SHORT COMMUNICATION
The Student’s Dilemma, Liver Edition: Incorporating the Sonographer’s Language Into Clinical Anatomy Education M. Kennedy Hall,1 S. Ali Mirjalili,2 Christopher L. Moore,1 Lawrence J. Rizzolo3* 1 Department of Emergency Medicine, Yale University, School of Medicine, New Haven, Connecticut 2 Department of Anatomy with Radiology, Faculty of Medical and Health Sciences, School of Medical Sciences, University of Auckland, Auckland, New Zealand 3 Department of Surgery, Yale University, School of Medicine, New Haven, Connecticut
Anatomy students are often confused by multiple names ascribed to the same structure by different clinical disciplines. Increasingly, sonography is being incorporated into clinical anatomical education, but ultrasound textbooks often use names unfamiliar to the anatomist. Confusion is worsened when ultrasound names ascribed to the same structure actually refer to different structures. Consider the sonographic main lobar fissure (MLF). The sonographic MLF is a hyper-echoic landmark used by sonographers of the right upper quadrant. Found in approximately 70% of people, there is little consensus on what the sonographic MLF is anatomically. This structure appears to be related to the main portal fissure (aka principal plane of the liver or principal hepatic fissure), initially described by anatomists and surgeons as in intrahepatic division along the middle hepatic vein which in essence divides the territories of the left and right hepatic arteries and biliary systems. By exploring the relationship between the main portal fissure and the sonographic MLF in cadaveric livers ex vivo, the data suggest the sonographic MLF is actually an extrahepatic structure that parallels the rim of the main portal fissure. The authors recommend that this structure be renamed the “sonographic cystic pedicle,” which includes the cystic duct and ensheathing fat and blood vessels. In the context of the redefined underlying anatomy, the absence of the sonographic cystic pedicle due to anatomic variation may serve an important clinical role in predicting complications from difficult laparoscopic cholecystectomies and is deserving of future study. Anat Sci Educ C 2015 American Association of Anatomists. 8: 283–288. V
Key words: gross anatomy education; medical education; ultrasonographic examination; anatomical sciences; emergency medicine; liver divisions; main lobar fissure; cystic duct
INTRODUCTION New radiological imaging modalities are rapidly gaining applicability in medical education as tools for addressing basic science questions and for supplementing traditional modes of learning (Chowdhury et al., 2008; Machado et al., 2013). One *Correspondence to: Dr. Lawrence J. Rizzolo; Department of Surgery, Yale University, PO Box 208062, New Haven, Connecticut, USA. E-mail: [email protected] Additional Supporting Information may be found in the online version of this article. Received 16 August 2014; Revised 2 December 2014; Accepted 22 December 2014. Published online 8 January 2015 in Wiley (wileyonlinelibrary.com). DOI 10.1002/ase.1518 C 2015 American Association of Anatomists V
Anatomical Sciences Education
MAY/JUNE 2015
Online
Library
such modality is focused ultrasound, which is used by nonradiology specialists to ask targeted clinical questions (Moore and Copel, 2011). As ultrasound machines become increasingly portable, affordable, and readily available, medical training in anatomy has begun incorporating focused ultrasound in early medical education (Hoppmann et al., 2011; Bahner et al., 2014). Focused ultrasound augments students’ understanding of key anatomic structures and translates the information learned in textbooks and the cadaver laboratory (Gogalniceanu et al., 2010; Moore and Copel, 2011; Hammoudi et al., 2013). One area that ultrasound can be especially helpful is in allowing visual exploration of physical structures. However, naming sonographic landmarks can lead to confusion, especially when structures are termed by a small hyper-specialized group. As a case in point, this report explores the sonographic main lobar fissure (MLF), a common sonographic landmark that is rarely mentioned in modern anatomic textbooks. Anat Sci Educ 8:283–288 (2015)
Multiple Languages can be Confusing A major hindrance in learning anatomy is that the vocabulary varies among specialties. For example, anatomists refer to the supracristal plane as an anatomical transverse line at the level of the L4 vertebrae plane, whereas anesthesiologists call it the intercristal or Tuffier’s line (Snider et al., 2008; Baud et al., 2011; Mirjalili et al., 2012). A related confusion occurs when structures are misidentified using newer technologies such as ultrasound. For example, ocular sonographers believed that measurement of the dark borders behind the optic disk represented the optic nerve sheath diameter, an area sensitive to elevated intracranial pressure changes (Hall et al., 2013). Unfortunately, this is likely a shadowing artifact cast by the optic disk, and misattribution of this structure has led to considerable controversy as to the best way to assess elevated intracranial pressure using ultrasound (Blehar et al., 2008; Copetti and Cattarossi, 2009). In this report, these inconsistencies are highlighted in the case of the liver. The complexities of the liver have presented a longstanding challenge for physicians and anatomists to describe and teach, leading to multiple conventions for describing anatomical landmarks. Anatomical divisions. It is based on surface anatomy (the classical “lobes”). Only one of the three main liver fissures is visible on the parietal surface—the umbilical fissure formed by the falciform ligament. This fissure divides liver into the classical right and left lobes (Skandalakis et al., 2004; AbdelMisih and Bloomston, 2010). These are not the functional left and right lobes of the liver. On the inferior surface of the liver, the umbilical fissure continues as the notch for the ligamentum teres and fissure for the ligamentum venosum. The latter separates the caudate lobe from the classical right lobe. The quadrate lobe is a prominence on the inferior of the right lobe, but as discussed in the next section, it is functionally part of the left. Functional divisions. The functional segments of the liver are based on the territories of the portal vein, biliary system, and hepatic artery that travel through the center of each segment and the hepatic veins that run through nonvisible fissures that separate the segments. The fissure that separates the left and right livers contains the middle hepatic vein (Cantlie’s line). This functional division of the liver was initially proposed by a Scottish physician, Sir James Cantlie in 1898 whereby the liver was divided into left and right parts by the “midline” of the liver (later renamed Cantlie’s line), running anteriorly from a line between the long axis of the gallbladder fossa and middle of the inferior vena cava along the middle hepatic vein (Cantlie, 1897; Hata et al., 1999). This divide was cemented in 1953 by Healey and Schroy who made casts of the portal triad within the liver. The studies revealed a plane that separated the territories of the left and right hepatic arteries. Further, biliary ducts failed to cross this plane, which the authors called the “lobar fissure” (Healey and Schroy, 1953; Rutkauskas et al., 2006). At roughly the same time Healey and Schroy published their work, a French surgeon Claude Couinaud proposed a division for the functional (and surgical) right and left lobes of the liver based on the portal venous system (Couinaud, 1954). Couinaud developed several schemes to segment the liver, but considered his eight-portal-segment scheme to be the most important (Sutherland and Harris, 2002). The right liver contains segments V–VIII with segments V and VIII bordering Cantlie’s line. The right portal fissure, containing the right portal 284
vein, separates segments VI/VII from V/VIII. The left liver contains segments II–IV with segment IV and its quadrate lobe bordering Cantlie’s line. The left portal fissure, containing the left portal vein, separates segments II and III. Segment I, the caudate lobe has an independent system of hepatic veins and can be supplied by the left and right portal veins. The proposal that the functional left and right liver are supplied by left and right portal veins and hepatic arteries corresponds to Cantlie’s line and the lobar fissure proposed by Healey and Schroy (Ger, 1989; Rutkauskas et al., 2006). Further discussed along with anatomical variants of blood supply, this structure was renamed the “main lobar fissure” for the first time in 1966 (Michels, 1966). Other common names include the principal plane of the liver or principal hepatic fissure, which is preferred by many surgeons and anatomists (Ger, 1989; Gray et al., 1995). The Terminologia Anatomica term is “main portal fissure” (FCAT, 1998; Baud et al., 2011).
