal part of theinterventricular septum (IVS). Some chorda-likeconnections are observed between the bases of thepapillary muscles parvi and magnus. The muscle papillarissubarteriosus (MPS) appears as small muscular knobsprojecting from the interventricular septum within itsproximal one-third. The septomarginal trabecula (SMT,raised on a green rod) is also shown.

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Three commissures were seen between the threeleaflets of the monkey tricuspid valve. Theanguloparietal commissure received commissuralchordae tendineae from the apices of the musclepapillaris parvi, the parietoseptal commissure from themuscle papillaris subarteriosus, and the anguloseptalcommissure from the apex of the muscle papillarismagnus. The commissures were identified by the fan-shaped pattern of ramifying chordae tendineae.

The Papillary Muscles of the Right Ventricle: Themuscle papillaris magnus of the monkey wasdemonstrated as a uniapical single belly attached tothe anterior (ventral) wall of the right ventricle within itsdistal one-third. The chordae arose from its apex to bedirected towards the leaflets angularis and septalis,and the anguloseptal commissure.

The muscle papillaris parvi was a triapical musclemass attached to the distal one-third of the septal wallof the ventricle. Its apices gave chordae tendineae tothe leaflets angularis and parietalis, and to theanguloparietal commissure.

The muscle papillaris subarteriosus was composedof small, short and ill- developed muscular projectionsthat were adherent to the interventricular septum within

Fig. 8: A,B,C&D: Photographs of excised and pinned out tricuspid valve- complexes of man (A), camel (B), sheep (C) and monkey (D),showing the annulus fibrosus (AF) receiving the attachment of the bases of the three leaflets of each valve: anterior (AL) orangularis (LA), posterior (PL) or parietalis (LP), and septal (SL) or septalis (LS). The three papillary muscles are demonstrated:anterior (APM) or muscle papillaris magnus (MPM), posterior (PPM) or muscle papillaris parvi (MPP), and septal (SPM) ormuscle papillaris subarteriosus (MPS). The different types of chordae tendineae are also shown: free edge (1), rough marginalzone (2), basal zone (arrows), commissural (3), and cleft (4) chordae. The septomarginal trabecula (SMT) and the interventricularseptum (IVS) are noted.

its proximal one-third. The apices of these musclemasses and the interventricular septum gave rise tochordae tendineae that gained attachment to theleaflets septalis and parietalis, and the parietoseptalcommissure.

The Chordae tendineae of the Tricuspid Valve (Figs.8: A,B, C&D) : The chordae tendineae of the tricuspidvalve, in all species investigated, originated from theapices and sides of the papillary muscles. In the animalvalves, few chordae in addition arose directly from theinterventricular septum. The tricuspid valve chordaewere of commissural and leaflet types. The leafletchordae tendineae were observed to be of four types,according to the sites of their attachment to the leaflets:free edge, rough marginal zone, basal zone and cleftchordae. The free edge, rough zone and basal zonechordae were coarse primary or they showed furthersecondary ramifications before gaining attachment tothe free margin, rough zone on the ventricular surfaceof the leaflets close to their free margins, and the basalzone on the ventricular surface of the leaflets close tothe annulus fibrosus of the valve; respectively. The cleftand commissural chordae tendineae exhibited acharacteristic fan-shaped mode of fine secondary and

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tertiary ramifications before gaining attachment to theclefts of the leaflets and commissural areas of the valve.

B. The Morphometric study (Tables 1-14)The mean values of the different measurements

of the human tricuspid valve leaflets revealedinsignificant sex-differences except for the total leafletannular length, and the heights of the posterior andseptal leaflets that showed significantly lower valuesin females than in males (Table 1).

Table 1: Measurments of the leaflets of the human tricuspid valvein both sexes.

*P <0.05=Significant

The number of the chordae tendineae arising fromthe posterior papillary muscle of the human right ventricleshowed significantly lower mean value in females thanin males. The chordal length exhibited significantlyhigher female mean values of the human septal leafletrough zone chordae and anteroposterior commissuralchordae. The rest of the human chordal number andlength values showed insignificant differences relatedto sex (Table 2).

In animal species investigated, insignificant sex-differences were detected regarding the measurementsof the leaflets of the tricuspid valve except for the totalleaflet annular length of the camel and monkey valvesthat showed significantly higher mean values infemales than in males. The number of the chordaearising from the muscle papillaris parvi in each of thecamel and monkey showed significantly lower femalevalues. The number of the leaflet chordae in sheeprevealed significantly higher female values regardingthe leaflet angularis basal zone chordae, and the leafletsparietalis and septalis free edge chordae. The leafletsparietalis and septalis basal zone chordae as well as

Table 2: The number and length of the different chordac tendineaeof the human tricuspid valve in both sexes.

