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Introduction
The intricate anatomy and physiology of the human heart are marvels of biological engineering. Among its many remarkable features, the papillary muscles (PMs) standout, as an anchor for the atrioventricular valves which is crucial for its proper functioning. The heart is structurally defined by its base, apex, and various surfaces including anterior, inferior, left and right pulmonary surfaces [1].
The conventional arrangement of PMs in the right ventricle (RV) typically involves three: one (anterior) associated with the sternocostal (Sc) surface, one (posterior) with the diaphragmatic surface, and one with the septal wall [2]. The anterior PM of RV holds the distinction of being the largest, while the septal PM is comparatively the smallest in size [3]. The medial PM of the RV, also known as the PM of the conus, the muscle of Luschka, and the muscle of Lancisi, displays considerable morphological variations. Consequently, its effectiveness as an anatomical landmark in the RV is somewhat restricted. To address these significant variations, Wenink [4] proposed the term “medial papillary complex.” In contrast, the left ventricle (LV) has only two PMs, positioned on the Sc and diaphragmatic surfaces respectively, which support the mitral valve flaps [1, 5]. These muscles exhibit distinct attachment pattern on the left ventricular wall. It may appear “finger-like,” characterized by a small focal point of attachment and minimal trabecular connections, or “tethered,” featuring a broader base of attachment and numerous trabecular bridges [6]. However, it’s also common for PM not to have a direct attachment to the left ventricular wall but rather to a network of trabeculae carneae [7].
Chordae tendineae (CT) form a delicate fibrous connection between the PMs and the leaflets of both the mitral and tricuspid valves [3]. CT is crucial for maintaining valve function, preventing their prolapse into the atria during ventricular contraction. It typically arises from the tip, apical third, and sometimes the base of the PM [1]. Because these CT connect to the tips of both mitral valve leaflets, injury to a single PM can impact both leaflets [8]. The anterolateral PM is supplied by the left anterior descending and the diagonal or a marginal branch of the circumflex artery, giving it a dual blood supply. The posteromedial PM is supplied by the posterior descending coronary artery, making it more susceptible to rupture following a myocardial infarction (MI) due to its single arterial supply. The PM are the last portion of the heart to be perfused and therefore are at higher risk of ischemia [8-10].
Embryonic development of PM, begins around the fifth week of embryogenesis with the formation of a muscular ridge, and this process completes by the nineteenth week [11]. Disruptions in their development can lead to abnormal accessory atrioventricular connections [12] or asymmetric mitral valves [11]. During the early phase of ventricular development, abnormalities in stage-specific markers of cardiomyocyte differentiation, such as SRY-box 2, GATA binding protein 4, and myosin heavy chain 6, or in signalling pathways like Notch, bone morphogenetic protein, and WNT/β-catenin, which regulate myocardial trabeculation, can lead to improper formation of PMs and CT [13]. During mid-gestation, improper compaction of ventricular myocardium can result in underdeveloped PM, potentially causing left ventricular non-compaction cardiomyopathy (LVNC). It is linked to heart failure, arrhythmias, and thromboembolic events, may involve abnormal PM contributing to mitral regurgitation. Up to 20% of Duchenne and Becker muscular dystrophy patients also develop LVNC, worsening left ventricular dysfunction and mortality [14]. Additionally, improper PM formation or attachment can lead to mitral or tricuspid valve regurgitation or prolapse, such as in mitral valve prolapse (MVP) or tricuspid valve dysplasia [15].
Congenital abnormalities, such as abnormal insertion or CT attachment, may culminate in clinical condition like parachute mitral valve causing mitral stenosis or regurgitation [16, 17]. Left ventricular remodelling from cardiomyopathy or ischemia can lead to secondary mitral regurgitation due to PM displacement, impairing valve leaflet coaptation [18]. A deep understanding of its anatomy is crucial to avoid mistaking hypertrophied or variant muscle for a thrombus, or vice versa [19]. Moreover, PM rupture, frequently triggered by acute MI or trauma, poses grave risk [20, 21]. Furthermore, neoplasms affecting PM may manifest with obstructive symptoms, thromboembolic events, or arrhythmias, necessitating comprehensive management strategies [22]. The prevalence of PM connections is notably high among patients with PM arrhythmia. These muscular connections have been linked with increased recurrence of clinical arrhythmia post ablation [23]. This study delves into the intricate landscape of PM anatomy, development, variations, and its clinical correlations aiming to elucidate their pivotal role in cardiac health and disease.