Which Aspects of the Liver Might Correspond to the Sonographic Main Lobar Fissure? The sonographic MLF was first described in 1979 as a “linear echo within the liver, seen best on parasagittal planes, which appeared to be a useful and reliable indicator of the location of the gallbladder” (Callen and Filly, 1979). Based on comparison with CT’s of the same region in that study of 100 patients, 68 of whom had a hyper-echoic structure connecting the gallbladder to the porta hepatis; the authors postulated that this hyper-echoic structure probably correlates with the cleft in the posteriomedial aspect of the visceral surface of the liver which corresponds to the (main) lobar fissure proposed by Healy and Schroy and cemented by Michels (Healy and Schroy, 1953; Michels, 1966; Callen and Filly, 1979). A second CT/sonogram study that included cadaveric livers, related the sonographic MLF to this cleft, but also a “main fissure” that connected the gallbladder to the right portal vein on cadaveric specimens (Sexton and Zeman, 1983). Although possible that the sonographic MLF corresponds to the echogenic tissue created by the fissure, an issue is that the authors of the sonographic MLF are taking a physical structure on the ultrasound screen and comparing it to the theoretical negative space which constitutes a fissure that is, in-part, intrahepatic according to the cast-model system proposed by Healy and Schroy (1953). By referencing their ultrasound findings to the MLF proposed by Health and Schroy, the sonographic term “main lobar fissure” was cemented, to be repeated in multiple ultrasound articles and ultrasound textbooks, and the “MLF” is now the ubiquitous name for the hyper-echoic landmark used to sonographically locate the gallbladder and the porta hepatis (Ghazle and Rubens, 2004; Hagen-Ansert, 2012). Nonetheless, in the authors’ experience with ultrasounds of this region, the sonographic MLF appears to be extrahepatic. When rotating the probe from the long axis view into the short axis, the sonographic MLF remains extrahepatic. Therefore, livers were excised from the cadavers that Yale medical students used in their dissection course. Because the sonographic MLF gives the appearance of linking the gallbladder to the porta hepatis, the pedicle of the gallbladder was examined. In 20 specimens, the length of the pedicle was variable and made an impression on the liver. Examples of long and short pedicles are shown in Figure 1.
Hall et al.
Figure 1. (A) A liver was dissected along the principal fissure to reveal the middle hepatic vein (MHV). The dissection bisects the gallbladder fossa (GBF). The gallbladder (GB) and cystic pedicle are reflected to one side. The inferior vena cava (IVC) was incised longitudinally. The arrow points to the porta hepatis. The box is enlarged in (B). The arrowheads delineate the ends of a trough on the visceral surface of the liver that houses branches of the portal triad and the cystic pedicle. Panels (C and D) show a second liver with the gallbladder in situ (C) or reflected to reveal a long trough between the gallbladder fossa and the porta hepatis (D). Panels (E and F) show a counter example where the trough between the gallbladder fossa and the porta hepatis was very short. Arrows, porta hepatis; arrowheads, trough for cystic pedicle.
DEMONSTRATION OF THE MAIN LOBAR FISSURE To demonstrate the relationship between the main portal fissure and the pedicle of the gallbladder, an incision was made along the length of the gallbladder fossa and cleft formed by the pedicle to the porta hepatis. Where the incision met the superficial surface of the liver at the distal tip of the gallbladder fossa, the incision was continued along the diaphragmatic surface to the inferior vena cava. As predicted by standard anatomy texts, the main portal fissure of the liver was revealed when the incisions were deepened (Gray et al., 1995; Standring, 2008). The plane was confirmed by the lonAnatomical Sciences Education
MAY/JUNE 2015
gitudinally bisected middle hepatic vein of the liver. Nothing unusual in the parenchyma was observed along this plane. (Figs. 1A and 1B). Similarly, no unusual features were noted by magnetic resonance imaging. To relate the main portal fissure of the liver and the coplanar cystic pedicle to the sonographic MLF, two livers were selected: one with a long and one with a short pedicle (Figs. 1D and 1F). The gallbladder and its pedicle were dissected from their fossa and groove. The livers were submerged in a tap-water bath to provide the proper acoustic window. They were scanned using a C6-2 curvilinear transducer, which is a 2–6 MHz broadband sector probe, and a Philips Sparq ultrasound system (Royal Philips Electronics, Amsterdam, The
285
Figure 2. Water bath ultrasound images of the liver (L) and gallbladder (GB) simulating an in vivo anterior abdominal approach. In panel (A) the sonographic cystic pedicle (SCP) is visible when the cystic pedicle and gallbladder occupy their fossa. In panel (B), when the gallbladder and cystic pedicle are reflected away from the gallbladder fossa (GBF), the SCP disappears from the region indicated by the box. A grazing section of the gallbladder is seen, but the cystic pedicle is out of the plane of the image. The pedicle can be seen moving out of the plane in the movie included in Supporting Information. Panel (C) Ultrasound of a liver that has a short cystic pedicle fails to reveal a SCP in the region of the box. Panel (D) An example of an in vivo ultrasound of a gallbladder in a long-axis view, with the SCP visible connecting the gallbladder (GB) to the portal vein in the vicinity of the porta hepatis (PH). Subtle fanning with the probe would reveal the portal triad in the porta hepatis (not shown). Courtesy of CLM and the resident teaching library, Yale University.