*P <0.05=Significant

the anguloseptal commissural chordae of the sheepshowed significantly lower number in females. The restof the animal valve values presented insignificant sex-differences (Tables 3-8).

Comparing the measurements of man and animaltricuspid leaflets, there was a significant increase inthe annular length of the leaflet angularis, height of theleaflet parietalis, and heights of the anguloseptal andparietoseptal commissures in camel than those of theirhomologues in man (Table 9). The leaflet angularis

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Table 3: Measurments of the leaflets of the camel tricuspid valvein both sexes.

*P <0.05=Significant

Table 4: The number and length of the different chordae tendineaeof the camel tricuspid valve in both sexes.

*P <0.05=Significant

Table 5: Measurments of the leaflets of the sheep tricuspid valvein both sexes.

*P <0.05=Significant

Table 6: The number and length of the different chordae tendineaeof the sheep tricuspid valve in both sexes.

*P <0.05=Significant

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Table 7: Measurments of the leaflets of the monkey tricuspidvalve in both sexes.

*P <0.05=Significant

Table 8: The number and length of the different chordae tendineaeof the monkey tricuspid valve in both sexes.

*P <0.05=Significant

Table 9: Measurments of the leaflets of the tricuspid valve in manand camel.

Table 10: Measurments of the leaflets of the tricuspid valve inman and sheep.

*P < 0.05 = Significant** Camel names corresponding to those of human.

*P < 0.05 = Significant** Sheep names corresponding to those of human.

annular length and height, and the anguloparietalcommissural height showed significantly lower meanvalues in sheep than in man (Table 10). The heights ofthe leaflets parietalis and septalis, and of the three

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commissures had significantly lower values in monkeythan in man (Table 11 ).

The number of the camel chordae was significantlydecreased at all of the three papillary muscles and mostof the leaflets but significantly increased at theanguloparietal commissure, when compared with thenumber of homologous chordae in man. The length ofthe camel chordae attached to the leaflet septalis roughand basal zones, and the anguloseptal commissuredisplayed significantly higher mean values than thoseof human counter chordae (Table 12).

In sheep, there was a significant decrease in thenumber of the chordae arising from the musclespapillaris magnus and subarteriosus, and the chordaeattached to the leaflet angularis basal zone and freeedge, and the leaflet septalis basal zone~ whencompared to human chordae. The numbers of the leafletseptalis free edge chordae and anguloparietalcommissural chordae in sheep showed significantlyhigher mean values than those of the correspondinghuman chordae. The mean lengths of the sheep leafletsparietalis and septalis rough zone chordae showedsignificant decrease while the mean lengths of the leafletseptalis basal zone chordae and anguloparietalcommissural chordae showed significant increase, whencompared to their corresponding values in man (Table13).

Table 11: Measurments of the leaflets of the tricuspid valve inman and monkey.

*P < 0.05 = Significant** Monkey names corresponding to those of human.

Table 12: The number and length of the different chordaetendineae of the tricuspid valve in man and camel.

*P <0.05 = Significant** Camel names corresponding to those of human.

In monkey, when compared to man, there was asignificant decrease in the number of chordae tendineaearising from all of the three papillary muscles, and of

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Table 13: The number and length of the different chordaetendineae of the tricuspid valve in man and sheep.

*P <0.05 = Significant** Camel names corresponding to those of human.

the chordae attached to the rough and basal zones ofthe leaflets angularis and septalis, the basal zone andfree edge of the leaflet parietalis, and the anguloparietal

*P <0.05 = Significant** Monkey names corresponding to those of human.

