Opinion Review Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Exp Med. Jun 20, 2024; 14(2): 92157
Published online Jun 20, 2024. doi: 10.5493/wjem.v14.i2.92157
Liver surface depressions in the presence of diaphragmatic muscular bands on trans-illumination
Shamir O Cawich, Department of Surgery, University of the West Indies, St Augustine, Trinidad and Tobago
Michael T Gardner, Ramanand Shetty, Jean Pierre Louboutin, Zenica Dabichan, Section of Anatomy, Department of Basic Medical Sciences, University of the West Indies, Kingston KIN7, Jamaica
Shaneeta Johnson, Department of Surgery, Morehouse School of Medicine, Atlanta, GA 30310, United States
ORCID number: Shamir O Cawich (0000-0003-3377-0303); Michael T Gardner (0000-0002-0352-7022); Ramanand Shetty (0000-0002-3190-0533).
Author contributions: Cawich SO, Gardner MT, Shetty R, Louboutin JP and Johnson S designed the research; Cawich SO, Gardner MT and Shetty R performed the research; Cawich SO, Gardner MT and Shetty R wrote the paper; Shetty R, Louboutin JP and Johnson S contributed analytic tools; Shetty R, Louboutin JP and Dabichan Z analyzed the data.
Conflict-of-interest statement: There are no conflicts of interest to declare for any of the authors.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Shamir O Cawich, FACS, Professor, Department of Surgery, University of the West Indies, St. Augustine Campus, St Augustine, Trinidad and Tobago. socawich@hotmail.com
Received: January 20, 2024
Revised: February 6, 2024
Accepted: March 18, 2024
Published online: June 20, 2024
Processing time: 150 Days and 12.1 Hours

Abstract

Traditional descriptions of liver anatomy refer to a smooth, convex surface contacting the diaphragm. Surface depressions are recognized anatomic variants. There are many theories to explain the cause of the depressions. We discuss the theory that these are caused by hypertrophic muscular bands in the diaphragm.

Key Words: Liver; Anatomy; Depressions; Fissure; Groove; Sulcus; Variant

Core Tip: Surface depressions of the liver are a recognized anatomic variant Transillumination is a method that is useful to evaluate the association with hypertrophic muscular bands in the diaphragm. Using this technique, we determined that hypertrophic bands are associated with surface depressions in 67% of cases. Diaphragmatic muscular bands play a prominent role in the formation of surface depressions.



INTRODUCTION

Traditional descriptions of liver anatomy refer to a smooth, rounded, convex surface contacting the diaphragm, as demonstrated in Figure 1[1]. The presence of surface depressions is a recognized anatomic variant[2-4].

Figure 1
Figure 1 Anatomic specimen of a human liver with conventional surface anatomy. Both right (R) and left (L) hemi-livers have a smooth, convex surface in contact with the diaphragm.

While the cause for these surface depressions has not been definitively elucidated, several theories have been put forward, including: compression by ribs[5,6], pulmonary emphysema[7], congenital parenchymal weakness zones[8-10], hepatic trauma[11], tumour necrosis leading to desmoplasia and subsequent capsular retraction[10,11,12], regression of liver metastases after chemotherapy[11,13], adjacent inflammatory foci (gallbladder empyema, liver abscesses or cirrhosis) leading to parenchymal scarring and capsular retraction[14], localized iatrogenic injury after trans-arterial chemo-embolization (TACE)[15], fibrous bands and diaphragmatic scars[16]. Although none have been definitively proven as the cause for surface depressions, diaphragmatic muscular bands have gained little attention as an aetiologic factor. These are well-defined fascicles that connect the central diaphragmatic tendon to the rib cage. We discuss our observations during cadaveric dissections regarding the association of diaphragmatic muscular bands and surface depressions on the liver.

WHAT IS THE PREVALENCE OF SURFACE DEPRESSIONS?

The prevalence of surface depressions is difficult to discern, because there is no standardized nomenclature for this variant. A review of the literature revealed that many names have been ascribed to this variant, such as: hepatic surface grooves[5,7,11,16], diaphragmatic grooves[3], accessory sulci[6,8,16], hepatic fissures[3,8], portal fissures[8], accessory fissures[4], and capsular retraction[10,12]. Although there is heterogeneity in nomenclature, a detailed review of the descriptions appearing in the anatomic literature suggest that surface depressions are encountered in 5%[17] to 51%[18] of unselected persons across the globe.

