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Ann Anat 190 (2008) 81—87
www.elsevier.de/aanat
RESEARCH ARTICLE
The clinical anatomy of the crista terminalis,
pectinate muscles and the teniae sagittalis
Marios Loukasa,b,, R. Shane Tubbsc, Jonathan M. Tongsond,
Shrikaant Polepallia, Brian Currya, Robert Jordana, Teresa Wagnere
a
Department of Anatomical Sciences, School of Medicine, St. George’s University, Grenada, West Indies
b
Department of Education and Development, Harvard Medical School, Boston, MA, USA
c
Department of Cell Biology and Pediatric Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, USA
d
American University of the Caribbean, St. Maarten, Netherlands Antilles, USA
e
Department of Pathology, Institute of Rheumatology, Warsaw, Poland
Received 2 February 2007; accepted 31 May 2007
KEYWORDS Summary
Crista terminalis;
The crista terminalis (CT) is an important anatomic landmark due its close
Tenia sagittalis;
association with the sinoatrial node artery and the origin of the pectinate muscles
Pectinate muscles;
(PM). However, the gross anatomy of the PM in relation to the CT has not been well
Tricuspid valve;
described. The aim of our study has been to investigate the location and the
SA node artery;
morphology of PM in relation to the CT. We examined 300 adult formalin-fixed human
Right atrial
hearts. All PM originated from the CT and extended along the wall of the appendage
catheterization;
toward the vestibule of the tricuspid valve. It was observed that the PM varied
Right atrial anatomy
significantly with respect to arrangement and course of its fibers. We were able to
classify the course of the PM, including the most prominent PM called the tenia
sagittalis (TS), into 6 different patterns with 3 different TS types. In Type A (15%),
the TS was absent. Type B (65%) demonstrated a single TS and Type C (20%) was
characterized by the presence of multiple TS. Furthermore, the course of the PM was
classified into 6 patterns: Type I (40%), the PM was oriented perpendicular to the CT
with uniform spacing and lack of crossover (trabeculation); Type II (20%), non-
uniform PM was organized in a haphazard, trabecular fashion with numerous
crossovers; Type III (15%), the PM had uniform spacing with no trabeculation with
fibers oriented parallel to the CT; Type IV (10%), had arborizing PM originating from a
common muscular trunk (solitary trunk); Type V (10%), fibers were oriented both
perpendicular and parallel to the CT, similar in architecture to Type III, but with
more than one common muscular trunk; Type VI (5%), prominent muscular column
with velamentous PM with potential implications in cardiac catheterization
Corresponding author at: Department of Anatomical Sciences, School of Medicine, St. George’s University, Grenada, West Indies.
Tel.: +473 444 4175x2556; fax: +473 444 2887.
E-mail addresses: edsg2000@yahoo.com, mloukas@sgu.edu (M. Loukas).
0940-9602/$ - see front matter & 2007 Elsevier GmbH. All rights reserved.
doi:10.1016/j.aanat.2007.05.002
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82 M. Loukas et al.
procedures. The exact morphology of PM and TS may be clinically important in right
atrial catheterization procedures, as well as in the development of arrhythmias but
further investigations are now necessary to prove this theory.
& 2007 Elsevier GmbH. All rights reserved.
Introduction Materials and methods
The atrium proper and the auricle are separated The Institutional Review Board of St. George’s
from the sinus venosus by a smooth muscu- University approved this study (TRB/06014).
lar boundary termed the crista terminalis (CT) Individual consent was waived as data collection
(Standring, 2005; Hollinshead, 1956) corresponding (age and patient history) was obtained from
externally to the sulcus terminalis (Clemente, cadaver records. We examined a total of 300 adult
1985). The pectinate muscles (PM) are muscular human hearts. A total of 100 hearts were examined
ridges extending anterolaterally from the CT to during the ‘‘human body’’ course at Harvard
reach the auricle, to form several trabeculations Medical School, throughout the academic seme-
(Standring, 2005). The largest and most prominent sters of 2001–2005. The hearts were derived from
PM forming the bridge of the sulcus terminalis 40 female and 60 male cadavers ranging in age from
internally, upon external inspection, is called the 55 to 86 years with a mean age of 72 years.