Table 14: The number and length of the different chordaetendineae of the tricuspid valve in man and monkey.

commissure. The mean number of the leaflet angularisfree edge chordae and the anguloseptal commissural

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Fig. 9

Fig. 10

Fig. 11

Figs.9-15 : Photomicrographs of the anterior (Figs. 9-11),posterior (Figs. 12&13), and septal (Fig. 14) leaflets of the humantricuspid valve, showing a fibrous core (F.C.) of collagenousbundles enclosed between two endothelial layers. The endotheliumat atrial aspect (A) of the anterior leaflet shows fine folds (shortthin arrows). The collagenous fibres are packed in the centre ofthe leaflets, arranged in wavy parallel bundles (long thin arrows)near the atrial surface, and loosely disposed near the ventricularsurface (V) of the leaflets being converging towards the sites of

chordae in monkey was significantly increased thanthat of the corresponding chordae in man. The meanlength of the leaflet angularis rough zone chordae aswell as that of anguloseptal and anguloparietalcommissural chordae in monkey was significantlyshorter than in man. The mean lengths of the monkeyleaflet angularis free edge chordae, leaflet parietalisbasal zone and free edge chordae, and parietoseptalcommissural chordae were significantly longer thanthose of man (Table 14).

C. The histological study:C1. The tricuspid valve-complex in Man (Figs. 9-15)

Light microscopic examination of the leaflets ofthe human tricuspid valve

showed that each leaflet was formed of anendothelial fold enclosing a core of much collagenousbundles and few elastic fibres (Figs. 9-14). Theendothelium covering the atrial surface of the anteriorleaflet characteristically revealed fine folds orcorrugations that extended along this surface in aproximo-distal direction (Figs. 9& 10). The collagenousfibres were condensed in the centre of the leaflet butloosely disposed beneath the atrial and ventricularsurface endothelium. They were arranged into wavybundles that ran parallel with the base-to-apex axis ofthe leaflet near its atrial aspect and they were obliquelyor irregularly disposed towards the ventricular aspectof the leaflet (Figs. 9-11). At the sites of attachmentsof the chordae tendineae to the ventricular surface ofthe leaflets, the chordal connective tissue fibres mergedfreely into the subendothelial connective tissue of theleaflets (Fig. 10). The elastic fibres were scarce andconfined to the subendothelial zone particularly that ofthe atrial surface of the leaflet (Fig. 11&12). The leafletcore was thicker at the peripheral basal margin of theleaflet and tapering towards its central free margin (Figs.12-14). Blood capillaries and small blood vessels werenoticed at the basal portions of the posterior and septalleaflets (Figs. 12-14). Muscle fibres could not bedemonstrated in the human tricuspid leaflets.

Histological examination of cross sections of thechordae tendineae of the human tricuspid valverevealed that they were mostly rounded but slightlyoval near their attachments. They were ensheathed witha layer of endothelium, and were composed of densebundles of collagenous fibres and scarce elastic fibres(Fig. 13).

The papillary muscles of the human right ventriclewere observed to be exactly similar, in structure, tothe cardiac muscle. They were formed of parallel andbranching muscle fibres, each possessed one to twonuclei and an increased amount of cytoplasm (Fig. 15).

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chordal attachments (short thick arrows). Few elastic fibres (darkbrown in figs. 11&12) are seen in the subendothelium of the atrialsurface of the leaflets. Blood vessels (B .V. ) are observed in thebasal parts of the both posterior and septal leaflets. A chordaetendinea (Ch. T. ) is seen formed of dense collagenous fibressurrounded by endocardium (Fig. 13). A longitudinal section of ahuman papillary muscle (Fig. 15) shows that is formed of paralleland branching myocardial fibres; each has one to two nuclei andabundant cytoplasm.

Fig. 12

Fig. 13

Fig. 14

Fig. 16

Figs. (9 & 14): H & E, X40; Figs. (10 & 13): Masson's trichrome,X40; Figs. (11 & 12): Orcein, X40; Fig. (15): H & E, X100.

C2. The tricuspid valve-complex in Camel (Figs. 16-22)Each of the leaflets of the camel tricuspid valve

was formed of two layers of endothelium enclosing thelamina fibrosa that was composed of closely packedbundles of collagenous fibres (Figs. 16-20). Theendothelial covering of the atrial surface of the camelleaflet parietalis showed fine folds imparting it acharacteristic festooned appearance (Fig. 18). Thelamina fibrosa was thicker at the base of the leafletand it tapered towards the apex of the leaflet. At thebase of the leaflet, the lamina fibrosa merged with thesubendocardial collagenous tissue of the atrial andventricular walls (Fig. 18). At both the atrial andventricular surfaces of the lamina fibrosa, thecollagenous fibres were loosely disposed forming theatrialis and ventricularis zones respectively (Figs. 16-20). In most of its parts, the ventricularis was thickerthan the atrialis (Figs. 17-20). Few elastic fibres wereidentified in the subendothelial loose tissue of the cameltricuspid leaflets particularly at their atrial surfaces(Figs. 16,18&20). Blood vessels were observed at the

Fig. 15

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Fig. 17

Fig. 18

Fig. 19

Fig. 20

bases of the leaflets parietalis and septalis (Figs.18&20). No muscle fibres could be identified within thecamel leaflets.