WHAT IS THE RATIONALE FOR TRANSILLUMINATION?

In a prior publication on cadavers with liver surface depressions, we reported that the diaphragm appeared normal in all cases, without evidence of scars, fibrotic slips, ligamentous thickening or thickened muscular bands[16]. In fact, we wrote in our conclusion that our findings “did not support diaphragmatic pathology as a plausible explanation” for surface depressions[16]. Subsequently, however, we had the opportunity to inspect the diaphragm in living persons undergoing surgery, and observed thickened muscular bands in vivo while performing open surgery[19] as well as laparoscopic operations[20]. These observations directly challenged our prior statements and we were forced to re-visit this issue.

We postulated that the reason we had not observed diaphragmatic muscular bands in cadaveric studies was because they were not ligamentous thickening, scars or fibrotic slips. Instead, these areas appeared to be composed of hypertrophic muscular bands. Therefore, when muscle tone was absent at the post-mortem examinations, these bands would not be easily visible. However, if the bands were hypertrophic muscle, they should still be discernable by transillumination (Figure 2).

Figure 2
Figure 2 Anatomic specimen of a human liver with variant surface anatomy. Multiple surface depressions (arrows) are demonstrated on the diaphragmatic surface of liver.

After approval was granted from the local institutional review board (CREC_SA.1034/06/2021), we observed cadaveric dissections for academic medical curricula at two university campuses in the Caribbean. From a total of 120 cadaveric dissections observed, 18 (15%) cadavers had surface depressions on the liver. During academic teachings, the liver and diaphragm were excised en-bloc and studied on the dissecting bench. We took this opportunity to apply a light source against the thoracic surface of the diaphragm and observations were made from the abdominal side (Figure 3). The presence of hypertrophic muscular bands, when present, and their correlation with surface depressions were recorded.

Figure 3
Figure 3 Our technique for observation by trans-illumination. A light source is applied to the thoracic surface of the diaphragm, allowing hypertrophic muscular bands to be identified (arrow).
WHAT IS THE RELATIONSHIP OF MUSCULAR BANDS AND SURFACE DEPRESSIONS?

There were hypertrophic muscular bands visible on trans-illumination in 12 (67%) of the cadavers with surface depressions (Figure 4). Apart from hypertrophic muscular bands, there were no other causes of compression in these 12 cases.

Figure 4
Figure 4 The trans-illumination technique allows hypertrophic muscular bands to be demonstrated (white arrows) in the diaphragm corresponding to surface depressions on the liver (yellow arrows).

These bands were not readily visible upon gross inspection. Admittedly, we did not appreciate differences in the diaphragm in our previous publications[16]. Upon close inspection after transillumination, however, we noted that the diaphragmatic thickness was greater adjacent to surface depressions (Figure 5).

Figure 5
Figure 5 The thickness of the diaphragm is greater (white arrow) adjacent to the surface grooves (yellow arrow), and becomes thin at the smooth liver surface (red arrow).

In addition, we noticed the presence of muscular bands occurring adjacent to surface depressions in all of seven living patients undergoing abdominal imaging for varied indications (Figure 6). These observations support our theory that hypertrophic muscular bands are intimately related to the corresponding surface depressions.

Figure 6
Figure 6 Magnetic resonance imaging of a patient’s abdomen. There is a deep surface depression in the right hemi-liver (white arrow) and thickened diaphragmatic band (red arrow) can be seen intimately related to the depression.
IS THERE A MOLECULAR BASIS OF SURFACE DEPRESSIONS?

At the turn of the century, animal studies demonstrated that beta-catenin was an important factor responsible for stimulating hepatocyte growth, and its regulation had the potential to alter the size and shape of the liver[21,22]. Suksaweang et al[22] also theorized that there were specific areas in the liver, known as growth zones, that are susceptible to changes in beta-catenin activity.

