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Journal of the Anatomical Society of India

Comparative Anatomical, Morphometric and Histological Studies of the Tricuspid Valve-Complex in Human and Some Mammalian Hearts

Author(s): Mohamed A.B. Motabagani

Vol. 55, No. 1 (2006-01 - 2006-07)

Department of Anatomy, College of Medicine, King Faisal University, Dammam, Saudi Arabia

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.

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).

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

The papillary muscles of the human right ventricle are described to be three in number. The anterior and posterior muscles were found in all autoptic specimens investigated by Nigri et al. (2001) while the septal papillary muscle was absent in 21.5% of hearts examined. Each of the reported anterior and posterior papillary muscles possessed 1-4 heads. Comparative investigations of the tricuspid valvecomplex in man and animals have proved to be useful not only for academic purposes but also for selection of the appropriate valve tissue suitable for valvular bioprosthesis in man. Primary valve replacement of the tricuspid valve is preferred to valve repair in extensive tricuspid valve destruction as a result of acute endocarditis (Lange et al. 1996). Few studies dealing with the detailed anatomy, structure and morphometry of the A V valve- complexes in animals are available in the literature (Harasaki et al. 1975, Icardo et al. 1993, Munro et al. 1995, Hayashi et al. 1996, Haroun et al. 1999 a&b, Maish et al. 2003, Nozynski et al. 2003).

Aim of the Work

The aim of the present work is to describe, in detail, the morphology, morphometry and structure of the tricuspid valve in man and in some animals like Arabian camel, sheep and monkey. This study will reveal the aspects of similarity and dissimilarity between these species. The anatomical description of the right atrioventricular valve in these animals will be of great help for academic comparative studies. The study will also offer a valuable guidance for clinicians regarding the possibility of utilization of any of these animal valves as a bioprosthesis in human tricuspid valve replacement.

Materials and Methods

A total of 40 apparently healthy adult hearts were enrolled in this work; 10 hearts (five male and five female) of each of the following species: human, Arabian camel (Camelus Dromedarius), Arabian Naimi sheep (Ovis Aries), and Arabian Baboon monkey (papio Hamadryas). The human hearts were obtained from the postmortem room, College of Medicine, King Faisal University, Dammam, KSA and their ages ranged from 35 to 55 years. The camel and sheep hearts were retrieved from A1- Dammam Slaughter House, KSA immediately after sacrifice. The Baboon monkeys (aged 17-20 years and weighing 10-16 kg) were hunted from the Southern Province of Saudi Arabia, anaesthetized and sacrificed by ether and thiopental, and their hearts were then excised. The sheep hearts were obtained from animals aged 4-5 years and weighing 22-25 kg while the camels were aged 18-20 years and weighed 300-350 kg.

In each heart, the right atrium and ventricle were incised along their right lateral walls, the walls were carefully retracted, and the interior was thoroughly washed with saline. The tricuspid valve was then opened by cutting through the annulus fibrosus and the anterior leaflet of the human hearts or the angular leaflet of the animal hearts. The tricuspid valve-complex was examined, photographed in situ, and then excised out of the heart to be morphologically studied and again photographed. The presence of clefts, commissures, cusp scallops, and extra leaflet tissue was looked for and reported.

In each heart of each species group, the measurements of the different components of the tricuspid valve-complex were determined before and after excision of the valve using fine caliper, nonstretchable nylon thread and flexible metric ruler. All measurements obtained were recorded, tabulated and subjected to statistical analysis using SPSS program and Chi Square test for comparison. These measurements 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 to the middle of its free edge. When scallops were identified in a leaflet, the sum and mean of their heights 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 valvecomplexes were chosen to get portions of their components including annulus fibrosus, leaflets, chordae tendineae, tips of papillary muscles, and small parts of adjacent atrial and ventricular walls. The excised elements were fixed in 10 % formol saline, routinely processed for paraffin – blocks, sectioned at 7 Ám, stained with haematoxylin and eosin, Masson’s trichrome, as well as orcein stains, examined by the light microscope and then photographed.

Results

A. The Morphological study

Al. 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 bounded by the free margins of three leaflets: anterior, posterior and septal.