Netherlands). With the gallbladder in place, the hyper-echoic line contiguous with the gallbladder neck in a long-axis view was isolated but was only visible if the cystic pedicle was long. The gallbladder fundus, neck, and fatty pedicle were retracted while recording a continuous ultrasound clip. The signal disappeared when the cystic pedicle was removed from the impression it made in the liver and returned when the cystic pedicle was replaced (Fig. 2). The movie (Supporting Information) captures the signal as the cystic pedicle moves out of place, demonstrating that this structure is the source of the signal that has previously been named as the sonographic MLF. To further investigate this sonographic cystic pedicle, the hyper-echoic structure from the ultrasound image was examined histologically. The cystic pedicle from the specimen of Figures 1C and 1D was sectioned and stained by H&E, PAS, and Mallory trichrome. Although the histology was not as crisp as in freshly prepared tissue, the embalmed cadaveric samples revealed the typical histology of the cystic pedicle (Fig. 3). The cystic duct was surrounded by numerous mucous glands that have been characterized as stem cell niches (Sutton et al., 2012; Dipaola et al., 2013), and there was evidence of the spiral valve of Heister. Blood vessels were observed in the periductal fat. This echogenic structure 286
appeared to be within the normal limits for a typical cystic pedicle.
DISCUSSION Specialty-specific language can confuse clinical students two ways. First, simply naming the same structure differently makes it harder for a learner to synthesize information. For reasons of uniformity and practicality, anatomical societies have striven to develop a descriptive language whereby the name reveals information about the structure (Baud et al., 2011). Despite this good intention, once students leave the anatomy laboratory, the vast majority of subsequent instructors will use traditional names, typically eponyms (Mirjalili et al., 2012). The transition of students from anatomy to clinical courses is facilitated when eponyms and anatomic names are combined: the angle formed at the manubriosternal joint, the “sternal angle” or “angle of Louis,” becomes the “sternal angle of Louis,” as one example (Rizzolo, 2014). Clinicians at this institution who taught physical examination were amazed at how much “brighter” students appeared to be when this practice was first introduced. Sonographers have adopted many anatomical names for features of the liver. Although the field correctly identifies the Hall et al.
Figure 3. Cross-section of the cystic pedicle. Paraffin sections were stained with H & E and photographed at 4003 magnification. Arrows, clusters of glands; arrowhead, spiral valve of Heister.
deserves future study because of several interesting questions and limitations raised during this investigation. As the sonographic cystic pedicle is extrahepatic, there may be several reasons why approximately 30% of right upper quadrant ultrasounds exhibit a poorly visualized line (Callen and Filly, 1979): gallbladder function, pathology, and anatomic variants. First, the sonographic signal might be sensitive to preprandial and postprandial states. Second, it is not known how the sonographic cystic pedicle might change in pathologic states including neoplasms or inflammation due to infection or inflammation. Lastly, a clinical question arises that is particularly interesting and deserving of further investigation. In this study, the ex vivo liver with a short cystic pedicle on gross pathology did not have a sonographic cystic pedicle. It is known that a short cystic duct is one predictor of common bile duct injury during laparoscopic cholecystectomy surgery (Machado, 2011). For this commonly performed procedure, it stands to reason that a simple, noninvasive ultrasound study with a poorly visualized sonographic cystic pedicle could alert the surgeon to an incrementally difficult intraoperative course and potentially greater complications. For all of these reasons, this recharacterized extrahepatic structure deserves new attention in the anatomy classroom, as well as renewed study in the clinical arena.
ACKNOWLEDGMENTS portal vein or portal triad within the porta hepatis, “porta hepatis” would clarify the location of the structure. An example of a common eponym for the hepatorenal (subhepatic) recess is Morison’s pouch (Valleix et al., 1987; Hoppmann et al., 2011). The recess is clinically important, because this potential space becomes fluid filled in certain diseases and may be detected by ultrasonography or computed tomography. Applying the common strategy articulated above, anatomy instructors are encouraged to draw attention to this feature and identify it as the “hepatorenal recess of Morison.” The second, more troubling confusion, is illustrated by the sonographic MLF and main portal fissure. Rather than two names for the same structure, this confusion results from mistakenly believing that two names refer to the same structure. It has long been believed that the main portal fissure, Cantlie’s line, and the sonographic MLF were the same structure. Whereas it might be appropriate to identify the functional boundary of the left and right livers as the “main portal fissure of Cantlie,” the sonographic MLF is a different structure. Although the sonographic MLF lies along one edge of the plane described by Cantlie, it is a cylindrical extrahepatic structure that houses the cystic duct and associated glands, fat, and blood vessels. Terminologia Anatomica only mentions the cystic duct, but the surgical literature began using the more inclusive term “cystic pedicle” more than 20 years ago (Nathanson et al., 1991). Accordingly, the authors propose that anatomists and sonographers refer to this sonographic feature as the “sonographic cystic pedicle” to include the nonductal components of the structure. This contrasts with early radiologic studies state that the sonographic MLF is a fissure on the visceral surface of the liver (Callen and Filly, 1979; Sexton and Zeman, 1983). The importance of this new distinction lies in its classroom and clinical relevance. In the classroom, the “sonographic MLF” can now be linked with its corresponding structure. However, before doing so, the “sonographic cystic pedicle” Anatomical Sciences Education
MAY/JUNE 2015
The authors are grateful for the Donors who when they were alive willed their remains to the Yale Body Donation program for education, training, and research thereby making this study possible. Additionally, the authors thank Lucy Kornblith, M.D. for her guidance in preparing this manuscript.
NOTES ON CONTRIBUTORS M. KENNEDY HALL, M.D., is a clinical instructor and the chief ultrasound fellow in the Department of Emergency Medicine at the Yale University School of Medicine, New Haven, Connecticut. He teaches physician-performed ultrasound as part of the integrated first-year medical student gross anatomy curriculum. S. ALI MIRJALILI, M.D., Ph.D., P.G.Dip.Surg.Anat., P.G.Cert.C.P.U., is a clinician and lecturer in the Department of Anatomy with Radiology at the University of Auckland, School of Medicine, Auckland, New Zealand. He lectures on surgical and clinical anatomy at the university. CHRISTOPHER L. MOORE, M.D., R.D.M.S., R.D.C.S., is an associate professor of emergency medicine in the Department of Emergency Medicine at the Yale University School of Medicine, New Haven, Connecticut. He is the director of the Section of Emergency Ultrasound, and Director of the Emergency Ultrasound Fellowship. LAWRENCE J. RIZZOLO, Ph.D., F.A.R.V.O., is an associate professor and director of Medical Studies in the Section of Anatomy, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut. He directs the anatomy course for medical students and has a research programs in curriculum development and in retinal cell biology. LITERATURE CITED Abdel-Misih SR, Bloomston M. 2010. Liver anatomy. Surg Clin North Am 90: 643–653.