‘‘taenia sagittalis (TS)’’, literally translated, ‘‘the A further 50 hearts were derived from St. George’s
sagittal worm’’ (Van Praagh, 1980). University, during the academic training semesters
Although descriptions of the gross structure and of 2005 and 2006. The hearts were derived from 22
fiber orientation of the external right atrium are female and 38 male cadavers ranging in age from 65
detailed (Ho et al., 2002a, b; Shirani and Alaeddini, to 71 years with a mean age of 69 years. The
2000), the gross anatomy of the PM in relation to remaining 150 hearts were derived from the
the CT has not been well described. Interestingly Department of Pathology, Institute of Rheumatol-
enough, CT and PM have recently received increas- ogy in Warsaw, Poland, during routine autopsies
ing attention. This stems largely from the discovery performed during 1997–2001. The hearts were
that the morphology of the CT has a functional role derived from 79 female and 70 male cadavers
in electrophysiology and cardiac conduction; thus, ranging in age from 45 to 83 years with a mean age
this structure has inherent implications in arrhyth- of 73 years. All hearts were fixed in a formalin/
mias (Sanchez-Quintana et al., 2002; Olgin et al., phenol/alcohol solution.
1995; Schumacher et al., 1999; Kaiman et al., The specimens selected for this study were
1998). without any evidence of previous surgical proce-
Sanchez-Quintana et al. (2002) previously de- dures or traumatic lesions to the heart. Further-
scribed the role of the CT as a natural barrier to the more, specimens were collected from subjects with
cardiac conduction system. The same type of no macroscopic pathology of the heart. Specimens
conduction block is observed as a common feature with grossly evident atherosclerotic lesions in the
in patients with atrial flutter (Sanchez-Quintana coronary arteries but without any other cardiac
et al., 2002; Olgin et al., 1995; Schumacher et al., pathology were included in the study.
1999). Two-thirds of focal right atrial tachycardias In order to correct for individual examiner
seen in the absence of structural heart disease arise variability, each specimen was examined by two
along the CT (Sanchez-Quintana et al., 2002; co-authors, independently. The specimens derived
Kaiman et al., 1998). Furthermore, the role of from Harvard Medical School were examined by
the PM, if any, is yet to be determined. M.L. and S.P., the specimens derived the Depart-
The aim of this study has been to describe the ment of Anatomical Sciences at St. George’s
morphologic patterns of PM and tenia sagittalis University were examined by S.P. and B.C., while
and their relation to the CT. In addition, we the specimens derived from the Department of
postulate that the anatomic variants in the Pathology in the Institute of Rheumatology
distribution of PM, and, more importantly, the TS, were examined by M.L. and T.W. All cadavers
may play important roles in the development of were routinely fixed in a formalin/phenol/alcohol
thrombus formation and possibly represent poten- solution.
tial sites of cardiac injury during catheterization In order to obtain maximal visualization of the CT
procedures. and PM, the IVC and SVC were opened posteriorly
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Crista terminalis 83
along a longitudinal axis to expose the right atrium.
A second anterolateral incision was made perpen-
dicular to the original cut, parallel to the coronary
sulcus, thus preserving the morphology of the CT
and PM. Observations of the CT as well as gross
structural characteristics (including orientation of
PM, variation in TS and relationship to CT) of the TS
and PM were digitally analyzed.
Digitized images of the CC, PM and TS, together
with the surrounding structures, were stored in the
Lucia Software. After applying a standard 1 mm
scale to all pictures, the program was able to use
this information to calculate pixel differences
between two selected points, as previously de-
Figure 1. A Type I PM oriented perpendicular to crista
scribed (Loukas et al., 2005). The purpose of the
terminalis.
software was to allow easy and accurate translation
of pixel differences into metric measurements.
Subsequently, the hearts derived from St.
George’s Department of Anatomical Sciences were
also examined using a Stryker endoscopic unit
(prior to gross dissection) including a Stryker
Quantum 4000 light source, Stryker 3-chip camera
System and a Wolf 2.5 mm 30 cm, 01 endoscope.
Images were recorded with ESS image capture and
catalog software, as previously described (Loukas
et al., 2006). Access to the right atrium was via the
inferior vena cava. The purpose of entering and
exploring the CT, PM and TS endoscopically, before
gross dissection was to identify and appreciate any
significant variations before removal of the right
atrial wall. After endoscopic investigation, the
variations of the CT, PM and TS were preserved
grossly.
