Laparoscopic cholecystectomy (LC) is an advanced and commonly performed minimally invasive surgery; however, its safety has been questioned because of the increasing incidence of injury to the hepatobiliary structures [1]. Therefore, the incidence and complications associated with LC should neither be overestimated nor underestimated. There are several common causes of hepatobiliary injuries, including a shrunken and fibrotic gallbladder (GB) as well as unawareness and misidentification of various anatomical variations of the right hepatic artery (RHA) and biliary system during surgery [2,3].

Anatomic variants are seen in 18% to 39% of cholecystostomies, and 3% to 6% lead to an increased risk of biliary tract injuries [3]. The fundamental step in LC is the thorough evaluation of Calot’s triangle and its associated variations in the biliary tracts and blood vessels [4]. Since anatomical variations can extend beyond this narrow triangle, Calot’s triangle assessment alone is not sufficient to perform a safe LC. It is important to have a good understanding of the hepatocystic triangle and different anatomical anomalies to avoid iatrogenic injuries.

This study aimed to assess the incidence of anatomical variations discovered during LC at and beyond the hepatocystic triangle under limited-resource conditions. This study is the first of its kind from our region (Aden, Yemen), and it emphasizes the importance of understanding the safe zone of dissection in LC.

We believe that the exceptional, interesting cases and promising outcomes of this study will prove advantageous to young surgeons operating in challenging circumstances, thereby fostering their willingness to perform appropriate LC.

This is a single-center, descriptive, prospective assessment of all patients with symptomatic GBs and acute and chronic calcular and acalculous cholecystitis between June 2012 and June 2019. The study included 375 patients (female, 355 and male, 20).

All patients underwent abdominal ultrasonography before surgery as it is mostly available, not coasting, and effective for the diagnosis of GB diseases. Abdominal computed tomography scans and magnetic resonance imaging are reserved to rule out serious conditions in suspicious cases. No other special tests were performed to study the biliary tree before surgery. A liver function test is strictly recommended as a preoperative measure to rule out biliary diseases or obstructions. The study excluded patients with obstruction of the biliary tract, irrespective of their underlying pathology. Before surgery, all patients had medical fitness and were carefully assessed by the anesthetist.

All surgeries in this study were performed by the same surgical team led by the corresponding author at the same center using a standard four-port LC (as we are familiar with this technique, and single-port instruments are not yet available in our center). During the surgery, we used to peel off a wide area and start the dissection far from the Calot’s triangle beginning at the lower third of the GB bed, via the hepatocystic triangle, and down to the Calot’s triangle and around. The important anatomical landmarks in the extrahepatic region were visualized during the procedure. Particular emphasis was placed on identifying and documenting any laparoscopic anatomical variations of the cystic artery (CA), cystic duct (CD), and RHA in the pericystic region, comprising the hepatocystic triangle, cystic bed, and the area behind the CD and GB.

The intraoperative evaluation of the extrabiliary tree using indocyanine green, cholangiography, or intraoperative laparoscopic ultrasound was not utilized in challenging cases as it was beyond our capabilities. Rouvière’s anomaly was not documented in this study; however, it is regarded as a common anatomical feature that should be avoided to prevent iatrogenicity during dissection [5].

Most patients were discharged from the hospital in good condition on the postoperative day 2 or 3. Women with tense and frozen hepatocystic triangles who had partial LC were excluded from the study. In complex cases, the subhepatic intraoperative tube drain was preserved and removed after 24 hours when the postoperative abdominal ultrasound and serum liver function tests showed normal results.

Data were collected based on intraoperative findings and postoperative records. The IBM SPSS for Windows, version 22.0 (IBM Corp.) was used to analyze the data. The background characteristics of the study population and variables related to practice scope were described using simple descriptive statistics (means ± standard deviations and frequencies with percentages).

During the study period, 375 patients were admitted to our surgical unit and underwent LC. The study included 20 male (5.3%) and 355 female patients (94.7%). The ratio of female to male was 18 to 1. The mean age of the study population was 45 ± 12.2 years, and the majority of them belonged to the age group of 18 to 60 years, with a percentage of 93.3% (Table 1).

Table 1 . Distribution of the study population according to age group and sex.

Variable	Data
No. of patients	375
Sex, female:male	355:20
Age (yr)	45 ± 12.2
6–17	6 (1.6)
Female	4
Male	2
18–60	350 (93.3)
Female	336
Male	14
61–80	19 (5.1)
Female	15
Male	4

Values are presented as number only, number (%), or mean ± standard deviation..

The high female ratio in this study could be coincidental. However, other factors may have contributed to this increase such as our center not being a referral center and some charities covering surgery costs for females more than males; therefore, we haven’t a large number of male patients. In addition, most people in our traditions do not consume alcohol and have a low-fat diet due to financial issues.

Only 26 patients (6.9%) presented with laparoscopic anatomical variations. The incidence of laparoscopic vascular variations was 73.1%, higher than that of biliary-related variations. The most common abnormalities were a double CA (DCA) with separate origins (26.9%) followed by Moynihan’s hump (23.1%). Next, thin and long CDs and DCAs of a single origin were observed (15.4%). Considering that most of the patients who underwent surgery were female, most anomalies were detected among female patients (n = 21, 80.8%) compared to male patients (Table 2).