287
Bahner DP, Goldman E, Way D, Royall NA, Liu YT. 2014. The state of ultrasound education in U.S. medical schools: Results of a national survey. Acad Med 89:1681–1686. Baud RH, Neumann PE, Sprumont P (Editors). 2011. Terminologia Anatomica 1998 On-line Version. Federative International Programme on Anatomical Terminologies. Universite de Fribourg, Fribourg, Switzerland. URL: http://www. unifr.ch/ifaa/Public/EntryPage/HomePublic.html [accessed 1 December 2014]. Blehar DJ, Gaspari RJ, Montoya A, Calderon R. 2008. Correlation of visual axis and coronal axis measurements of the optic nerve sheath diameter. J Ultrasound Med 27:407–411. Callen PW, Filly RA. 1979. Ultrasonographic localization of the gallbladder. Radiology 133:687–691. Cantlie J. 1897. On a new arrangement of the right and left lobes of the liver. Proc Anat Soc Great Brit Ireland 32:4–9. Chowdhury R, Wilson ID, Oeppen RS. 2008. The departments of radiology and anatomy: New symbiotic relations? Clin Radiol 63:918–920. Copetti R, Cattarossi L. 2009. Optic nerve ultrasound: Artifacts and real images. Intensive Care Med 35:1488–1489. Couinaud C. 1954. Liver lobes and segments: Notes on the anatomical architecture and surgery of the liver. Presse Med 62:709–712. Dipaola F, Shivakumar P, Pfister J, Walters S, Sabla G, Bezerra JA. 2013. Identification of intramural epithelial networks linked to peribiliary glands that express progenitor cell markers and proliferate after injury in mice. Hepatology 58:1486–1496. FCAT. 1998. Federative Committee on Anatomical Terminology, Terminologia Anatomica: International Anatomical Terminology. 1st Ed. Stuttgart, Germany: Thieme. 292 p. Ger R. 1989. Surgical anatomy of the liver. Surg Clin North Am 69:179–191. Ghazle H, Rubens DJ. 2004. The liver. In: Dogra V, Rubens DJ (Editors). Ultrasound Secrets: Questions and Answers Reveal the Secrets to Skillful Ultrasound Examination and Diagnosis. 1st Ed. Philadelphia, PA: Hanley & Belfus. p 130–149. Gogalniceanu P, Sheena Y, Kashef E, Purkayastha S, Darzi A, Paraskeva P. 2010. Is basic emergency ultrasound training feasible as part of standard undergraduate medical education? J Surg Educ 67:152–156. Gray H, Williams PL, Bannister LH. 1995. Gray’s Anatomy: The Anatomical Basis of Medicine and Surgery. 38th Ed. New York, NY: Churchill Livingstone. 2092 p. Hagen-Ansert SL. 2012. The liver. In: Hagen-Ansert SL (Editor). Textbook of Diagnostic Sonography. 7th Ed. Maryland Heights, MO: Mosby, Inc. p 205– 266. Hall MK, Spiro DM, Sabbaj A, Moore CL, Hopkins KL, Meckler GD. 2013. Bedside optic nerve sheath diameter ultrasound for the evaluation of suspected pediatric ventriculoperitoneal shunt failure in the emergency department. Childs Nerv Syst 29:2275–2280. Hammoudi N, Arangalage D, Boubrit L, Renaud MC, Isnard R, Collet JP, Cohen A, Duguet A. 2013. Ultrasound-based teaching of cardiac anatomy and physiology to undergraduate medical students. Arch Cardiovasc Dis 106:487–491.
288
Hata F, Hirata K, Murakami GEN, Mukaiya M. 1999. Identification of segments VI and VII of the liver based on the ramification patterns of the intrahepatic portal and hepatic veins. Clin Anat 244:229–244. Healey JE Jr, Schroy PC. 1953. Anatomy of the biliary ducts within the human liver: Analysis of the prevailing pattern of branchings and the major variations of the biliary ducts. AMA Arch Surg 6:599–616. Hoppmann RA, Rao VV, Poston MB, Howe DB, Hunt PS, Fowler SD, Paulman LE, Wells JR, Richeson NA, Catalana PV, Thomas LK, Britt Wilson L, Cook T, Riffle S, Neuffer FH, McCallum JB, Keisler BD, Brown RS, Gregg AR, Sims KM, Powell CK, Garber MD, Morrison JE, Owens WB, Carnevale KA, Jennings WR, Fletcher S. 2011. An integrated ultrasound curriculum (iUSC) for medical students: 4-year experience. Crit Ultrasound J 3:1–12. Machado JA, Barbosa JM, Ferreira MA. 2013. Student perspectives of imaging anatomy in undergraduate medical education. Anat Sci Educ 6:163–169. Machado NO. 2011. Biliary complications postlaparoscopic cholecystectomy: Mechanism, preventive measures, and approach to management: A review. Diagn Ther Endosc 2011:967017. Michels NA. 1966. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg 112:337–347. Mirjalili SA, McFadden SL, Buckenham T, Wilson B, Stringer MD. 2012. Anatomical planes: Are we teaching accurate surface anatomy? Clin Anat 25:819– 826. Moore CL, Copel JA. 2011. Point-of-care ultrasonography. N Engl J Med 364: 749–757. Nathanson LK, Easter DW, Cuschieri A. 1991. Ligation of the structures of the cystic pedicle during laparoscopic cholecystectomy. Am J Surg 161:350–354. Rizzolo LJ (Editor). 2014. Anatomy Clinic. Human Anatomy and Development: Dissection, Radiology and Web Exercises. Department of Surgery, Yale University School of Medicine, New Haven, CT. URL: http://www.anatomy. yalemedicine.org/ [accessed 1 December 2014]. Rutkauskas S, Gedrimas V, Pundzius J, Barauskas G, Basevicius A. 2006. Clinical and anatomical basis for the classification of the structural parts of liver. Medicina (Kaunas) 42:98–106. Sexton CC, Zeman RK. 1983. Correlation of computed tomography, sonography, and gross anatomy of the liver. Am J Roentgenol 141:711–718. Skandalakis JE, Skandalakis LJ, Skandalakis PN, Mirilas P. 2004. Hepatic surgical anatomy. Surg Clin North Am 84:413–435. Snider KT, Kribs JW, Snider EJ, Degenhardt BF, Bukowski A, Johnson JC. 2008. Reliability of Tuffier’s line as an anatomic landmark. Spine 33:E161–E165. Standring S (Editor). 2008. Gray’s Anatomy: The Anatomical Basis of Clinical Practice. 40th. Ed. London, UK: Churchill Livingston. 1576 p. Sutherland F, Harris J. 2002. Claude Couinaud: A passion for the liver. Arch Surg 137:1305–1310. Sutton ME, Op den Dries S, Koster MH, Lisman T, Gouw AS, Porte RJ. 2012. Regeneration of human extrahepatic biliary epithelium: The peribiliary glands as progenitor cell compartment. Liver Int 32:554–559. Valleix D, Sautereau D, Pouget X, Descottes B, Outrequin G, Hureau J, Caix M. 1987. Ultrasonographic anatomy of the liver. Surg Radiol Anat 9:123–134.
