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ORIGINAL ARTICLE

Anatomical appraisal of safe cholecystectomy: a prospective study

Mohammad Ibrarullah ,* Laxminarayan Mohanty,* Abhishek Mishra,* Ashirbad Panda* and


Sadiq S. Sikora †
*Department of Surgical Gastroenterology, Apollo Hospitals, Bhubaneswar, Odisha, 751005, India and
†Institute of Digestive & HPB Sciences, Sakra World Hospital, Bangalore, India

Key words Abstract


biliovascular anatomy, cystic artery, cystic duct,
laparoscopic cholecystectomy, Rouviere’s sulcus, Background: Principles of safe cholecystectomy include dissection of the hepatocystic
safe cholecystectomy. triangle and identification of the bilio-vascular structures to achieve critical view of safety.
The aim of the present study was to document the variations in anatomical landmarks and
Correspondence bilio-vascular structures exposed during laparoscopic cholecystectomy.
Professor Mohammad Ibrarullah, Department of Methods: All consecutive patients who underwent laparoscopic cholecystectomy were
Surgical Gastroenterology, Apollo Hospitals,
included in the study. Recommended techniques of safe cholecystectomy were followed.
Bhubaneswar 751005, Odisha, India.
Rouviere’s sulcus was classified into four types. Cystic duct was assessed for its length and
Email: ibrarullahm60@gmail.com
diameter. A new classification was suggested for cystic artery.
M. Ibrarullah MS, MCh; L. Mohanty MS, DNB; Results: Five hundred patients were included in the study. Critical view of safety was
A. Mishra MS; A. Panda MS; S. S. Sikora MS, achieved in 463 (92.6%) patients. Type1 Rouviere’s sulcus was the most common variant
FRCS. found in 263 (52.6%). Normal cystic duct was present in 339 (67.8%). Wide cystic duct of
normal length was the most common variant found in 71 (14.2%). Single cystic artery
Accepted for publication 5 March 2023.
supero-medial to cystic duct (type1-s) was the most common variant found in
doi: 10.1111/ans.18387 384 (76.8%). Inferior cystic artery i.e. artery infero-lateral to cystic duct (type-2) was the
second most common variant, found in 40 (8%). Multiple cystic arteries in the
hepatocystic triangle were due either to early division of single cystic artery (type-1m) or
double cystic artery (type-3). Aberrant right hepatic artery giving off a small cystic artery
(type-4) was seen in 12 (2.4%).
Conclusion: Wide variation in the anatomical structures is noted when principles of safe
laparoscopic cholecystectomy is followed. Awareness is paramount to avoid bilio-vascular
injury during surgery.

important anatomical landmarks and a clear dissection of the criti-


Introduction
cal anatomy in relation to GB. Though there is no dearth of publi-
Cholecystectomy is the commonest abdominal surgery performed shed literature on anatomy related to cholecystectomy, most of
across the world. With the emergence of laparoscopic cholecystec- these are cadaveric studies that provide an elaborate description of
tomy (LC) as the gold standard, a major concern has been the the structures and their variability.5–8 On the contrary, there are
occurrence of bilio-vascular injury associated with the procedure. only a few studies that focussed on identification of the variability
Critical view of safety (CVS), conceptualized in 1995, has emerged of the biliovascular structures dissected during LC.9,10 Knowledge
as the most reproducible and reliable step in performing a safe cho- and awareness of the operative rather than the cadaveric anatomy,
lecystectomy.1 Demonstration of CVS entails three components— is more important for performing safe cholecystectomy. For exam-
(i) clearance of all fibrofatty tissue in the hepatocystic triangle ple, in cholecystectomy, identifying the variability of CA in the
(HCT), (ii) dissection of the distal 1/3 of gallbladder (GB) from the HCT is more important than its origin whether from the right
cystic plate and (iii) identification of only two structures, that is, hepatic artery (RHA), common hepatic artery or otherwise. Simi-
cystic duct (CD) and cystic artery (CA) joining the GB. Several larly, CD, whether parallel or across the common bile duct (CBD),
international societies have since come out with guidelines endors- inserting into its medial or lateral aspect, are not so relevant since a
ing CVS as one of the important steps of safe cholecystectomy.2–4 safe dissection of the CD mandates delineation of its junction with
The major emphasis in these guidelines is identification of GB rather than the CBD.