The anterior leaflet was always ( 100% ) the largest, triangular and devoid of clefts. The posterior leaflet was the second in size and also triangular .It had either no clefts in two hearts (20% ) or a single cleft in the remaining human hearts (80%). When there was a cleft, the posterior leaflet was divided into a major scallop towards the anteroposterior commissure and a minor scallop towards the posteroseptal commissure.

Fig. 1: (Unavailable) A photograph of the interior of the human right ventricle of an adult male, showing a cleft (thick arrow) in the triangular posterior leaflet (PL) of the tricuspid valve dividing it into a larger scallop (1) towards the anteroposterior commissure (a pc) and a smaller scallop (2) towards the posteroseptal commissure (psc). The septal leaflet (SL) is semicircular and divided by a cleft (thin arrow) into a smaller scallop (a) towards the posteroseptal commissure and a larger scallop (b) towards the anteroseptal commissure (asc). The anterior leaflet (AL) of the valve is divided by dissection into two parts. The anterior papillary muscle (APM) is formed of a biapical single conical belly cut at its base and then longitudinally split by dissection while the septal papillary muscle (SPM) is formed of two conical masses: one is uniapical and the other is biapical, attached to the interventricular septum (IVS). The posterior papillary muscle (PPM) is seen attached to the diaphragmatic surface of the ventricle. Note the septomarginal trabecula (SMT) and the fan-shaped branching of the commissural and cleft chordae tendineae.

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

Three commissures were observed to intervene between the three leaflets of the human tricuspid valve: anteroposterior, posteroseptal and anteroseptal. The clefts and commissures were grossly identified by the attachment of the fan-shaped ramification of the cleft and commissural chordae tendineae. The anteroposterior and posteroseptal commissures received commissural chordae originating from the medial most apex of the anterior and posterior papillary muscles respectively.

The anteroseptal commissure received chordae that arose from one of the masses of the septal papillary muscle or directly from the septal wall of the right ventricle.

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 papillary muscle was always the largest in the form of a biapical single-based conical belly. The base of the anterior muscle was attached to the sternocostal wall of the right ventricle within its lower one-third.

The posterior papillary muscle of the human tricuspid valve-complex was the second muscle in size and also in the form of a biapical single belly. It arose from about the middle of the diaphragmatic wall of the right ventricle close to the interventricular septum. Most of the chordae tendineae arose from the apices but few from the sides of the anterior and posterior papillary muscles. The chordae from the anterior papillary muscle got attached to the anterior and posterior leaflets as well as to the anteroposterior commissure while those arising from the posterior papillary muscle were attached to the posterior and septal leaflets as well as to the posteroseptal commissure.

The septal papillary muscle was formed of small conical masses, some uniapical and others biapical; all were tethered to the interventricular septum. The chordae tendineae originated from the apices of these masses and from the septal wall of the ventricle as well and they gained attachment to the septal and anterior leaflets, and the anteroseptal commissure between them.

Apart from smaller size of the heart and its valves in females, no more magnificent morphological sexdifferences were observed in the human tricuspid valve complex.

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 free margins of three leaflets named: the “leaflet angularis”, the “leaflet parietalis” and the “leaflet septalis”, according to the nomenclature reported for other animals in the literature (Sisson & Grossman, 1975).

The leaflets angularis and parietalis of the camel tricuspid valve were triangular in outline while the leaflet septalis was semicircular along its free margin (Figs. 2-4). The leaflet angularis looked to be the largest of the three leaflets in all camel hearts examined (100%) while the leaflet observed to be next in size was the leaflet septalis in six camel hearts (60% ) and the leaflet parietalis in the remaining four hearts (40%). In all camel hearts investigated (100%), the leaflet angularis did not show clefts.

The leaflet parietalis showed no clefts in two out of ten camel hearts examined (20%, Fig. 2), single cleft in other two hearts (20%, Fig. 3), and double clefts in the remaining six hearts (60%, Fig. 4). The single cleft, when present, was located nearer to the parietoseptal commissure (Fig. 3). When there were double clefts, the leaflet parietalis was divided into three scallops of which the middle one was the largest (Fig. 4).

The leaflet septalis of the camel tricuspid valve showed either two clefts in seven hearts (70%) dividing the leaflet into three scallops of which the middle one is the smallest (Fig. 2) or one cleft nearer to the parietoseptal commissure in two hearts (20%, Fig. 4). In one camel heart (10%), the leaflet septalis possessed no clefts (Fig. 3).