Beta-catenin has since been shown to be up-regulated in humans with venous congestion secondary to cardiac failure[23]. It is also well known that there are areas between the inter-segmental and inter-sectional planes of the liver where the parenchyma is relatively less-well vascularized[11,24]. These “watershed areas” would be less responsive to the effect of beta-catenin up-regulation, and hence not proliferate as readily as surrounding parenchyma[11]. We suggest that hypertrophic muscular bands in proximity to these “watershed areas” could be responsible for the surface depressions. This could also explain the frequent location of surface depressions closely related to the inter-sectional planes[8,25].

DOES THIS HAVE CLINICAL SIGNIFICANCE?

The presence of surface depressions does have clinical significance, especially in light of the popularity of medical imaging in modern medicine. As more patients are subjected to medical imaging and these variants will be detected increasingly. When detected, these variants can be misinterpreted for metastatic liver secondaries in patients with known malignancies[1,2,4]. In those who have sustained blunt abdominal trauma, the depressions can be mistaken for liver lacerations[2,16]. There are also prior reports of these variants being mistaken for Chilaiditi’s syndrome on imaging[13]. In all of these cases, mis-interpretations can negatively affect clinical care decisions[16].

On the other hand, we have found that surface depressions can sometimes be advantageous. For example, in patients who require liver resections, we have modified our practice to routinely attempt to transect the parenchyma where surface depressions are present. This significantly reduces the thickness of the parenchymal transection line, reduces bleeding and so has the potential to improve patient outcomes[16].

CONCLUSION

Surface depressions of the liver are a recognized anatomic variant, with clinical implications when present. We suggest that it is time to adopt standardized nomenclature. We also theorize that diaphragmatic muscular bands play a prominent role in the formation of surface depressions.

Footnotes

Provenance and peer review: Invited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Anatomy and morphology

Country/Territory of origin: Trinidad and Tobago

Peer-review report’s scientific quality classification

Grade A (Excellent): 0

Grade B (Very good): B

Grade C (Good): 0

Grade D (Fair): 0

Grade E (Poor): 0

P-Reviewer: Gragnaniello V, Italy S-Editor: Zhang H L-Editor: A P-Editor: Yuan YY