The camel papillary muscles (Fig. 21) and chordaetendineae (Fig. 22) were exactly similar in structure totheir human homologues (Figs. 13&15).

Figs. (16-22) Photomicrographs of the leaflets angularis(Figs. 16&17), parietalis (Fig.18), and septalis (Figs. 19&20) of thecamel tricuspid valve, showing the lamina fibrosa (L.F .) of densecollagenous fibres enclosed between two endothelial layers. Thelamina is seen to be continuous with the subendocardial tissue ofthe cardiac wall (Fig. 18). The atrialis (A) and ventricularis (V) arezones of loosely arranged collagenous fibres bounding the atrialand ventricular surfaces of the lamina fibrosa respectively. Theventricularis is mostly thicker as it receives the attachments (thick

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C3. The tricuspid valve-complex in Sheep (Figs. 23-28)Microscopy of the leaflets, chordae, and papillary

muscles of the sheep (Figs. 23- 28) proved to be similarto those of the camel. Blood vessels were detected inthe leaflets angularis (Fig. 23) and septalis (Fig. 26).The sheep papillary muscles (Fig. 27) displayed similarstructure to those of human and camel. An obviousmyotendineous transitional zone was observed at theapices of the sheep papillary muscles (Fig. 27).

Figs. (23-28): Photomicrographs of the leaflets angularis (Fig.23), parietalis (Figs. 24&25), and septalis (Fig. 26) of the sheeptricuspid valve, showing the lamina fibrosa (L.F.), atrialis (A) andventricularis (V) of each leaflet. The lamina fibrosa is continuouswith the subendocardial connective tissue (long thin arrows) ofthe ventricular wall (Figs. 24&25). The ventricularis looks thickerat the sites (short thick arrows) of chordal attachments (Figs. 24-26). The atrial endothelium of the leaflet parietalis shows fine folds(short thin arrows, Fig. 24). Blood vessels (B.V.) are observednear the bases of the leaflets angularis and septalis (Figs. 23&26).Longitudinal sections of the chordae tendineae ( Ch. T .) showedtheir constitution of wavy bundles of many collagenous fibres andfew elsatic fibres; all surrounded by! endocardium (Figs. 23,27&28).A longitudinal section of a sheep papillary muscle (PM, Fig. 27)displays a structure similar to that of each of human and camel

Fig. 21

Fig. 22

arrows) of the leaflet chordae tendineae (Ch.T.). The endotheliumof the atrial surface of the leaflet parietalis shows the fine festoons(thin arrows in Fig. 18). Blood vessels (B .V. ) are observed in thebasal parts of the leaflets parietalis and septalis (Figs. 18&20).Few elastic fibres (dark brown in figs. 16,18&20) are seen in thesubendothelium at the atrial surface of the leaflets. A camel papillarymuscle (Fig. 21 ) and a chorda tendinea (Ch. T., Fig. 22) are similarin structure to those of human (Figs. 13&15). Figs. (16, 18,20 &22): Orcein, X40; Figs. (17 & 19): H& E, X40; Fig. (21): H& E, X100.

Fig. 23

Fig. 24

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Fig. 25

Fig. 26

Fig. 27

Fig. 28

and, in addition, an obvious myotendineous transitional zone wasobserved at the papillary apex.

Figs. (23, 24 & 26): H & E, X40; Fig. (25): Masson's trichrome,X40; Fig. (27): Orcein, X40; Fig. (28): Masson's trichrome, X100.

C4. The tricuspid valve-complex in Monkey (Figs. 29-35)The leaflets, chordae and papillary muscles of the

monkey tricuspid valve (Figs. 29-34) were consistentlysimilar, in structure, to those of the other three speciesinvestigated although they proved to be markedly

smaller and thinner. Blood vessels (B. v. ) were seen inthe basal parts of the leaflets angularis (Fig. 30) andparietalis (Fig. 31 ). The apical myotendineous transitionof the monkey papillary muscles was also clearlyshowing (Fig. 34).

Figs. (29-35): Photomicrographs of the leaflets angularis (Figs.29&30), parietalis (Figs. 31&32), and septalis (Fig. 33) of the

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