Fig. 2: (Unavailable) A photograph of the tricuspid valve-complex of an adult female camel, showing two clefts (straight arrows) dividing the semicircular leaflet septalis (LS) into three scallops (a,b&c) of which the middle one (b) is the smallest. The muscle papillaris magnus (MPM) is a biapical mass being severed at its base (curved arrow) by dissection. The muscle papillaris parvi (MPP) is a uniapical single belly attached to the interventricular septum (IVS) at a more distal level than that of the muscle papillaris subarteriosus (MPS). Note the septomarginal trabeculs (SMT), the leaflets angularis (LA) and parietalis (LP) devoid of clefts, the commissures: anguloparietal ( apc ), parietoseptal (psc) and anguloseptal ( asc ), and the fan-shaped ramification of the commissural and cleft chordae tendineae.

Fig.3: (Unavailable) A photograph of the tricuspid valve-complex of an adult female camel, showing the biapical single-based muscle papillaris magnus (MPM) attached to the lateral wall of the right ventricle. The muscles papillaris parvi (MPP) and subarteriosus (MPS) are attached to the interventricular septum (IVS). The leaflet parietalis (LP) is divided by a cleft (straight arrow) into two scallops (a&b) of which the smaller (b) lies towards the parietoseptal commissure (psc). Note the septomarginal trabecula (SMT), the leaflets angularis (LA) and septalis (LS) devoid of clefts, and the fan-shaped commissural ( curved arrows) and cleft chordae tendineae.

Fig. 4: (Unavailable) A photograph of the tricuspid valve-complex of an adult male camel, showing two clefts (thick arrows) dividing the triangular 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 parietoseptal commisure (psc) and a larger one (b) towards the anguloseptal commissure (asc). The leaflet angularis (LA) and the biapical single-based muscle papillaris magnus (MPM) are divided by dissection. The muscle papillaris parvi (MPP) is a biapical single conical belly attached to about the middle of the interventricular septum (IVS). The muscle papillaris subarteriosus (MPS) is formed of small muscular knobs tethered to the interventricular septum within its upper one- third. Note the septomarginal trabecula (SMT) and the fan-shaped ramification of the commissural and cleft chordae tendineae.

Three commissures were interposed as a junctional tissue between the leaflets of the camel tricuspid valve: anguloparietal, parietoseptal and anguloseptal commissures (Figs. 2-4). The commissures and clefts were identified by the fan- shaped mode of branching of the commissural and cleft chordae tendineae. The anguloparietal and parietoseptal commissures received commissural chordae tendineae arising from the medialmost apices of the muscles papillaris magnus and parvi respectively (Figs. 2-4). The anguloseptal commissure gained commissural cordae tendineae originating from the apex of one of the masses of the muscle papillaris subarteriosus and/or from the septal wall of the ventricle in addition (Figs. 2-4).

The Papillary Muscles of the Right Ventricle: Three papillary muscles were identified in the camel right ventricle and they were named according to the reported nomenclature for animals (Nickel et al. 1981): the muscle papillaris magnus, the muscle papillaris parvi and the muscle papillaris subarteriosus (Figs. 2-4). The muscle papillaris magnus, the largest and longest, was always demonstrated as a biapical single belly attached to about the middle of the right lateral wall of the ventricle. Chordae tendineae arose mostly from the apices and to a lesser extent from one side of the muscle (Figs. 2-4). These chordae gained attachment into the leaflets angularis and parietalis, and the anguloparietal commissure in between (Fig. 4). The muscle papillaris parvi, being smaller and shorter than the former, was observed as either a uniapical (20%, Fig. 2) or a biapical (80%, Fig.4) single conical belly attached, by its base, to the interventricular septum variably below the parietoseptal commissure (Figs. 2-4). The chordae arose from the apices and sides of the muscle to be attached to the leaflet parietalis, leaflet septalis and parietoseptal commissure (Figs. 2- 4).

The muscle papillaris subarteriosus was the smallest in the form of multiple small and short muscle masses attached to the interventricular septum below the anguloseptal commissure and at a more proximal level than that of the muscle papillaris parvi (Figs. 2&4). The chordae arose from both the apices of these muscle masses and the interventricular septum to be inserted into the leaflet septalis, leaflet angularis and anguloseptal commissure (Figs. 2-4).