Hall et al.
The Student’s Dilemma, Liver Edition: Incorporating the Sonographer’s Language Into Clinical Anatomy Education M. Kennedy Hall,1 S. Ali Mirjalili,2 Christopher L. Moore,1 Lawrence J. Rizzolo3* 1 Department of Emergency Medicine, Yale University, School of Medicine, New Haven, Connecticut 2 Department of Anatomy with Radiology, Faculty of Medical and Health Sciences, School of Medical Sciences, University of Auckland, Auckland, New Zealand 3 Department of Surgery, Yale University, School of Medicine, New Haven, Connecticut
Anatomy students are often confused by multiple names ascribed to the same structure by different clinical disciplines. Increasingly, sonography is being incorporated into clinical anatomical education, but ultrasound textbooks often use names unfamiliar to the anatomist. Confusion is worsened when ultrasound names ascribed to the same structure actually refer to different structures. Consider the sonographic main lobar fissure (MLF). The sonographic MLF is a hyper-echoic landmark used by sonographers of the right upper quadrant. Found in approximately 70% of people, there is little consensus on what the sonographic MLF is anatomically. This structure appears to be related to the main portal fissure (aka principal plane of the liver or principal hepatic fissure), initially described by anatomists and surgeons as in intrahepatic division along the middle hepatic vein which in essence divides the territories of the left and right hepatic arteries and biliary systems. By exploring the relationship between the main portal fissure and the sonographic MLF in cadaveric livers ex vivo, the data suggest the sonographic MLF is actually an extrahepatic structure that parallels the rim of the main portal fissure. The authors recommend that this structure be renamed the “sonographic cystic pedicle,” which includes the cystic duct and ensheathing fat and blood vessels. In the context of the redefined underlying anatomy, the absence of the sonographic cystic pedicle due to anatomic variation may serve an important clinical role in predicting complications from difficult laparoscopic cholecystectomies and is deserving of future study. Anat Sci Educ C 2015 American Association of Anatomists. 8: 283–288. V
Key words: gross anatomy education; medical education; ultrasonographic examination; anatomical sciences; emergency medicine; liver divisions; main lobar fissure; cystic duct
INTRODUCTION New radiological imaging modalities are rapidly gaining applicability in medical education as tools for addressing basic science questions and for supplementing traditional modes of learning (Chowdhury et al., 2008; Machado et al., 2013). One *Correspondence to: Dr. Lawrence J. Rizzolo; Department of Surgery, Yale University, PO Box 208062, New Haven, Connecticut, USA. E-mail: [email protected] Additional Supporting Information may be found in the online version of this article. Received 16 August 2014; Revised 2 December 2014; Accepted 22 December 2014. Published online 8 January 2015 in Wiley (wileyonlinelibrary.com). DOI 10.1002/ase.1518 C 2015 American Association of Anatomists V
Anatomical Sciences Education
MAY/JUNE 2015
Online
Library
such modality is focused ultrasound, which is used by nonradiology specialists to ask targeted clinical questions (Moore and Copel, 2011). As ultrasound machines become increasingly portable, affordable, and readily available, medical training in anatomy has begun incorporating focused ultrasound in early medical education (Hoppmann et al., 2011; Bahner et al., 2014). Focused ultrasound augments students’ understanding of key anatomic structures and translates the information learned in textbooks and the cadaver laboratory (Gogalniceanu et al., 2010; Moore and Copel, 2011; Hammoudi et al., 2013). One area that ultrasound can be especially helpful is in allowing visual exploration of physical structures. However, naming sonographic landmarks can lead to confusion, especially when structures are termed by a small hyper-specialized group. As a case in point, this report explores the sonographic main lobar fissure (MLF), a common sonographic landmark that is rarely mentioned in modern anatomic textbooks. Anat Sci Educ 8:283–288 (2015)
Multiple Languages can be Confusing A major hindrance in learning anatomy is that the vocabulary varies among specialties. For example, anatomists refer to the supracristal plane as an anatomical transverse line at the level of the L4 vertebrae plane, whereas anesthesiologists call it the intercristal or Tuffier’s line (Snider et al., 2008; Baud et al., 2011; Mirjalili et al., 2012). A related confusion occurs when structures are misidentified using newer technologies such as ultrasound. For example, ocular sonographers believed that measurement of the dark borders behind the optic disk represented the optic nerve sheath diameter, an area sensitive to elevated intracranial pressure changes (Hall et al., 2013). Unfortunately, this is likely a shadowing artifact cast by the optic disk, and misattribution of this structure has led to considerable controversy as to the best way to assess elevated intracranial pressure using ultrasound (Blehar et al., 2008; Copetti and Cattarossi, 2009). In this report, these inconsistencies are highlighted in the case of the liver. The complexities of the liver have presented a longstanding challenge for physicians and anatomists to describe and teach, leading to multiple conventions for describing anatomical landmarks. Anatomical divisions. It is based on surface anatomy (the classical “lobes”). Only one of the three main liver fissures is visible on the parietal surface—the umbilical fissure formed by the falciform ligament. This fissure divides liver into the classical right and left lobes (Skandalakis et al., 2004; AbdelMisih and Bloomston, 2010). These are not the functional left and right lobes of the liver. On the inferior surface of the liver, the umbilical fissure continues as the notch for the ligamentum teres and fissure for the ligamentum venosum. The latter separates the caudate lobe from the classical right lobe. The quadrate lobe is a prominence on the inferior of the right lobe, but as discussed in the next section, it is functionally part of the left. Functional divisions. The functional segments of the liver are based on the territories of the portal vein, biliary system, and hepatic artery that travel through the center of each segment and the hepatic veins that run through nonvisible fissures that separate the segments. The fissure that separates the left and right livers contains the middle hepatic vein (Cantlie’s line). This functional division of the liver was initially proposed by a Scottish physician, Sir James Cantlie in 1898 whereby the liver was divided into left and right parts by the “midline” of the liver (later renamed Cantlie’s line), running anteriorly from a line between the long axis of the gallbladder fossa and middle of the inferior vena cava along the middle hepatic vein (Cantlie, 1897; Hata et al., 1999). This divide was cemented in 1953 by Healey and Schroy who made casts of the portal triad within the liver. The studies revealed a plane that separated the territories of the left and right hepatic arteries. Further, biliary ducts failed to cross this plane, which the authors called the “lobar fissure” (Healey and Schroy, 1953; Rutkauskas et al., 2006). At roughly the same time Healey and Schroy published their work, a French surgeon Claude Couinaud proposed a division for the functional (and surgical) right and left lobes of the liver based on the portal venous system (Couinaud, 1954). Couinaud developed several schemes to segment the liver, but considered his eight-portal-segment scheme to be the most important (Sutherland and Harris, 2002). The right liver contains segments V–VIII with segments V and VIII bordering Cantlie’s line. The right portal fissure, containing the right portal 284
vein, separates segments VI/VII from V/VIII. The left liver contains segments II–IV with segment IV and its quadrate lobe bordering Cantlie’s line. The left portal fissure, containing the left portal vein, separates segments II and III. Segment I, the caudate lobe has an independent system of hepatic veins and can be supplied by the left and right portal veins. The proposal that the functional left and right liver are supplied by left and right portal veins and hepatic arteries corresponds to Cantlie’s line and the lobar fissure proposed by Healey and Schroy (Ger, 1989; Rutkauskas et al., 2006). Further discussed along with anatomical variants of blood supply, this structure was renamed the “main lobar fissure” for the first time in 1966 (Michels, 1966). Other common names include the principal plane of the liver or principal hepatic fissure, which is preferred by many surgeons and anatomists (Ger, 1989; Gray et al., 1995). The Terminologia Anatomica term is “main portal fissure” (FCAT, 1998; Baud et al., 2011).