© 2023 Royal Australasian College of Surgeons. ANZ J Surg (2023)


2 Ibrarullah et al.

Aims and objectives <2 cm as short and >4 cm as long CD. The CD that required large
(L) size Hemolok (Weck, nonabsorbable polymer ligating clip), LT
In a prospective study we have attempted to identify the anatomical
400 ligaclip (Ethicon Endosurgery ltd) or suture ligation, was con-
landmarks and the bilio-vascular anatomy (BVA) that presents
sidered wide. The CA was isolated close to the cystic LN. Its
when the principles of safe cholecystectomy are followed and docu-
course and branching (when present) in the HCT were meticulously
ment the variation of the anatomy and classify it in the con-
dissected and noted. Based on the observed pattern, we have
text of LC.
suggested a classification of the CA. The GB was dissected off its
bed to complete the requirements of CVS. Presence of any addi-
tional biliary or vascular structure was noted. When conventional
Material and methods dissection appeared difficult, the CA was isolated, clipped close to
In a prospective study all consecutive patients who underwent LC GB surface or lateral to the cystic LN and divided. This (artery first
during March 2020–January 2023 were included. LC was per- technique) often facilitated dissection of the HCT to achieve CVS.
formed with strict attention to the principles of safe cholecystec- However, in case of severe inflammation, fibrosis, and obliteration
tomy.1 All surgeries were either performed or supervised by the of the HCT, a retrograde dissection (fundus first) was attempted
senior most surgeon in the team. The fundus of GB and Hartman’s that often ended in subtotal cholecystectomy. All stones were
pouch were grasped and appropriately retracted to identify the ana- retrieved from the remnant infundibulum which then was suture
tomical landmarks i.e. Rouviere’s sulcus (RS), the cystic lymph approximated or closed with endo-loop. The entire surgery was
node (LN) and the structures in the hepatoduodenal ligament. Dis- video recorded for review, analysis and confirmation of the opera-
section was started close to GB surface remaining strictly ventral to tive anatomy when required.
the RS. The HCT was approached from both anterior as well as
posterior aspect to clear all the fibrofatty tissue, leaving behind the
Results
CD and CA. The CD was dissected from infundibulum downwards
as far safely as possible with no attempt to define its junction with A total of 500 patients (male 180, female 320, mean age 48 years,
CBD. The dissected length of 2–4 cm was considered normal, and range 18–82 year) were included in the study.

Fig. 1. Types of Rouviere’s sulcus (RS): (a) Absent or rudimentary sulcus. (b) Medial end of the sulcus open, (c) Medial end fused. (d) Sulcus fused in the
middle. (e) Slit—small and shallow (<1 cm) sulcus away from the hepatic hilum. (f) Scar-completely fused sulcus, appearing as a white linear scar.
(g) Double sulcus. (h) Sulcus not identifiable

© 2023 Royal Australasian College of Surgeons.