No evident morphological features were observed as sex-related differences in the tricuspid valvecomplex 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 three leaflets named in the same way as those of the camel tricuspid valve but they looked smaller and thinner. The leaflets angularis and parietalis were triangular in shape, nearly of the same size, and devoid of clefts while the leaflet 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 all sheep hearts examined (100%). The cleft was nearer to either the anguloseptal commissure in three hearts (30%, Fig. 5) or the parietoseptal commissure in the remaining sheep hearts (70%, Fig. 6). Three commissures were observed to intervene between the three leaflets of the sheep valve. The commissures and clefts were also identified by the fanshaped branching chordae tendineae. The anguloparietal, parietoseptal and anguloseptal commissures received their chordae from the apices of the muscles papillaris magnus, parvi and subarteriosus respectively (Figs. 5&6)

Fig. 5: (Unavailable) A photograph of the interior of the right half of the heart of an adult male sheep, showing the triangular leaflets angularis (LA) and parietalis (LP) of the tricuspid valve devoid of clefts. The leaflet septalis (LS) is the largest, semicircular and divided by a cleft (straight arrow) into a larger scallop (a) towards the parietoseptal commissure (psc) and a smaller one (b) towards the anguloseptal commissure (asc). The biapical muscle papillaris magnus (MPM) is cut at its base (curved arrow) then longitudinally bisected. The muscle papillaris parvi (MPP) appears as a biapical single belly attached to the interventricular septum (IVS) at a more distal level than that of the muscle papillaris subarteriosus. Note the septomarginal trabecula (SMT) and the fan-shaped commissural and cleft chordae tendineae.

Fig. 6: (Unavailable) A photograph of the interior of the right half of the heart of an adult female sheep, showing the biapical and longitudinally bisected muscle papillaris magnus (MPM), the biapical muscle papillaris parvi (MPP), and the muscle papillaris subarteriosus as small muscular knobs ( curved arrows) tethered to the interventricular septum (IVS). The leaflet 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 larger scallop (b) towards the anguloseptal commissure (asc). Note the leaflet parietalis (LP), the two dissected parts of the leaflet angularis (LA), and the septomarginal trabecula (SMT).

The Papillary Muscles of the Right Ventricle: The three papillary muscles of the sheep right ventricle were named in the same way like those of the camel. The muscle papillaris magnus was constantly ( 100% ) in the form of a biapical single conical belly attached to the middle one- third of the ventral wall of the right ventricle and sending its chordae to the leaflets angularis and parietalis, and the anguloparietal commissure as well (Figs. 5&6).

The muscle papillaris parvi was also a biapical single belly attached to the septal wall of the ventricle distal to the parietoseptal commissure. It sent its chordae to the leaflets parietalis and septalis, and the parietoseptal commissure in between (Figs. 5&6).

The muscle papillaris subarteriosus was the smallest in the form of multiple short muscular knobs tethered to the interventricular septum distal to the anguloseptal commissure but more proximal than the septal attachment of the parvi muscle (Figs. 5&6). The chordae arose from the pointed apices of these knobs and from the septum itself to be received into the anguloseptal commissure and the leaflet tissue on each side.

The morphology of the tricuspid valve-complex of the 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 by markedly thin three leaflets. The leaflet angularis was the largest while the parietalis was the smallest. The leaflets angularis and parietalis were triangular in shape while the leaflet septalis was semicircular. The leaflets angularis and septalis showed no clefts.

The leaflet parietalis of the monkey heart showed either no clefts in three hearts (30%) or a single cleft in seven hearts (70%). The cleft divided this leaflet into a major scallop towards the anguloparietal commissure and a minor scallop towards the parietoseptal commissure.

Fig. 7: (Unavailable) A photograph of the interior of the right half of the heart of an adult male monkey, showing the annulus fibrosus (AF) of the tricuspid valve divided by dissection at the triangular leaflet angularis (LA) and also at the semicircular leaflet septalis (LS) near the anguloseptal commissure (asc). The leaflet parietalis (LP) is also triangular in shape exhibiting a cleft (arrow) that divides it into a larger scallop (a) towards the anguloparietal commissure (a pc) and a smaller 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 a triapical muscle mass attached to the distal part of the interventricular septum (IVS). Some chorda-like connections are observed between the bases of the papillary muscles parvi and magnus. The muscle papillaris subarteriosus (MPS) appears as small muscular knobs projecting from the interventricular septum within its proximal one-third. The septomarginal trabecula (SMT, raised on a green rod) is also shown.