Table 2 . Distribution of the study population according to detected anomalies and distribution of anomalies according to the patients’ sex.

Variation type	Total variation	Female	Male	Percentage of total patients (n = 375)
No. of patients	26 (100)	21 (80.8)	5 (19.2)	6.9
Vascular variation	19 (73.1)	16 (61.5)	3 (11.5)	5.1
Double CA with the separate origin	7 (26.9)	7 (26.9)	0 (0)	1.9
Moynihan’s hump	6 (23.1)	5 (19.2)	1 (3.8)	1.6
Early division of CAa)	4 (15.4)	3 (11.5)	1 (3.8)	1.1
CA hooking the CD	2 (7.7)	1 (3.8)	1 (3.8)	0.5
Biliary variations	7 (26.9)	5 (19.2)	2 (7.7)	1.9
Long thin CD	4 (15.4)	2 (7.7)	2 (7.7)	1.1
Subvesical duct	3 (11.5)	3 (11.5)	0 (0)	0.8

Values are presented as number (%) or percentage only..

CA, cystic artery; CD, cystic duct..

^a)Double CA with single origin..

During surgery, the most gross GB findings were chronic and complicated cholecystitis. This could be attributed to improper primary health care, and our patients not seeking medical attention unless in an advanced stage of the disease (Table 3).

Table 3 . The frequency of the gross laparoscopic gallbladder pathology found during laparoscopic cholecystectomy.

Variable	Total	Female	Male
No. of patients	375 (100)	355	20
Pathology
Cholelithiasis	81 (21.6)	81	0
Acute cholecystitis	47 (12.5)	43	4
Chronic cholecystitis	134 (35.7)	125	9
Empyema	36 (9.6)	32	4
Mucocele	50 (13.3)	49	1
Acalculous cholecystitis	27 (7.2)	25	2

Values are presented as number (%) or number only..

Conversion to open cholecystectomy occurred in two patients (0.5%) due to severe adhesion to rule out a possible intraoperative biliary ductal injury. One female underwent late laparotomy after 48 hours because of intraabdominal bile collection due to iatrogenic injury to the missed subvesical duct (SVD). Furthermore, one patient experienced continuous bile leakage of 150 mL/day via the subhepatic drain, probably due to a poorly secured, wide, and short CD.

No significant main biliary ductal or vascular injuries were recorded during this study, and the patients showed good postoperative recovery. The accuracy rate was determined to be 98.9%, which was calculated by dividing the number of uncomplicated surgeries by the total number of surgeries and multiplying by 100.

Although LC has become the preferred method for the treatment of symptomatic cholelithiasis owing to its many advantages over standard open cholecystectomy, numerous studies have shown that LC is associated with a higher frequency of complications [2]. Laparoscopic iatrogenic injuries often occur because of extrabiliary vascular and ductal anatomical variations, severe adhesions, and malpractice.

Anatomical variations in and around the hepatobiliary triangle are frequent, accounting for 20% to 50% of patients [6,7]. In the present study, the overall incidence of anatomical variations was 26 (6.9%). This low rate can be attributed to the fact that this study was conducted laparoscopically on living patients, thus patients’ safety is the most important issue of concern regardless of the objectives of the research; we did not go further to explore the HD, common bile duct (CBD), and RHA regions to discover anomalies in these areas (as it can be easily performed on cadaveric subjects) to avoid any potential iatrogenic injuries to these important structures. In some cases, due to severe pathological conditions and frozen hepatocystic triangle and to avoid iatrogenicity and bleeding we kept dissection close to the GB body and didn’t make further exploration to detect anatomical anomalies, consequently, some anomalies were expected to be overlooked in some of these cases.

The CA is usually single and arises from the RHA when the latter crosses the common hepatic duct (CHD) posteriorly, and most commonly 81.5% traverses the hepatocystic triangle to supply the GB through its two branches—superficial and deep [8–10]. We found that 94% of patients had this common presentation.

The incidence of vascular variation in this study was 19 (73.1%), which was significantly higher than that of biliary variation. As described in numerous studies, the CA exhibits a higher degree of variation (25%–50%) based on its origin, position, and number than the biliary duct. Therefore, accurate knowledge of variations in the extrabiliary vasculature is crucial to avoid accidental bleeding and its fatal consequences in cholecystitis [11–15].

Early division of the CA after its origin in the RHA is an unusual laparoscopic variant. This variation was found in four patients, accounting for 15.4% of the total variations and 1.1% of the total study population.

In their cadaveric study, Sidana et al. [14] reported that the accessory CA may arise from one of its branches and that the CA often bifurcates close to its origin, giving rise to two vessels that approach the GB. Al-Sayigh [16] reported early division of the CA before reaching Calot’s triangle in two patients (4%) of nine patients (18%) with vascular laparoscopic variations in a 50-patient sample size. In this study, both variations were observed in the early CA divisions. In the first instance, the CA splits at the level of its origin in the RHA, resulting in a V-shaped DCA. In contrast, when the CA branches early, after leaving the RHA at the level of the hepatocystic triangle, before approaching the neck of the GB, it results in a Y-shaped CA (Fig. 1).