Anatomy of safe cholecystectomy 3

Table 1 Rouviere’s sulcus (n = 500): Various types as per Ibrarullah & was absent in 117 (23.4%) patients and could not be delineated in
Sikora’s classification11 and the respective incidences 77 (15.4%) due to subhepatic adhesions. When visible, a well-
Type Description n % formed sulcus—Type 1 was the most common variant. Double sul-
cus (type-4) was noted in one patient only.
0 Absent or rudimentary sulcus (Fig. 1a) 117 23.4
1 Deep sulcus 263 52.6 Various patterns of the CD were observed and documented as in
a. Medial end of the sulcus is open (Fig. 1b) 198 39.6 Table 2. CD was considered normal in 339 (67.8%) patients and
b. Medial end of the sulcus is fused (Fig. 1c) 57 11.4 absent in one patient. Wide CD with normal length was the most
c. Sulcus is fused in the middle (Fig. 1d) 08 1.6
2 Slit—small and shallow (<1 cm) sulcus away 25 5 common variant (14.2%). Wide CD was a result of calculi in 9 and
from the hepatic hilum (Fig. 1e) choledocholithiasis in 16 patients. It was not safe to dissect due to
3 Scar—completely fused sulcus, appearing as 17 3.4 inflammation and/or fibrosis in 29 (5.8%) patients
a white linear scar (Fig. 1f)
4 Double sulcus (Fig. 1g) 01 0.2 The CA was identified close to the cystic LN. Small branches
NI Sulcus is not identifiable because of 77 15.4 supplying the CD were noted before the artery divided close to the
subhepatic adhesions (Fig. 1h) GB surface into superficial and deep branches (Fig. 2a). The super-
ficial branch supplied the GB neck and infundibular region. The
deep branches running between GB and liver bed ended in GB wall
or mesentery or into the liver bed. Depending on its number and
Eighty-one patients were operated for acute cholecystitis. At sur- course in the HCT, the CA was classified into four types. The clas-
gery, four patients were identified to have cirrhosis of liver. Extra- sification and the respective incidences have been presented in
hepatic portal vein thrombosis and left sided GB was detected in Table 3. Type 1s was the most common variant found in
one patient each. 384 (76.8%) patients. Multiple arteries in HCT due to early division
Rouviere’s sulcus was the first anatomical landmark that was (type 1 m) or double CA (type 3) was seen in 24 (4.8%) and
looked for at the start of dissection. Depending on the appearance, 10 (2%) of patients respectively. Aberrant RHA in HCT (type 4)
the RS was classified into four types.11 The incidence and various was noted in 12 (2.4%) patients.
types of the sulcus in our study has been presented in Table 1. RS CVS was achieved in 463 patients (92.6%). It was complete in
407 patients (81.4%) in whom both CA and CD were displayed.
In five patients (1%) it was considered incomplete where the distal
Table 2 Cystic duct (CD) anatomy and variations (n = 500)
1/3 of the GB could not be completely lifted from the cystic plate.
In 51 (10.2%) patients the CA was divided first (artery first tech-
Type Description n % nique) to facilitate dissection of the HCT and identify the cystic
Normal Dissected length of the CD is 339 67.8 duct. Infundibular technique, though considered unsafe, had to be
2 cm-4 cm performed in one patient only in view of gross bowel distention
Wide CD requiring large (L) size Hemolok 71 14.2
making exposure of the HCT almost impossible. Fundus first
(Weck, nonabsorbable polymer
ligating clip), LT 400 ligaclip and/or subtotal cholecystectomy was performed in the remaining
(Ethicon endosurgery ltd) or suture 28 (5.6%) where CVS could not be achieved. Eight patients
ligation
(1.6%) were converted to open cholecystectomy due to difficult
Long Dissected length of the CD is >2 cm 30 6
Short Dissected length of the CD is <2 cm 07 1.4 anatomy. Additional findings noted in the GB bed (cystic plate)
Short & wide As above 22 4.4 were, dilated veins in six and cholecystohepatic duct in one
Long & wide As above 01 0.2
patient.
Sessile CD length not definable 01 0.2
NI CD not identifiable due to 29 5.8 There was no perioperative mortality. Two patients with subtotal
inflammation and/or fibrosis cholecystectomy had minor bile leak in the postoperative period
that subsided in the second week with conservative management.

Fig. 2. (a) Single cystic artery (CA) superomedial


to cystic duct in the hepatocystic triangle dividing
into superficial (SCA) and deep (DCA) branches
close to the gallbladder surface. (b) Early division
of the cystic artery giving rise to superficial (SCA)
and deep (DCA) branches that requires individual
control.

© 2023 Royal Australasian College of Surgeons.


4 Ibrarullah et al.

Fig. 3. Inferior cystic artery, that is, cystic artery


(CA) arising infero lateral to the cystic duct
(CD) (a) anterior view, as it crosses the CD ante-
riorly to enter the hepatocystic triangle to supply
the gallbladder. (b) posterior view of the same.
(c) inferior cystic artery inserting posteriorly in
the gallbladder. (d) Inferior cystic artery dividing
into superficial (SCA) and deep branches (DCA)