Materials and Methods
The present observational study was conducted in the Department of Anatomy at Lady Hardinge Medical College, New Delhi. Forty hearts were examined, and finally, thirty-eight grossly normal hearts, ranging in age from 40 years to 82 years (27 males and 11 females), were included in the study. The hearts were dissected to reveal the LV and RV using standard dissection techniques. Both ventricles were thoroughly washed with water to eliminate blood clots. The morphology of the PM, including both normal and variant forms, was documented based on the following parameters:
1. Total number PMs present on ventricular surfaces (Sc, diaphragmatic, and septal surfaces of both the ventricles).
2. The types of PMs based on their shapes at the base and apex, pattern of interconnection between the PMs were observed separately for the LV and RV (Fig. 1).
Type I: Broad based (BB), BB with broad apex
Type II: BB with bifid apex
Type III: BB with trifid or multifid apex
Type IV: “H” shaped, two PM interconnected by transverse band
Type V: “b” shaped, single curved branch of PM connected with base
Type VI: Small broad based (sBB), small broad base with small height
Type VII: Bifurcated based, base is perforated
Type VIII: Conical, broad base with conical apex
Type IX: Long cylindrical, long slender shaped
Type X: Small papillary projections, very small projections of PM
Statistical analysis
A comparison of the number of muscle bellies on the ventricular surfaces of the LV and RV was conducted using Fisher’s exact test.
Ethical statement
This study was conducted on donated bodies. The consent was obtained at the time of donation for the body to be used for research and teaching purposes. Ethical committee and local government have approved the studies on cadavers donated for research and teaching purposes. The study was approved by ethical committee of Lady Hardinge Medical College, New Delhi-IEC/thesis/2019/1.
Results
In this study wide variations of PMs were observed in both the ventricles with classical pattern [1, 2, 5] evident only in six hearts of the total specimens. Classical description where single papillary muscle is present in Sc, diaphragmatic surface of both the ventricles and one additinal from septal surface in case of RV.
On the Sc surface of LV we recorded one PM in 71.05%, two in 15.79%, three in 10.53% of specimens and it was absent in 2.63%. Similarly, the diaphragmatic surface exhibited one PM in 57.89%, two in 28.95%, and three in 13.16% of the total specimens (Table 1). In contrast, on the Sc surface of RV we recorded one PM in 89.47%, two in 7.90% and it was absent in 2.63%. Similarly, the diaphragmatic surface exhibited one PM in 63.16%, two in 26.31%, and three in 10.53% of the total specimens (Table 1).
Considering the various shapes of PMs in the LV on the Sc and diaphragmatic surfaces, the BB type (Type I) was the most common, appearing in 55.26% and 44.73% of cases, respectively. This was followed by the conical type (Type VIII), found in 28.96% and 31.58% of cases. In 2.63% of specimens, the base was BB with a bifurcated apex (Type II), while in 5.26% of cases, the apex was trifurcated (Type III) on the Sc surface. The “H” shaped (Type IV), where two PM bellies were interlinked, was observed on the Sc surface in 5.26% of cases and 7.90% on the diaphragmatic surface. Additionally, a small “b” shaped muscle (Type V) was identified on the diaphragmatic surface in 2.63% of cases (Table 2). In one instance, the PMs of both the surfaces of LV were joined together at the base, forming a conjoint variety (2.63%; Figs. 2, 3).
In the RV, the most common type was the conical-shaped (Type VIII), found in 71.05% and 2.63% on Sc and diaphragmatic surfaces, followed by the BB PM (Type I) in 7.90% and 44.74% on both surfaces. Another type of BB muscle, which was shorter in height (sBB, Type VI), was observed in 9 specimens. PM with a perforated base and conical apex (Type VIII) was present in only 2.63% of specimens on the Sc surface. PMs with bifid and trifid apexes (Types II and III) were seen only on the Sc surface in 2.63% of cases, but not on the diaphragmatic or septal surfaces. Single long cylindrical muscles (Type IX) were less frequent on the Sc and diaphragmatic surfaces, observed in 7.90% and 21.05% of cases, respectively. Small PM projections (Type X) were observed in 10.53% on the diaphragmatic surface and 76.32% on the septal surface. In 23.68% of cases, we observed that the tendinous cords were directly attached to the interventricular septal wall, without connecting to any part of the PM belly (Table 3). A unique webbed shaped configuration of the PM was found exclusively in the RV (2.63%). In this configuration, two septomarginal bands were attached to a single anterior PM, with the CT directly connected to it (Figs. 4, 5).