In addition, we measured the distance from the
origin of the CT to its termination. We also
measured the thickness of both the CT and TS at Figure 2. A Type II PM, in which non-uniform PM are
their mid-distance from the origin to their termina- organized in a haphazard, trabecular fashion with
tion. Our results were analyzed with ‘‘Student’s numerous crossovers.
t-test’’ using Statistica for Windows (version 6.2)
and considered statistically significant when To facilitate comparisons between specimens and
values were po0.05. Preparations intended to be analysis of the various patterns, the results of the
used in photographs for publication were not dissection of the 300 specimens were classified into
made following the regular incisions as described 6 groups.
above. They were especially planned and per- The course of the PM was classified into 6 types:
formed in order to expose hidden details and Type I, PM oriented perpendicular to the CT with
intricate relations of the cardiac structures (see uniform spacing and lack of crossover (trabecula-
also Figures 1–7 for details). tion); Type II, non-uniform PM organized in a
haphazard, trabecular fashion with numerous
crossovers; Type III, PM with uniform spacing and
no trabeculation with fibers oriented parallel to CT;
Results Type IV, arborizing PM originating from a common
muscular trunk (solitary trunk); Type V, fibers
The CT was identified in all 300 specimens and, as oriented both perpendicular and parallel to CT,
expected, the morphology of the CT with the similar in architecture to Type III, but with more
corresponding PM and TS was subject to a wide than one common muscular trunk; Type VI,
spectrum of variability. prominent muscular column with velamentous PM.
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84 M. Loukas et al.
Figure 3. A Type III PM, in which PM exist with uniform spacing and no trabeculation with fibers oriented parallel to CT.
Figure 4. Arborizing PM of Type IV originating from a common muscular trunk (solitary trunk). Fibers oriented both
perpendicular and parallel to CT.
These results are summarized in Table 1 and thickness, and length of CT, PM and CT (Student’s t-
graphically represented in Figures 1–7. Further- test; p40.05), respectively.
more, in 45 (15%) specimens the TS was absent, in
195 (65%) specimens a single TS was observed and
in 60 (20%) specimens multiple TS were present
(Table 2). Discussion
The TS in all dissected specimens was measured
and found to have a thickness ranging from 0.2 to The CT is a significant anatomic landmark with
0.6 mm with a mean of 0.4 mm and lengths ranging clinical and surgical relevance. This has been
from 4 to 15 mm with a mean of 12 mm. Measure- largely demonstrated in experimental and clinical
ment of the CT yielded a thickness from 0.5 to studies suggesting that the CT forms the anatomic
11 mm with a mean of 0.8 mm and a length ranging substrate underlying intercaval conduction block
from 40 to 62 mm with a mean of 51 mm. There was (Becker et al., 2001; Friedman et al., 2000;
no significant difference between race, gender, age Schoels et al., 1990; Yamashita et al., 1987, 1992;
and institution of cadaver derivation with regard to Schumacher et al., 1999; Arenal et al., 1999;
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Crista terminalis 85
Olgin et al., 1995; Tai et al., 1998). Recent physiology in the CT, and examined the PM
literature also describes the role of the CT in the originating from the CT in 97 human necropsy heart
electrophysiology of cardiac muscle (Sanchez- specimens. The PM with highly trabeculated muscle
Quintana et al., 2002; Olgin et al., 1995; Schuma- fiber bundles may facilitate the non-uniform spread
cher et al., 1999; Kaiman et al., 1998). Becker of the excitatory impulse. With this characteristic
et al. (2001) have described the orientation of anisotropic spread of excitation from the SA node,
fibers from the CT and PM in canine myocardium this may lead to the phenomenon of impulse
potentially forming an anatomic/electrophysiologic ‘‘re-entry’’ due to the timing of depolarization
basis for intercaval conduction block. Similar and refractory rates of the excitable cells.
studies in human hearts demonstrated the role of This could potentially predispose patients, with
the CT as a natural barrier to conduction in patients significantly trabeculated PM types, to atrial
with atrial flutter (Olgin et al., 1995; Schumacher arrhythmias.
et al., 1999). The CT in patients with atrial flutter may be
Recently, Sanchez-Quintana et al. (2002) inves- particularly significant since the most common atrial
tigated morphological features relevant to electro- flutters are counter-clockwise isthmus-dependent
Figure 7. An endoscopic view of the right atrium. Note
Figure 5. PM (of Type V) with uniform spacing and no two prominent muscular columns (the TS) with velamen-
trabeculation with fibers oriented parallel to the CT, but tous PM (Type VI) having potential clinical implications in
with more than one common muscular trunk. cardiac catheterization procedures.
Figure 6. A prominent muscular column, the TS, with velamentous PM (Type VI) having potential clinical implications in
cardiac catheterization procedures.
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86 M. Loukas et al.
Table 1. Subclassification based on the orientation of We hypothesize that hearts with Types VI TS and
fibers to the crista terminalis and the tenia PM, composed of a prominent muscular column
with velamentous PM, may have a higher chance of
Type Occurrence (%) Morphology
being damaged during catheterization. During a
Type I 40 PM oriented perpendicular catheterization procedure, it is possible that the
to the CT with uniform tip of a cardiac catheter may become stuck behind
spacing and lack of the TS. An injudicious push at this point could result
crossover (trabeculation) in right atrial perforation (Van Praagh, 1980).