Which Aspects of the Liver Might Correspond to the Sonographic Main Lobar Fissure? The sonographic MLF was first described in 1979 as a “linear echo within the liver, seen best on parasagittal planes, which appeared to be a useful and reliable indicator of the location of the gallbladder” (Callen and Filly, 1979). Based on comparison with CT’s of the same region in that study of 100 patients, 68 of whom had a hyper-echoic structure connecting the gallbladder to the porta hepatis; the authors postulated that this hyper-echoic structure probably correlates with the cleft in the posteriomedial aspect of the visceral surface of the liver which corresponds to the (main) lobar fissure proposed by Healy and Schroy and cemented by Michels (Healy and Schroy, 1953; Michels, 1966; Callen and Filly, 1979). A second CT/sonogram study that included cadaveric livers, related the sonographic MLF to this cleft, but also a “main fissure” that connected the gallbladder to the right portal vein on cadaveric specimens (Sexton and Zeman, 1983). Although possible that the sonographic MLF corresponds to the echogenic tissue created by the fissure, an issue is that the authors of the sonographic MLF are taking a physical structure on the ultrasound screen and comparing it to the theoretical negative space which constitutes a fissure that is, in-part, intrahepatic according to the cast-model system proposed by Healy and Schroy (1953). By referencing their ultrasound findings to the MLF proposed by Health and Schroy, the sonographic term “main lobar fissure” was cemented, to be repeated in multiple ultrasound articles and ultrasound textbooks, and the “MLF” is now the ubiquitous name for the hyper-echoic landmark used to sonographically locate the gallbladder and the porta hepatis (Ghazle and Rubens, 2004; Hagen-Ansert, 2012). Nonetheless, in the authors’ experience with ultrasounds of this region, the sonographic MLF appears to be extrahepatic. When rotating the probe from the long axis view into the short axis, the sonographic MLF remains extrahepatic. Therefore, livers were excised from the cadavers that Yale medical students used in their dissection course. Because the sonographic MLF gives the appearance of linking the gallbladder to the porta hepatis, the pedicle of the gallbladder was examined. In 20 specimens, the length of the pedicle was variable and made an impression on the liver. Examples of long and short pedicles are shown in Figure 1.
Hall et al.
Figure 1. (A) A liver was dissected along the principal fissure to reveal the middle hepatic vein (MHV). The dissection bisects the gallbladder fossa (GBF). The gallbladder (GB) and cystic pedicle are reflected to one side. The inferior vena cava (IVC) was incised longitudinally. The arrow points to the porta hepatis. The box is enlarged in (B). The arrowheads delineate the ends of a trough on the visceral surface of the liver that houses branches of the portal triad and the cystic pedicle. Panels (C and D) show a second liver with the gallbladder in situ (C) or reflected to reveal a long trough between the gallbladder fossa and the porta hepatis (D). Panels (E and F) show a counter example where the trough between the gallbladder fossa and the porta hepatis was very short. Arrows, porta hepatis; arrowheads, trough for cystic pedicle.
DEMONSTRATION OF THE MAIN LOBAR FISSURE To demonstrate the relationship between the main portal fissure and the pedicle of the gallbladder, an incision was made along the length of the gallbladder fossa and cleft formed by the pedicle to the porta hepatis. Where the incision met the superficial surface of the liver at the distal tip of the gallbladder fossa, the incision was continued along the diaphragmatic surface to the inferior vena cava. As predicted by standard anatomy texts, the main portal fissure of the liver was revealed when the incisions were deepened (Gray et al., 1995; Standring, 2008). The plane was confirmed by the lonAnatomical Sciences Education
MAY/JUNE 2015
gitudinally bisected middle hepatic vein of the liver. Nothing unusual in the parenchyma was observed along this plane. (Figs. 1A and 1B). Similarly, no unusual features were noted by magnetic resonance imaging. To relate the main portal fissure of the liver and the coplanar cystic pedicle to the sonographic MLF, two livers were selected: one with a long and one with a short pedicle (Figs. 1D and 1F). The gallbladder and its pedicle were dissected from their fossa and groove. The livers were submerged in a tap-water bath to provide the proper acoustic window. They were scanned using a C6-2 curvilinear transducer, which is a 2–6 MHz broadband sector probe, and a Philips Sparq ultrasound system (Royal Philips Electronics, Amsterdam, The
285
Figure 2. Water bath ultrasound images of the liver (L) and gallbladder (GB) simulating an in vivo anterior abdominal approach. In panel (A) the sonographic cystic pedicle (SCP) is visible when the cystic pedicle and gallbladder occupy their fossa. In panel (B), when the gallbladder and cystic pedicle are reflected away from the gallbladder fossa (GBF), the SCP disappears from the region indicated by the box. A grazing section of the gallbladder is seen, but the cystic pedicle is out of the plane of the image. The pedicle can be seen moving out of the plane in the movie included in Supporting Information. Panel (C) Ultrasound of a liver that has a short cystic pedicle fails to reveal a SCP in the region of the box. Panel (D) An example of an in vivo ultrasound of a gallbladder in a long-axis view, with the SCP visible connecting the gallbladder (GB) to the portal vein in the vicinity of the porta hepatis (PH). Subtle fanning with the probe would reveal the portal triad in the porta hepatis (not shown). Courtesy of CLM and the resident teaching library, Yale University.