While examining the shapes of PMs in both ventricles, it was noted that Types I, II, III, and VIII were present in both the ventricles. BB PM (Type I) emerged as the most frequent variant based on shape. In the LV, Type I appeared bulkier and often grouped together. Types IV, V, and conjoint type (Figs. 1–3) were exclusive to the LV, while Types VI, VII, IX, X, and webbed shaped PM (Figs. 1, 4, 5) were identified only in the RV. A unique finding in the RV, was the small projection of PM (Type X), and the sBB PM (Type VI). Additionally, a solitary long cylindrical (Type IX) muscle belly with a single tendinous cord attached to its tip was observed only in the RV. An interesting feature in the RV was the direct attachment of tendinous cords to the ventricular septal wall (Fig. 5). A comparison of the number of muscle bellies on the ventricular surfaces of both ventricles was conducted using Fisher’s exact test (χ²=0.21, df=1, P=0.84). The results indicated that there was no significant difference in the number of muscle bellies between the two ventricular surfaces.
Discussion
The structural complexity of PM within the heart encompasses a spectrum of variations and pathologies, significantly influencing cardiac function. These muscles are vital for valve integrity and function, exhibiting diverse morphological variants stemming from developmental anomalies [24], neoplastic formations, or traumatic injuries. The morphological diversity of PM includes variations in the number of muscle heads and whether they have shared or separate basal origins [17], as well as shapes ranging from conical to bifurcated or trifurcated configurations [5].
Classical and atypical patterns of papillary muscle and their related pathologies
In the standard literature [1], classical pattern of the PM is described as two major PM in the LV in anterolateral and posteromedial positions and three PM in the RV in anterior, inferior, and septal positions. However, our study revealed considerable deviation from this classical pattern, with only 6 out of 38 hearts exhibiting this traditional configuration. As noted by Harrigan et al. [25] and Rajiah et al. [17], the non-traditional configuration and number of PMs in the LV are associated with hypertrophic cardiomyopathy (HCM), which can lead to mid-cavity obstruction. Quantitative understanding of the PM is crucial, as the presence of extra muscles serves as a key morphological marker for HCM and is also important for screening family members for this condition [26].
Present study observed significant variations in the morphology of PM in both ventricles, aligning with previous research by Saha and Roy [2, 5], Victor and Nayak [27], Bhadoria et al. [28], Gheorghitescu et al. [29], and Chiechi et al. [30]. Additionally, our study found extra PM on the Sc and diaphragmatic surfaces, consistent with findings by Valli and Gohila [31] and Victor and Nayak [27]. Kavimani et al. [32] in similar kind of study observed that 62.00% of single PM in Sc surface, two PM in 31.00% and three PM in 2.00% of total PM (Table 4).
Notably, a single PM was typically observed on the Sc surface of the RV, in agreement with findings by Saha and Roy [2], Hosapatna et al. [33], and Priya et al. [34] (Table 5). The presence of extra PM provides more options for determining the degree and direction of realignment for surgical correction [35]. Researchers have linked variations in the number of PMs on both the anterior and posterior surfaces of the RV to various cardiac rhythm disorders, including extrasystoles [36, 37]. Such variations could potentially be mistaken radiologically for valvular vegetations, papillary fibroelastoma, thrombus, or metastatic tumors and could potentially increase the risk of pulmonary embolism due to blood stasis [38]. In RV, our study found that more than one anterior PM was present in 7.90% of cases, with two and three posterior PMs observed in 26.31% and 10.53% of cases, respectively.
Previous studies have reported variations in PMs, including atypical positions and the presence of extra or abnormal PMs, which have been associated with conditions such as MVP, tricuspid dysplasia, and left ventricular outflow tract (LVOT) obstruction [17, 25, 26]. In our study, we identified similar PM types, however, the absence of specimen data prevents us from confirming a direct association with these conditions. In the context of mitral and tricuspid valve replacement surgeries, recognizing PM morphology is essential, particularly in cases of severe mitral valve regurgitation where using the patient’s own PM as a homograft is often preferred because of its superior blood supply, innervation, and natural integration with heart tissue [39]. Techniques like resection, repositioning, and realignment have shown considerable clinical benefits [40-42].
Variable shapes of papillary muscle, terminology, and clinical implications
The shapes of the PM varied across different ventricular surfaces and have been described differently by previous researchers. Victor and Nayak [27] and Aktas et al. [36] categorized PM as conical, sloped, arched, grooved, wavy, mamillated, flat-topped, stepped, and saucerised. Saha and Roy [5] adopted similar terminology, identifying flat-topped PM akin to Type I in our study, while Y-shaped and arched PM corresponded to Type I and Type V of PMs in our study. While searching the literature, we observed that there is no uniformity in the nomenclature used for the shapes of PM. The shapes of PM can significantly influence their mobility and the outflow of blood. In the current study, PM with multiple heads (Type III) were found to be 10.52%. According to Kwon et al. [43] and Maron et al. [44], this type of PM is more likely to be associated with HCM and contribute to LVOT narrowing and obstruction which may require modifications to the surgical approaches typically used for its treatment. In our study, 2.63% of PM exhibited a bifurcated form (Type II). Ker [45] suggests that this type of PM may be linked to hypermobility and premature ventricular complexes in a bigeminy pattern, even without obstruction.