References
1.  Srimani P, Saha A. Liver morphology: anatomical study about the outer aspects. Surg Radiol Anat. 2020;42:1425-1434.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 5]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
2.  Ragavan S, Muraleedharan A, Bage NN, Devi R. A comprehensive study and extensive review of morphological variations of liver with new insights. Surg Radiol Anat. 2022;44:455-466.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
3.  Chaudhari HJ, Ravat MK, Vaniya VH, Bhedi AN. Morphological Study of Human Liver and Its Surgical Importance. J Clin Diagn Res. 2017;11:AC09-AC12.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 8]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
4.  Sambhav K, Krishna H, Dixit SG, Ghatak S. Morphological Study of Variations of the Human Cadaveric Liver and Its Clinical Implications. Cureus. 2023;15:e35507.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
5.  Newell RLM, Morgan-Jones R. Grooves in the superior surface of the liver. Clin Anat. 1993;6:333-336.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 7]  [Article Influence: 0.2]  [Reference Citation Analysis (0)]
6.  Muktyaz H, Nema U, Suniti MR, Mahboobul H. Anatomical study of Accessory Sulci of Liver and its Clinical Significance in North Indian Population. Int J Med Health Sci. 2013;2:222-229.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Schumacher U. Groovy livers. Clin Anat. 1997;10:144-145.  [PubMed]  [DOI]  [Cited in This Article: ]
8.  Macchi V, Feltrin G, Parenti A, De Caro R. Diaphragmatic sulci and portal fissures. J Anat. 2003;202:303-308.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 31]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
9.  Joshi SD, Joshi SS, Athavale SA. Some interesting observations on the surface features of the liver and their clinical implications. Singapore Med J. 2009;50:715-719.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  Yang DM, Kim HS, Cho SW, Kim HS. Pictorial review: various causes of hepatic capsular retraction: CT and MR findings. Br J Radiol. 2002;75:994-1002.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 25]  [Cited by in F6Publishing: 25]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
11.  Cawich SO, Ali RRA, Gardner MT, Charles J, Sandy S, Pearce NW, Naraynsingh V. Hepatic surface grooves in Trinidad and Tobago. Surg Radiol Anat. 2020;42:1435-1440.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 1]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
12.  Sans N, Fajadet P, Galy-Fourcade D, Trocart J, Jarlaud T, Chiavassa H, Giron J, Railhac JJ. Is capsular retraction a specific CT sign of malignant liver tumor? Eur Radiol. 1999;9:1543-1545.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 22]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
13.  Young ST, Paulson EK, Washington K, Gulliver DJ, Vredenburgh JJ, Baker ME. CT of the liver in patients with metastatic breast carcinoma treated by chemotherapy: findings simulating cirrhosis. AJR Am J Roentgenol. 1994;163:1385-1388.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 89]  [Cited by in F6Publishing: 79]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
14.  Ohtomo K, Baron RL, Dodd GD 3rd, Federle MP, Ohtomo Y, Confer SR. Confluent hepatic fibrosis in advanced cirrhosis: evaluation with MR imaging. Radiology. 1993;189:871-874.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 89]  [Cited by in F6Publishing: 73]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]
15.  Kostov S, Selçuk I, Watrowski R, Dineva S, Kornovski Y, Slavchev S, Ivanova Y, Dzhenkov D, Yordanov A. Surgical Anatomy of the Liver-Significance in Ovarian Cancer Surgery. Diagnostics (Basel). 2023;13.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
16.  Gardner MT, Cawich SO, Shetty R, Pearce NW, Naraynsingh V. Hepatic surface grooves in an Afro-Caribbean population: a cadaver study. Ital J Anat Embryol. 2015;120:117-126.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Othman FB, Latiff AA, Suhaimi FH, Das S. Accessory sulci of the liver. An anatomical study with clinical implications. Saudi Med J. 2008;29:1247-1249.  [PubMed]  [DOI]  [Cited in This Article: ]
18.  Singh HR, Rabi S. Study of Morphoogical Variations of Liver in Humans. Transl Res Anat. 2019;14:1-5.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 1]  [Article Influence: 0.2]  [Reference Citation Analysis (0)]
19.  Cawich SO, Gardner MT, Pearce NW, Shetty R. Narayansingh V. Association between hepatic surface grooves and diaphragmatic slips. Italian J Anat Embryol. 2017;122:64-66.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Cawich SO, Spence R, Mohammed F, Gardner MT, Sinanan A, Naraynsingh V. The liver and Chilaiditi's syndrome: Significance of hepatic surface grooves. SAGE Open Med Case Rep. 2017;5:2050313X17744979.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 3]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
21.  Monga SP, Pediaditakis P, Mule K, Stolz DB, Michalopoulos GK. Changes in WNT/beta-catenin pathway during regulated growth in rat liver regeneration. Hepatology. 2001;33:1098-1109.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 205]  [Cited by in F6Publishing: 209]  [Article Influence: 9.1]  [Reference Citation Analysis (0)]
22.  Suksaweang S, Lin CM, Jiang TX, Hughes MW, Widelitz RB, Chuong CM. Morphogenesis of chicken liver: identification of localized growth zones and the role of beta-catenin/Wnt in size regulation. Dev Biol. 2004;266:109-122.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 83]  [Cited by in F6Publishing: 87]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
23.  Mahmoodzadeh S, Eder S, Nordmeyer J, Ehler E, Huber O, Martus P, Weiske J, Pregla R, Hetzer R, Regitz-Zagrosek V. Estrogen receptor alpha up-regulation and redistribution in human heart failure. FASEB J. 2006;20:926-934.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 104]  [Cited by in F6Publishing: 105]  [Article Influence: 5.8]  [Reference Citation Analysis (0)]
24.  Sureka B, Sharma N, Khera PS, Garg PK, Yadav T. Hepatic vein variations in 500 patients: surgical and radiological significance. Br J Radiol. 2019;92:20190487.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 14]  [Article Influence: 2.8]  [Reference Citation Analysis (0)]
25.  Ono ML, Murakami G, Sato TJ, Sawada K. Hepatic grooves and portal segmentation. Kaibogaku Zasshi. 2000;75:517-523.  [PubMed]  [DOI]  [Cited in This Article: ]