Three commissures were seen between the three leaflets of the monkey tricuspid valve. The anguloparietal commissure received commissural chordae tendineae from the apices of the muscle papillaris parvi, the parietoseptal commissure from the muscle papillaris subarteriosus, and the anguloseptal commissure from the apex of the muscle papillaris magnus. The commissures were identified by the fanshaped pattern of ramifying chordae tendineae.

The Papillary Muscles of the Right Ventricle: The muscle papillaris magnus of the monkey was demonstrated as a uniapical single belly attached to the anterior (ventral) wall of the right ventricle within its distal one-third. The chordae arose from its apex to be directed towards the leaflets angularis and septalis, and the anguloseptal commissure.

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

The muscle papillaris subarteriosus was composed of small, short and ill- developed muscular projections that were adherent to the interventricular septum within its proximal one-third. The apices of these muscle masses and the interventricular septum gave rise to chordae tendineae that gained attachment to the leaflets septalis and parietalis, and the parietoseptal commissure.

The Chordae tendineae of the Tricuspid Valve (Figs. 8: A,B, C&D): The chordae tendineae of the tricuspid valve, in all species investigated, originated from the apices and sides of the papillary muscles. In the animal valves, few chordae in addition arose directly from the interventricular septum. The tricuspid valve chordae were of commissural and leaflet types. The leaflet chordae 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 cleft chordae. The free edge, rough zone and basal zone chordae were coarse primary or they showed further secondary ramifications before gaining attachment to the free margin, rough zone on the ventricular surface of the leaflets close to their free margins, and the basal zone on the ventricular surface of the leaflets close to the annulus fibrosus of the valve; respectively. The cleft and commissural chordae tendineae exhibited a characteristic fan-shaped mode of fine secondary and tertiary ramifications before gaining attachment to the clefts 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 revealed insignificant sex-differences except for the total leaflet annular length, and the heights of the posterior and septal leaflets that showed significantly lower values in females than in males (Table 1).

Fig. 8: A,B,C&D: Photographs of excised and pinned out tricuspid valve- complexes of man (A), camel (B), sheep© and monkey (D), showing the annulus fibrosus (AF) receiving the attachment of the bases of the three leaflets of each valve: anterior (AL) or angularis (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) or muscle papillaris subarteriosus (MPS). The different types of chordae tendineae are also shown: free edge (1), rough marginal zone (2), basal zone (arrows), commissural (3), and cleft (4) chordae. The septomarginal trabecula (SMT) and the interventricular septum (IVS) are noted.

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

Measurments of the leaflets of the human tricuspid valve

*P <0.05=Significant

The number of the chordae tendineae arising from the posterior papillary muscle of the human right ventricle showed significantly lower mean value in females than in males. The chordal length exhibited significantly higher female mean values of the human septal leaflet rough zone chordae and anteroposterior commissural chordae. The rest of the human chordal number and length values showed insignificant differences related to sex (Table 2).

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

number and length of the different chordac tendineae of the human tricuspid valve

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

Measurments of the leaflets of the camel tricuspid valve

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

number and length of the different chordae tendineae of the camel tricuspid valve

Table 5: Measurements of the leaflets of the sheep tricuspid valve in both sexes.

Measurements of the leaflets of the sheep tricuspid valve

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

number and length of the different chordae tendineae of the sheep tricuspid valve

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

Measurments of the leaflets of the monkey tricuspid

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

number and length of the different chordae tendineae of the monkey tricuspid valve

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

Measurments of the leaflets of the tricuspid valve in man and camel

Table 10

Table 10

In animal species investigated, insignificant sexdifferences were detected regarding the measurements of the leaflets of the tricuspid valve except for the total leaflet annular length of the camel and monkey valves that showed significantly higher mean values in females than in males. The number of the chordae arising from the muscle papillaris parvi in each of the camel and monkey showed significantly lower female values. The number of the leaflet chordae in sheep revealed significantly higher female values regarding the leaflet angularis basal zone chordae, and the leaflets parietalis and septalis free edge chordae. The leaflets parietalis and septalis basal zone chordae as well as annular length and height, and the anguloparietal commissural height showed significantly lower mean values in sheep than in man (Table 10). The heights of the leaflets parietalis and septalis, and of the three commissures had significantly lower values in monkey than in man (Table 11 ).