Type II 20 Non-uniform PM organized Although this perforation is possible, the complica-
in a haphazard, trabecular tion rate of atrial flutter procedures is extremely
fashion with numerous low. Similarly, cardiac perforation is an uncommon
crossovers
even in flutter procedures.
Type III 15 PM with uniform spacing
Irrespective, of CT and PM types, in cardiac
and no trabeculation with
fibers oriented parallel to surgery, one should avoid transection of the CT in
CT order to avoid trauma to the SA node artery,
Type IV 10 Arborizing PM originating thrombosis of the SA nodal artery and trauma to the
from a common muscular SA node. SA nodal infarction is a common cause of
trunk (solitary trunk) tachycardia–bradycardia and sick sinus syndrome
Type V 10 Fibers oriented both postoperatively. Avoidance of trauma to the SA
perpendicular and parallel node and SA nodal artery, which are difficult to see
to CT grossly, can be accomplished surgically, by avoiding
Type VI 5 Similar architecture to the CT (Van Praagh, 1980). In addition, the risk of
Type III, but with more
thrombus formation may be reduced by the routine
than one common muscular
administration of heparin; however, this does not
trunk
exclude the possibility of local thrombus formation
in the cavotricuspid isthmus.
Recent embryologic studies, in chick atria,
Table 2. Classification of the crista terminalis the showed that a preferential pathway exists during
taenia sagittalis (n ¼ 300) development within the roof of the atria, transmit-
ting the impulse rapidly from the right-sided
Type Occurrence (%) Morphology
sinoatrial node to the left atrium. The morpholo-
Type A 15 Absent TS gical substrate of this pathway, the bundle of
Type B 65 Single TS Bachman, apparent from stage 29 onward, is a
Type C 20 Double TS prominent ridge of PM continuous with the CT
(Sedmera et al., 2006).
Our study has characterized the PM in a
systematic manner in its relation to the CT so that
arrhythmias arising near the terminal ramifications further studies may have a uniform method of
of the crest end. This type of atrial flutter is named classification when performing clinically significant
inferior since it arises near the lowest point of the CT experimentation. However, further studies of the
between the anterior rim of the IVC and inferior rim various types of TS and PM and their relations to the
of the tricuspid ring. In addition, it has been CT in specimens with atrial flutter may help to
proposed that in atrial flutter transverse block, the elucidate similarities and differences in human
block may occur in close proximity to the terminal hearts, as well as to determine if the proposed
crest lever (Friedman et al., 2000), and according scheme proves to be a useful and valid tool for
to the experimental work of Becker et al. (2001) future nomenclature and classification of these
the block can occur at the junction of the crest with anatomic structures. While the clinical implications
the PM. of the varied anatomic presentations of PM and TS
Further complications of atrial flutter include relative to CT are unknown, we hypothesize that
atrial thromboemboli. One of the most common patients with velamentous PM (Type VI, 5%) may be
ways of treating atrial flutter is the use of radio- at an increased risk for complications during
frequency catheter ablation in which the tissue catheterization procedures and may be predisposed
suspected of causing the arrhythmia is ablated to thrombus formation. Whether or not the
(Sanchez-Quintana et al., 2002). The morphology of morphology of the PM in relation to either the CT
the PM is pertinent in this procedure due to the risk or the TS possesses clinical significance remains to
of iatrogenic myocardial injury. be determined.
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Crista terminalis 87
References flutter: activation and entrainment mapping guided
by intracardiac electrocardiography. Circulation 92,
Arenal, A., Almendral, J., Alday, J.M., Villacastin, J., 1839–1848.
Ormaetxe, J.M., Perez-Castellano, N., Gonzalez, S., Sanchez-Quintana, D., Anderson, R.H., Cabrera, J.A.,
Ortiz, M., Delcan, J.L., 1999. Rate-dependent con- Climent, V., Martin, R., Farre, J., Ho, S.Y., 2002. The
duction block of the crista terminalis in patients with terminal crest: morphological features relevant to
typical atrial flutter influence on evaluation of electrophysiology. Heart 88, 406–411.