A study by O’Donnell et al. [46] reported that some benign tumors (myxomas) have a slender pedicle connecting them to the myocardium, while malignant tumors are typically BB. This is analogous to the BB Type I, Type II, and Type III PM found in the present study (55.26%, 2.63%, and 5.26%, respectively). According to Mollet et al. [19], occasionally, a hypertrophied PM similar to Type I variant of current study could be mistaken for a thrombus or vice versa.
Study done by Ho [47] describes PMs of LV are usually in groups arranged very close to each other. In the present study, “H” type (Type IV) of interconnection between the two PM was more prominent. Doty and Acar [35] described four types of PM based on the presence or absence of a division in the muscle and its location relative to the commissure. In his study, Type IV variant, which are similar to the conjoint variety found in the current study (2.63%), were considered unsuitable for implantation due to the potential risk of uneven tension on individual heads, leading to prolapse of one leaflet or restriction of the opposite leaflet. In our study, we identified a conjoint variant of PM characterized by multifid apex linked by the common base, originating at various levels along the ventricular wall. Krawczyk-Ożóg et al. [48] observed conglomerates of interconnected PM, a finding coherent with conjoint variety of PM of the current study. In the LV, H, Y, or N shaped interconnections between PM have been described by many authors. Bose et al. [49] noted that in the LV, 51.5% of PM had broad apices and 45% were conical, whereas in the study by Sinha et al. [50] broad apex was in 36.7% and conical apex in 33.3% which is similar to our observations. PM connections are highly prevalent in patients with PM arrhythmia. These connections have been associated with a higher recurrence rate of clinical arrhythmia following ablation procedures [23].
In the RV, our study revealed that conical-shaped PM (Type VIII) were predominant on the Sc surface, aligning with findings by Bhadoria et al. [28], Aktas et al. [36], and Hosapatna et al. [33]. The absence of the septal PM was reported by Aktas et al. [36] (11.75%), Nigri et al. [51] (21.5%), Kumar et al. [52] (38.88%), and Begum et al. [53] (24%), while our study noted this absence in only one heart (2.63%). Aktas et al. [36] also observed that the septal PM was smaller than those originating from other ventricular walls. The current analysis found little coincidence with the aforementioned studies. Additionally, we concur with Victor and Nayak’s [27] observation that PM are unique to each individual, much like fingerprints. This variability in the number and configuration of PM in the RV has significant clinical implications. Aktas et al. [36] reported conical and flat-topped shapes of PM and associated them with an increased risk of sudden cardiac death. We observed that conical-shaped PMs were predominant in the RV, and the absence of the septal PM was rarely noted. A distinctive webbed shaped PM was observed in the RV of one specimen, consistent with the findings of Lee and Hur [54], who reported this configuration in 30.6% of their cases.
Our study explored various PM shapes and configurations, correlating them with pathologies, diagnostic challenges, and surgical interventions documented in prior research. The use of varied and non-standardized terms can lead to confusion in interpreting diagnostic images and complicate surgical planning due to unclear communication. This lack of clarity in PM morphology descriptions may affect surgical outcomes and hinder research comparability. The present study reveals atypical PM patterns in both ventricles, deviating from classical anatomy. To understand these variations, it is crucial to explore factors such as regional sampling, demographic differences, methodological inconsistencies, and genetic influences. The study’s focus on a single region, combined with limited demographic and cadaveric data, hampers our ability to determine whether these variations arise from regional or genetic factors. Future research should address these gaps by broadening sample sizes, incorporating diverse populations, and leveraging advanced imaging technologies to better detect PM variations and assess their impact on long-term cardiac health.
In conclusion, our study reveals significant variability in the morphology, number, and arrangement of PM in both ventricles, reflecting complex developmental processes and potential pathologies. Comparing our findings with existing literature emphasizes the need for standardized terminology, as inconsistencies can hinder understanding of normal anatomy. Enhanced knowledge of PM improves diagnostic precision through advanced imaging techniques like transoesophageal echocardiography, cardiac computed tomography, and cardiac magnetic resonance imaging, ultimately aiding cardiothoracic surgeons, radiologists, and cardiologists in minimizing errors and refining surgical techniques. Therefore, a comprehensive understanding of PM is essential for advancing cardiac care.
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