Discussion dissection of GB should remain ventral to the plane joining the


sulcus and the base of segment 4.12,13 In a reported meta-analysis,
During laparoscopic cholecystectomy, RS is the first anatomical
the sulcus is present in 83%, with no difference in incidence
landmark to be identified. The sulcus lies below GB fossa, can be
between LC and cadaveric study. The sulcus is absent in
seen after lifting the Hartman’s pouch upwards and medially. The
10%–30% of patients.14 In our experience RS was demonstrable
sulcus represents the plane of the extrahepatic portal pedicle. It is
in 61%, absent in 23.4% and not visible in 15.4% due to sub-
recommended that in order to avoid injury to CBD, the
hepatic adhesions. We have not made any additional effort to
expose when it is obscured by dense inflammatory adhesions. The
incidence in our series is comparable with the published reports if
the non-visualized cases are excluded. However, non-visualization
of RS due to subhepatic inflammatory adhesions is a reality which
has not been addressed in the literature. It is our practice to follow
other safety guidelines for dissection if RS is either absent or not
visible. The RS has been broadly classified into open and closed
types when the medial end of the sulcus is either continuous with
the hepatic hilum or fused.13 Two more variants, that is, slit and
scar, have been identified in subsequent publications.10,15 We have
classified RS into four types.11 The variants type 1-c and type
4 were reported by us for the first time and incorporated in the pre-
sent series. Open type is the common variant accounting for 66%
of all cases.14 This contrasts with 41.2% (types 1a and 1c) in our
series. This discrepancy can be due to geographical variations,
inclusion of non-visualized cases and a more detailed subclassifi-
cation of the sulcus in our series. In 70% of patients, the RS con-
tains the right portal pedicle. Additionally, it may contain the vein
Fig. 4. Type 3: Double cystic artery (CA1 and CA2). One of the arteries to segment VI, anterior sectoral pedicle, or the cystic vein in 25%,
(CA1) appears to be an inferior cystic artery 5%, and 18%, respectively.16 Intraoperatively, however, it is

© 2023 Royal Australasian College of Surgeons.