cavotricuspid isthmus conduction block. Circulation Schoels, W., Gough, W.B., Restivo, M., Caref, E.B.,
99, 2771–2778. Gough, W.B., el-Sherif, N., 1990. Circus movement
Becker, R., Bauer, A., Metz, S., Kinscherf, R., Senges, atrial flutter in the canine sterile pericarditis model:
J.C., Schreiner, K.D., Voss, F., Kubler, W., Schoels, W., activation patterns during initiation, termination, and
2001. Intercaval block in normal canine hearts – role sustained reentry in vivo. Circ. Res. 67, 35–50.
of the terminal crest. Circulation 103, 2521–2526. Schumacher, B., Jung, W., Schmidt, H., Fischenbeck, C.,
Clemente, C.D., 1985. Gray’s Anatomy – 30th American Lewalter, T., Hagendorff, A., Omran, H., Wolpert, C.,
ed. Chambers of the Heart. Lea and Febiger, Phila- Luderitz, B., 1999. Transverse conduction capabilities
delphia, pp. 626–628. of the crista terminalis in patients with atrial flutter
Friedman, P.A., Luria, D., Fenton, A.M., Munger, T.M., and atrial fibrillation. J. Am. Coll. Cardiol. 34,
Jahangir, A., Shen, W.K., Rea, R.F., Stanton, M.S., 363–373.
Hammill, S.C., Packer, D.L., 2000. Global right atrial Sedmera, D., Wessels, A., Trusk, T.C., Thompson, R.P.,
mapping of human atrial flutter: the presence of Hewett, K.W., Gourdie, R.G., 2006. Changes in
posteromedial (sinus venosa region) functional block activation sequence of embryonic chick atria corre-
and double potentials: a study in biplane fluoroscopy late with developing myocardial architecture. Am. J.
and intracardiac echocardiography. Circulation 101, Physiol. Heart Circ. Physiol. 291, H1646–H1652.
1568–1577. Shirani, J., Alaeddini, J., 2000. Structural remodeling
Ho, S.Y., Anderson, R.H., Sanchez-Quintana, D., of the left atrial appendage in patients with chronic
2002a. Gross structure of the atriums: more than an non-valvular atrial fibrillation: implications for
anatomic curiosity. Pacing Clin. Electrophysiol. 25, thrombus formation, systemic embolism, and assess-
342–350. ment by transesophageal echocardiography. Cardio-
Ho, S.Y., Anderson, R.H., Sanchez-Quintana, D., 2002b. vasc. Pathol. 9, 95–101.
Atrial structures and fibers: morphologic bases of Standring, S., 2005. Gray’s Anatomy – 39th ed. The Heart
atrial conduction. Cardiovasc. Res. 54, 325–336. and Great Vessels. Elsevier, Churchill Livingstone,
Hollinshead, W.H., 1956. Anatomy for Surgeons: Vol. 2. Edinburgh, pp. 1000–1001 (Chapter 60).
The Heart and Great Vessels. Harper & Row, New York, Tai, C.T., Chen, S.A., Chen, Y.J., Yu, W.C., Hsieh, M.H.,
pp. 124–125. Tsai, C.F., Chen, C.C., Ding, Y.A., Chang, M.S., 1998.
Kaiman, J.M., Olgin, J.E., Karch, M.R., Hamdan, M., Lee, Conduction properties of the crista terminalis in
R.J., Lesh, M.D., 1998. ‘‘Cristal tachycardias’’: origin patients with typical atrial flutter: basis for a line of
of right atrial tachycardias from the crista terminalis block in the reentrant circuit. J. Cardiovasc. Electro-
identified by intracardiac echocardiography. J. Am. physiol. 9, 811–819.
Coll. Cardiol. 31, 451–459. Van Praagh, R., 1980. Congenital Heart Disease: Embry-
Loukas, M., Hüllet, J., Wagner, T., 2005. The clinical ology, Anatomy, and Approach to Diagnosis. Children’s
anatomy of the inferior phrenic artery. Clin. Anat. 18, Hospital Boston MA Publications, pp. 29–30.
357–365. Yamashita, K., Hiraoka, M., Adaniya, H., 1987. Conduc-
Loukas, M., Louis Jr., R.G., Van der Wall, B., Hallner, B., tion blocks in and around preferential pathway of dog
Tucker, J.J., Esguerra, F., Colborn, G.L., 2006. right atrium. Am. J. Physiol. 253, H16–H24.
Iliolumbar membrane, a newly recognized structure Yamashita, T., Inoue, H., Nozaki, A., Ajiki, K., Oikawa,
in the back. Folia Morphol. 65, 22–25. N., Kuo, T.T., Usui, M., Murakawa, Y., Sugimoto, T.,
Olgin, J.E., Kaiman, J.M., Fitzpatrick, A., Lesh, M.D., 1992. Role of anatomic architecture in sustained atrial
1995. Role of right atrial endocardial structures as reentry and double potentials. Am. Heart J. 124,
barriers to conduction during human type I atrial 938–946.