Netherlands). With the gallbladder in place, the hyper-echoic line contiguous with the gallbladder neck in a long-axis view was isolated but was only visible if the cystic pedicle was long. The gallbladder fundus, neck, and fatty pedicle were retracted while recording a continuous ultrasound clip. The signal disappeared when the cystic pedicle was removed from the impression it made in the liver and returned when the cystic pedicle was replaced (Fig. 2). The movie (Supporting Information) captures the signal as the cystic pedicle moves out of place, demonstrating that this structure is the source of the signal that has previously been named as the sonographic MLF. To further investigate this sonographic cystic pedicle, the hyper-echoic structure from the ultrasound image was examined histologically. The cystic pedicle from the specimen of Figures 1C and 1D was sectioned and stained by H&E, PAS, and Mallory trichrome. Although the histology was not as crisp as in freshly prepared tissue, the embalmed cadaveric samples revealed the typical histology of the cystic pedicle (Fig. 3). The cystic duct was surrounded by numerous mucous glands that have been characterized as stem cell niches (Sutton et al., 2012; Dipaola et al., 2013), and there was evidence of the spiral valve of Heister. Blood vessels were observed in the periductal fat. This echogenic structure 286
appeared to be within the normal limits for a typical cystic pedicle.
DISCUSSION Specialty-specific language can confuse clinical students two ways. First, simply naming the same structure differently makes it harder for a learner to synthesize information. For reasons of uniformity and practicality, anatomical societies have striven to develop a descriptive language whereby the name reveals information about the structure (Baud et al., 2011). Despite this good intention, once students leave the anatomy laboratory, the vast majority of subsequent instructors will use traditional names, typically eponyms (Mirjalili et al., 2012). The transition of students from anatomy to clinical courses is facilitated when eponyms and anatomic names are combined: the angle formed at the manubriosternal joint, the “sternal angle” or “angle of Louis,” becomes the “sternal angle of Louis,” as one example (Rizzolo, 2014). Clinicians at this institution who taught physical examination were amazed at how much “brighter” students appeared to be when this practice was first introduced. Sonographers have adopted many anatomical names for features of the liver. Although the field correctly identifies the Hall et al.
Figure 3. Cross-section of the cystic pedicle. Paraffin sections were stained with H & E and photographed at 4003 magnification. Arrows, clusters of glands; arrowhead, spiral valve of Heister.
deserves future study because of several interesting questions and limitations raised during this investigation. As the sonographic cystic pedicle is extrahepatic, there may be several reasons why approximately 30% of right upper quadrant ultrasounds exhibit a poorly visualized line (Callen and Filly, 1979): gallbladder function, pathology, and anatomic variants. First, the sonographic signal might be sensitive to preprandial and postprandial states. Second, it is not known how the sonographic cystic pedicle might change in pathologic states including neoplasms or inflammation due to infection or inflammation. Lastly, a clinical question arises that is particularly interesting and deserving of further investigation. In this study, the ex vivo liver with a short cystic pedicle on gross pathology did not have a sonographic cystic pedicle. It is known that a short cystic duct is one predictor of common bile duct injury during laparoscopic cholecystectomy surgery (Machado, 2011). For this commonly performed procedure, it stands to reason that a simple, noninvasive ultrasound study with a poorly visualized sonographic cystic pedicle could alert the surgeon to an incrementally difficult intraoperative course and potentially greater complications. For all of these reasons, this recharacterized extrahepatic structure deserves new attention in the anatomy classroom, as well as renewed study in the clinical arena.
ACKNOWLEDGMENTS portal vein or portal triad within the porta hepatis, “porta hepatis” would clarify the location of the structure. An example of a common eponym for the hepatorenal (subhepatic) recess is Morison’s pouch (Valleix et al., 1987; Hoppmann et al., 2011). The recess is clinically important, because this potential space becomes fluid filled in certain diseases and may be detected by ultrasonography or computed tomography. Applying the common strategy articulated above, anatomy instructors are encouraged to draw attention to this feature and identify it as the “hepatorenal recess of Morison.” The second, more troubling confusion, is illustrated by the sonographic MLF and main portal fissure. Rather than two names for the same structure, this confusion results from mistakenly believing that two names refer to the same structure. It has long been believed that the main portal fissure, Cantlie’s line, and the sonographic MLF were the same structure. Whereas it might be appropriate to identify the functional boundary of the left and right livers as the “main portal fissure of Cantlie,” the sonographic MLF is a different structure. Although the sonographic MLF lies along one edge of the plane described by Cantlie, it is a cylindrical extrahepatic structure that houses the cystic duct and associated glands, fat, and blood vessels. Terminologia Anatomica only mentions the cystic duct, but the surgical literature began using the more inclusive term “cystic pedicle” more than 20 years ago (Nathanson et al., 1991). Accordingly, the authors propose that anatomists and sonographers refer to this sonographic feature as the “sonographic cystic pedicle” to include the nonductal components of the structure. This contrasts with early radiologic studies state that the sonographic MLF is a fissure on the visceral surface of the liver (Callen and Filly, 1979; Sexton and Zeman, 1983). The importance of this new distinction lies in its classroom and clinical relevance. In the classroom, the “sonographic MLF” can now be linked with its corresponding structure. However, before doing so, the “sonographic cystic pedicle” Anatomical Sciences Education
MAY/JUNE 2015
The authors are grateful for the Donors who when they were alive willed their remains to the Yale Body Donation program for education, training, and research thereby making this study possible. Additionally, the authors thank Lucy Kornblith, M.D. for her guidance in preparing this manuscript.
NOTES ON CONTRIBUTORS M. KENNEDY HALL, M.D., is a clinical instructor and the chief ultrasound fellow in the Department of Emergency Medicine at the Yale University School of Medicine, New Haven, Connecticut. He teaches physician-performed ultrasound as part of the integrated first-year medical student gross anatomy curriculum. S. ALI MIRJALILI, M.D., Ph.D., P.G.Dip.Surg.Anat., P.G.Cert.C.P.U., is a clinician and lecturer in the Department of Anatomy with Radiology at the University of Auckland, School of Medicine, Auckland, New Zealand. He lectures on surgical and clinical anatomy at the university. CHRISTOPHER L. MOORE, M.D., R.D.M.S., R.D.C.S., is an associate professor of emergency medicine in the Department of Emergency Medicine at the Yale University School of Medicine, New Haven, Connecticut. He is the director of the Section of Emergency Ultrasound, and Director of the Emergency Ultrasound Fellowship. LAWRENCE J. RIZZOLO, Ph.D., F.A.R.V.O., is an associate professor and director of Medical Studies in the Section of Anatomy, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut. He directs the anatomy course for medical students and has a research programs in curriculum development and in retinal cell biology. LITERATURE CITED Abdel-Misih SR, Bloomston M. 2010. Liver anatomy. Surg Clin North Am 90: 643–653.