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

Measurments of the leaflets of the tricuspid valve in man and monkey

The number of the camel chordae was significantly decreased at all of the three papillary muscles and most of the leaflets but significantly increased at the anguloparietal commissure, when compared with the number of homologous chordae in man. The length of the camel chordae attached to the leaflet septalis rough and basal zones, and the anguloseptal commissure displayed significantly higher mean values than those of human counter chordae (Table 12).

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

number and length of the different chordae tendineae of the tricuspid valve in man and camel

In sheep, there was a significant decrease in the number of the chordae arising from the muscles papillaris magnus and subarteriosus, and the chordae attached to the leaflet angularis basal zone and free edge, and the leaflet septalis basal zone~ when compared to human chordae. The numbers of the leaflet septalis free edge chordae and anguloparietal commissural chordae in sheep showed significantly higher mean values than those of the corresponding human chordae. The mean lengths of the sheep leaflets parietalis and septalis rough zone chordae showed significant decrease while the mean lengths of the leaflet septalis basal zone chordae and anguloparietal commissural chordae showed significant increase, when compared to their corresponding values in man (Table 13).

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

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

number and length of the different chordae tendineae of the tricuspid valve

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

In monkey, when compared to man, there was a significant decrease in the number of chordae tendineae arising from all of the three papillary muscles, and of the chordae attached to the rough and basal zones of the leaflets angularis and septalis, the basal zone and free edge of the leaflet parietalis, and the anguloparietal commissure. The mean number of the leaflet angularis free edge chordae and the anguloseptal commissural chordae in monkey was significantly increased than that of the corresponding chordae in man. The mean length of the leaflet angularis rough zone chordae as well as that of anguloseptal and anguloparietal commissural chordae in monkey was significantly shorter than in man. The mean lengths of the monkey leaflet angularis free edge chordae, leaflet parietalis basal zone and free edge chordae, and parietoseptal commissural chordae were significantly longer than those of man (Table 14).

C. The histological study:

C1. The tricuspid valve-complex in Man (Figs. 9-15) Light microscopic examination of the leaflets of the human tricuspid valve showed that each leaflet was formed of an endothelial fold enclosing a core of much collagenous bundles and few elastic fibres (Figs. 9-14). The endothelium covering the atrial surface of the anterior leaflet characteristically revealed fine folds or corrugations that extended along this surface in a proximo-distal direction (Figs. 9& 10). The collagenous fibres were condensed in the centre of the leaflet but loosely disposed beneath the atrial and ventricular surface endothelium. They were arranged into wavy bundles that ran parallel with the base-to-apex axis of the leaflet near its atrial aspect and they were obliquely or irregularly disposed towards the ventricular aspect of the leaflet (Figs. 9-11). At the sites of attachments of the chordae tendineae to the ventricular surface of the leaflets, the chordal connective tissue fibres merged freely into the subendothelial connective tissue of the leaflets (Fig. 10). The elastic fibres were scarce and confined to the subendothelial zone particularly that of the atrial surface of the leaflet (Fig. 11&12). The leaflet core was thicker at the peripheral basal margin of the leaflet and tapering towards its central free margin (Figs. 12-14). Blood capillaries and small blood vessels were noticed at the basal portions of the posterior and septal leaflets (Figs. 12-14). Muscle fibres could not be demonstrated in the human tricuspid leaflets. Histological examination of cross sections of the chordae tendineae of the human tricuspid valve revealed that they were mostly rounded but slightly oval near their attachments. They were ensheathed with a layer of endothelium, and were composed of dense bundles of collagenous fibres and scarce elastic fibres (Fig. 13).

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

Figs.9-15: (Unavailable) Photomicrographs of the anterior (Figs. 9-11), posterior (Figs. 12&13), and septal (Fig. 14) leaflets of the human tricuspid valve, showing a fibrous core (F.C.) of collagenous bundles enclosed between two endothelial layers. The endothelium at atrial aspect (A) of the anterior leaflet shows fine folds (short thin arrows). The collagenous fibres are packed in the centre of the leaflets, arranged in wavy parallel bundles (long thin arrows) near the atrial surface, and loosely disposed near the ventricular surface (V) of the leaflets being converging towards the sites of chordal attachments (short thick arrows). Few elastic fibres (dark brown in figs. 11&12) are seen in the subendothelium of the atrial surface of the leaflets. Blood vessels (B .V. ) are observed in the basal parts of the both posterior and septal leaflets. A chordae tendinea (Ch. T. ) is seen formed of dense collagenous fibres surrounded by endocardium (Fig. 13). A longitudinal section of a human papillary muscle (Fig. 15) shows that is formed of parallel and branching myocardial fibres; each has one to two nuclei and abundant cytoplasm.