Anatomy of safe cholecystectomy 5

Table 3 Classification of the cystic artery and incidences of various types, of stone/s in either CD or CBD. Long cystic duct was noted in 6%
based on their appearance during laparoscopic cholecystec- of our patients compared to 7%–12% in other reports.10,18 This dis-
tomy (n = 500)
crepancy can be due to the variation in the extent of CD dissected
Type Description n % during surgery. Short CD and sessile GB were found in 1.4%,
1 s—single CA superomedial to CD in the HCT 384 76.8 0.2% of patients respectively. Despite the low incidence, such cases
(Fig. 2a) pose real technical challenges during LC. We did not observe any
m—multiple arterial branches in the HCT due 24 4.8 case of CD joining right hepatic duct or sectoral ducts as has been
to early division of the CA (Fig. 2b)
2 Inferior CA, that is, artery arising infero lateral 40 8 reported in a series.10 We attribute this to our policy of conservative
that may run behind or cross the CD to yet adequate dissection of CD where the display of its insertion into
enter the HCT to supply the GB. (Fig. 3a–d) the CBD is not persisted with.
3 Double CA—Both the arteries appear to arise 10 02
at different planes and, unlike early division The cystic artery is considered the most variable structure in the
of CA, do not appear to converge on a hepatocystic triangle.7,9 Failure to identify the variations, with
single artery in the HCT. (Fig. 4) respect to its number and position, may result in inadvertent injury
4 Small CA arising from aberrant right hepatic 12 2.4
artery in the HCT. (Fig. 5) to the artery and bleeding. Attempt to control the bleeding may lead
NI CA not identifiable due to inflammation/ 30 06 to further injury to adjacent structures. An over-simplified classifi-
fibrosis/ multiple small branches cation was proposed that classified CA into three types – CA inside
Abbreviations: CA, cystic artery; CD, cystic duct; HCT, hepatocystic trian- or outside the Calot’s triangle or both.19 The classification
gle; GB, gallbladder. suggested by us is based on real-time dissection in a large number
of patients. Type 1, that is, single CA superomedial to the CD in
the HCT, was the commonest variant. Our observation in this
neither possible nor important to know the exact contents of the regard (76.8%) is similar to what has been reported in literature
sulcus though portal pedicle at times can be clearly identified in it. (72%–80%).7–9,20 The CA divides close to the GB surface into
The process of achieving CVS requires clear delineation of two superficial and deep branches that can be demonstrated with careful
structures namely CD and CA. Normal CD is around 2–4 cm long dissection though application of clips on the main trunk suffices for
and 2–3 mm in diameter. It can have variable course and insertion both. On the contrary, early division of the CA resulting in more
into the CBD.6,9 Dissection of CVS during LC requires isolation of than one arterial trunk (Type 1 m), found in 4.8% in the present
CD in the HCT and its junction with the GB infundibulum. It is not study, behaves like double CA that requires individual control.
important to trace the entire course of CD distally till it joins the Type 2 variant, 8% in our experience, known as inferior CA is seen
CBD. Such an attempt may even be hazardous.17 However, it is our in approximately 6%–10% of cases.8,10,19,20 This artery usually
practice to carefully dissect the CD distally as far as possible so that arises from gastroduodenal artery or common hepatic artery, runs
we do not leave behind a long stump with/without an unsuspected inferolateral to the CD to supply the GB.8 Though the artery in
stone inadvertently. Normal CD was clearly defined in 67.8% of most of its course lies outside the HCT, it may cross the CD anteri-
our patients which is comparable to 62.5%–87.8%.10,18 reported by orly or posteriorly to be identified in the HCT close to GB. Because
other authors. Wide cystic duct was the commonest abnormality of its position the artery can often be mistaken as CD till CVS is
found in our patients (normal length 14.2%, short 4.4%, and long completely established. Type-3, double CA was noted in 2% of our
0.2%). In nearly one fourth of patients this was due to the presence patients. The reported incidence of this variant in LC as well as
cadaveric studies ranges from 3% to 25%.5,7–9,19,20 Such wide vari-
ation in the incidence of double/multiple CA may be because of
cadaveric dissection, and/or mistakenly including deep and superfi-
cial branches from an early division of CA as double CA. In case
of double CA, the artery arising from RHA usually runs as deep
CA whereas the superficial branch can arise from any of the major
arteries in that region.21 Type-4, the short CA arising from RHA in
the HCT can be considered an anatomical trap. We found this vari-
ant in 2.4% in contrast to 3%–9.5% reported in literature.8,9,19 Pres-
ence of these CA variants re-emphasizes the need for careful
dissection of HCT to define its course. Alternatively, when a clear
dissection is not possible due to inflammation and/or fibrosis, a
safer alternative is to secure the CA lateral to the cystic LN on the
GB surface (artery first technique), thereby avoiding potential
injury to aberrant RHA. In the present series the CA was not identi-
fiable in 6%. This can be attributed to obscure anatomy, proper CA
replaced with multiple smaller branches or its absence.
The single most important step of a safe cholecystectomy
Fig. 5. Type 4: Small cystic artery (CA) arising from aberrant right hepatic entails achieving CVS after due dissection of HCT preceding
artery (RHA) which is the dominant artery in the hepatocystic triangle division of CA and CD.22 During this phase, it is important to be

© 2023 Royal Australasian College of Surgeons.


6 Ibrarullah et al.

aware of the aberrant anatomy so as to avoid any intraoperative 4. Bansal VK, Misra M, Agarwal AK et al. SELSI consensus statement
complication due to inadvertent injury to RHA or CBD.7,9 Simi- for safe cholecystectomy—prevention and management of bile duct
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Atlas. New York: CRC Press, Taylor & Francis, USA, 2022; 9–24.
Mohammad Ibrarullah: Conceptualization; data curation; 12. Gupta V, Jain G. The R4U planes for the zonal demarcation for safe
formal analysis; methodology; writing – review and editing. laparoscopic cholecystectomy. World J. Surg. 2021; 45: 1096–101.
Laxminarayan Mohanty: Conceptualization; data curation; formal 13. Hugh TB, Kelly MD, Mekisic A. Rouviere’s sulcus: a useful landmark
analysis; supervision; writing – original draft. Abhishek Mishra: in laparoscopic cholecystectomy. Br. J. Surg. 1997; 84: 1253–4.
Data curation; formal analysis; methodology; validation; writing – 14. Cheruiyot I, Nyaanga F, Kipkorir V et al. The prevalence of the
original draft. Ashirbad Panda: Data curation; formal analysis; Rouviere’s sulcus: a meta-analysis with implications for laparoscopic cho-
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Conflict of interest statement Rouviere’s sulcus. Scientific World Journal 2013; 2013: 1–4. https://
None declared. doi.org/10.1155/2013/254287.
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