287
Bahner DP, Goldman E, Way D, Royall NA, Liu YT. 2014. The state of ultrasound education in U.S. medical schools: Results of a national survey. Acad Med 89:1681–1686. Baud RH, Neumann PE, Sprumont P (Editors). 2011. Terminologia Anatomica 1998 On-line Version. Federative International Programme on Anatomical Terminologies. Universite de Fribourg, Fribourg, Switzerland. URL: http://www. unifr.ch/ifaa/Public/EntryPage/HomePublic.html [accessed 1 December 2014]. Blehar DJ, Gaspari RJ, Montoya A, Calderon R. 2008. Correlation of visual axis and coronal axis measurements of the optic nerve sheath diameter. J Ultrasound Med 27:407–411. Callen PW, Filly RA. 1979. Ultrasonographic localization of the gallbladder. Radiology 133:687–691. Cantlie J. 1897. On a new arrangement of the right and left lobes of the liver. Proc Anat Soc Great Brit Ireland 32:4–9. Chowdhury R, Wilson ID, Oeppen RS. 2008. The departments of radiology and anatomy: New symbiotic relations? Clin Radiol 63:918–920. Copetti R, Cattarossi L. 2009. Optic nerve ultrasound: Artifacts and real images. Intensive Care Med 35:1488–1489. Couinaud C. 1954. Liver lobes and segments: Notes on the anatomical architecture and surgery of the liver. Presse Med 62:709–712. Dipaola F, Shivakumar P, Pfister J, Walters S, Sabla G, Bezerra JA. 2013. Identification of intramural epithelial networks linked to peribiliary glands that express progenitor cell markers and proliferate after injury in mice. Hepatology 58:1486–1496. FCAT. 1998. Federative Committee on Anatomical Terminology, Terminologia Anatomica: International Anatomical Terminology. 1st Ed. Stuttgart, Germany: Thieme. 292 p. Ger R. 1989. Surgical anatomy of the liver. Surg Clin North Am 69:179–191. Ghazle H, Rubens DJ. 2004. The liver. In: Dogra V, Rubens DJ (Editors). Ultrasound Secrets: Questions and Answers Reveal the Secrets to Skillful Ultrasound Examination and Diagnosis. 1st Ed. Philadelphia, PA: Hanley & Belfus. p 130–149. Gogalniceanu P, Sheena Y, Kashef E, Purkayastha S, Darzi A, Paraskeva P. 2010. Is basic emergency ultrasound training feasible as part of standard undergraduate medical education? J Surg Educ 67:152–156. Gray H, Williams PL, Bannister LH. 1995. Gray’s Anatomy: The Anatomical Basis of Medicine and Surgery. 38th Ed. New York, NY: Churchill Livingstone. 2092 p. Hagen-Ansert SL. 2012. The liver. In: Hagen-Ansert SL (Editor). Textbook of Diagnostic Sonography. 7th Ed. Maryland Heights, MO: Mosby, Inc. p 205– 266. Hall MK, Spiro DM, Sabbaj A, Moore CL, Hopkins KL, Meckler GD. 2013. Bedside optic nerve sheath diameter ultrasound for the evaluation of suspected pediatric ventriculoperitoneal shunt failure in the emergency department. Childs Nerv Syst 29:2275–2280. Hammoudi N, Arangalage D, Boubrit L, Renaud MC, Isnard R, Collet JP, Cohen A, Duguet A. 2013. Ultrasound-based teaching of cardiac anatomy and physiology to undergraduate medical students. Arch Cardiovasc Dis 106:487–491.
288
Hata F, Hirata K, Murakami GEN, Mukaiya M. 1999. Identification of segments VI and VII of the liver based on the ramification patterns of the intrahepatic portal and hepatic veins. Clin Anat 244:229–244. Healey JE Jr, Schroy PC. 1953. Anatomy of the biliary ducts within the human liver: Analysis of the prevailing pattern of branchings and the major variations of the biliary ducts. AMA Arch Surg 6:599–616. Hoppmann RA, Rao VV, Poston MB, Howe DB, Hunt PS, Fowler SD, Paulman LE, Wells JR, Richeson NA, Catalana PV, Thomas LK, Britt Wilson L, Cook T, Riffle S, Neuffer FH, McCallum JB, Keisler BD, Brown RS, Gregg AR, Sims KM, Powell CK, Garber MD, Morrison JE, Owens WB, Carnevale KA, Jennings WR, Fletcher S. 2011. An integrated ultrasound curriculum (iUSC) for medical students: 4-year experience. Crit Ultrasound J 3:1–12. Machado JA, Barbosa JM, Ferreira MA. 2013. Student perspectives of imaging anatomy in undergraduate medical education. Anat Sci Educ 6:163–169. Machado NO. 2011. Biliary complications postlaparoscopic cholecystectomy: Mechanism, preventive measures, and approach to management: A review. Diagn Ther Endosc 2011:967017. Michels NA. 1966. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg 112:337–347. Mirjalili SA, McFadden SL, Buckenham T, Wilson B, Stringer MD. 2012. Anatomical planes: Are we teaching accurate surface anatomy? Clin Anat 25:819– 826. Moore CL, Copel JA. 2011. Point-of-care ultrasonography. N Engl J Med 364: 749–757. Nathanson LK, Easter DW, Cuschieri A. 1991. Ligation of the structures of the cystic pedicle during laparoscopic cholecystectomy. Am J Surg 161:350–354. Rizzolo LJ (Editor). 2014. Anatomy Clinic. Human Anatomy and Development: Dissection, Radiology and Web Exercises. Department of Surgery, Yale University School of Medicine, New Haven, CT. URL: http://www.anatomy. yalemedicine.org/ [accessed 1 December 2014]. Rutkauskas S, Gedrimas V, Pundzius J, Barauskas G, Basevicius A. 2006. Clinical and anatomical basis for the classification of the structural parts of liver. Medicina (Kaunas) 42:98–106. Sexton CC, Zeman RK. 1983. Correlation of computed tomography, sonography, and gross anatomy of the liver. Am J Roentgenol 141:711–718. Skandalakis JE, Skandalakis LJ, Skandalakis PN, Mirilas P. 2004. Hepatic surgical anatomy. Surg Clin North Am 84:413–435. Snider KT, Kribs JW, Snider EJ, Degenhardt BF, Bukowski A, Johnson JC. 2008. Reliability of Tuffier’s line as an anatomic landmark. Spine 33:E161–E165. Standring S (Editor). 2008. Gray’s Anatomy: The Anatomical Basis of Clinical Practice. 40th. Ed. London, UK: Churchill Livingston. 1576 p. Sutherland F, Harris J. 2002. Claude Couinaud: A passion for the liver. Arch Surg 137:1305–1310. Sutton ME, Op den Dries S, Koster MH, Lisman T, Gouw AS, Porte RJ. 2012. Regeneration of human extrahepatic biliary epithelium: The peribiliary glands as progenitor cell compartment. Liver Int 32:554–559. Valleix D, Sautereau D, Pouget X, Descottes B, Outrequin G, Hureau J, Caix M. 1987. Ultrasonographic anatomy of the liver. Surg Radiol Anat 9:123–134.
Hall et al.