Figs. (9 & 14) (Unavailable): 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 the lamina fibrosa that was composed of closely packed bundles of collagenous fibres (Figs. 16-20). The endothelial covering of the atrial surface of the camel leaflet parietalis showed fine folds imparting it a characteristic festooned appearance (Fig. 18). The lamina fibrosa was thicker at the base of the leaflet and it tapered towards the apex of the leaflet. At the base of the leaflet, the lamina fibrosa merged with the subendocardial collagenous tissue of the atrial and ventricular walls (Fig. 18). At both the atrial and ventricular surfaces of the lamina fibrosa, the collagenous fibres were loosely disposed forming the atrialis and ventricularis zones respectively (Figs. 16- 20). In most of its parts, the ventricularis was thicker than the atrialis (Figs. 17-20). Few elastic fibres were identified in the subendothelial loose tissue of the camel tricuspid leaflets particularly at their atrial surfaces (Figs. 16,18&20). Blood vessels were observed at the bases of the leaflets parietalis and septalis (Figs. 18&20). No muscle fibres could be identified within the camel leaflets.

The camel papillary muscles (Fig. 21) and chordae tendineae (Fig. 22) were exactly similar in structure to their human homologues (Figs. 13&15).

Figs. (16-22)(Unavailable) Photomicrographs of the leaflets angularis (Figs. 16&17), parietalis (Fig.18), and septalis (Figs. 19&20) of the camel tricuspid valve, showing the lamina fibrosa (L.F .) of dense collagenous fibres enclosed between two endothelial layers. The lamina is seen to be continuous with the subendocardial tissue of the cardiac wall (Fig. 18). The atrialis (A) and ventricularis (V) are zones of loosely arranged collagenous fibres bounding the atrial and ventricular surfaces of the lamina fibrosa respectively. The ventricularis is mostly thicker as it receives the attachments (thick arrows) of the leaflet chordae tendineae (Ch.T.). The endothelium of the atrial surface of the leaflet parietalis shows the fine festoons (thin arrows in Fig. 18). Blood vessels (B .V. ) are observed in the basal parts of the leaflets parietalis and septalis (Figs. 18&20). Few elastic fibres (dark brown in figs. 16,18&20) are seen in the subendothelium at the atrial surface of the leaflets. A camel papillary muscle (Fig. 21 ) and a chorda tendinea (Ch. T., Fig. 22) are similar in 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.

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 similar to those of the camel. Blood vessels were detected in the leaflets angularis (Fig. 23) and septalis (Fig. 26). The sheep papillary muscles (Fig. 27) displayed similar structure to those of human and camel. An obvious myotendineous transitional zone was observed at the apices of the sheep papillary muscles (Fig. 27).

Figs. (23-28)(Unavailable): Photomicrographs of the leaflets angularis (Fig. 23), parietalis (Figs. 24&25), and septalis (Fig. 26) of the sheep tricuspid valve, showing the lamina fibrosa (L.F.), atrialis (A) and ventricularis (V) of each leaflet. The lamina fibrosa is continuous with the subendocardial connective tissue (long thin arrows) of the ventricular wall (Figs. 24&25). The ventricularis looks thicker at 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 observed near the bases of the leaflets angularis and septalis (Figs. 23&26). Longitudinal sections of the chordae tendineae ( Ch. T .) showed their constitution of wavy bundles of many collagenous fibres and few 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 and, in addition, an obvious myotendineous transitional zone was observed at the papillary apex.

Figs. (23, 24 & 26)(Unavailable): 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 consistently similar, in structure, to those of the other three species investigated although they proved to be markedly smaller and thinner. Blood vessels (B. v. ) were seen in the basal parts of the leaflets angularis (Fig. 30) and parietalis (Fig. 31 ). The apical myotendineous transition of the monkey papillary muscles was also clearly showing (Fig. 34).

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

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