Figure 1. Early division of the cystic artery (CA). Double CAs (DCAs) in V shape (A) and Y shape (B). CD, cystic duct.

The caterpillar, also known as Moynihan’s hump, is an additional significant and common anatomical variant of the RHA. It is characterized by a tortuous RHA running proximal and/or parallel to the CD and predisposes the patient to a small and/or short CA. The prevalence of Moynihan’s hump ranges from 1.3% to 16% [6,10].

In this study, Moynihan’s hump was found in six patients at a rate of 1.6%, representing 23.1% of the total discovered anatomical variations. The RHA in Moynihan’s hump has different anatomic courses; it may exist as an anterior or posterior presentation to the CHD, with the posterior presentation being the most common anatomical variation, with a 60% incidence rate [7,17]. The present study revealed that the anterior course of RHA incidence was higher (66.7%) than the posterior course (33.3%) (Fig. 2).

Figure 2. Moynihan’s hump. (A) Anterior course of the right hepatic artery (RHA) and a very short cystic artery (CA). (B) Posterior course of the RHA after division of the CA and the cystic duct (CD). CHD, common hepatic duct.

In a case report on a female cadaver Kamath [16] discovered a DCA in Moynihan’s hump; one came from the RHA and the other from the superior pancreaticoduodenal artery outside the hepatobiliary triangle. In this study, we reported a case in which there was a DCA and both seemed to originate from the RHA in Moynihan’s hump within the hepatobiliary triangle (Fig. 3).

Figure 3. Double cystic artery (DCA) originating from the anterior coursed the right hepatic artery (RHA) in Moynihan’s hump. CD, cystic duct.

Moynihan’s hump can be a high-risk factor for vascular injury, being one of the most serious lesions described, despite its low frequency [6]. Although it is not clearly reported, CA avulsion due to fundus over traction and RHA injury or ligation is expected during LC of Moynihan’s hump. This can lead to severe bleeding, resulting in injury to critical regional structures and subsequent conversion.

The incidence of DCAs with a separate origin was higher than that of other biliary anatomical anomalies. Suzuki et al. [18] observed DCAs in laparoscopic materials in 11.1% of cases. Akay and Leblebici [12], in their retrospective study, reported that the average prevalence of DCAs discovered during LC was 3.05%; however, the prevalence of DCAs varies from 2% to 25% in general. Sarkar et al. [13] reported that the DCA 63.9% originated from the RHA. Kim and Yoon [19] detected a case of DCA originating in the RHA and a segment IV hepatic artery during LC in their case report.

Of the 375 patients in the present study, seven had DCAs of separated origin, representing a higher rate of 26.9% of the total laparoscopic variations discovered. Six patients were diagnosed with a DCA, which was obtained from the RHA. One patient appeared to have a DCA that emanated from the RHA and the segment IV hepatic artery (Fig. 4).

Figure 4. (A) Double cystic artery (DCA) separately originating from the right hepatic artery (RHA). (B) DCA separately originating from the RHA (1) and from liver segment IV (2). CD, cystic duct.

Another rare condition of the biliary vascular system is the CA syndrome. In 2000, Suzuki et al. [18] described this condition as one in which a single CA originates from the RHA but has a course that wraps across and hooks around the CD from behind, reappearing at the peritoneal surface near the neck of the GB. Zubair et al. [11] reported four cases of CA syndrome in 220 patients who underwent LC in 2002.

In the present study, only two young (28 and 31 years of age) patients had CA syndrome (0.5%). This accounted for 7.7% of the 26 variations and 10.5% of the total vascular variations (Fig. 5). Suzuki’s theory [18] states that obstructed biliary flow due to partial obstruction of the CD is the root cause of biliary dysfunction in CA syndrome anomalies [11]. This may explain why both of these patients in this study developed biliary cholelithiasis at younger ages.

Figure 5. Cystic artery (CA) syndrome. CA hooking the cystic duct (CD).

The CD usually lies next to the CA and its usual length is 2 to 4 cm. It may be congenitally absent, double (very rare), or very long (5 cm or more) and 1 to 5 mm wide, but it can dilate in the presence of stones. The CD joins the GB at the neck at an acute angle. Generally, the CD enters the CHD from the right lateral aspect [20–22].

Cystic duct variations have been described in the literature based on their length, course, and insertion site with the CHD. Sarawagi et al. [22] and Sangameswaran [23] discovered during his cadaveric studies that the CD length varied between 0.8 and 11.5 cm, with a mean average of 2.9 cm. Talpur et al. [24] reported that of 61 laparoscopically revealed CD anomalies, 4.33% of CD variations were in the form of a short CD (2.67%) or a long CD (1% with low insertion).

Short CDs, as mentioned in numerous studies, cannot be accurately assessed in patients with symptomatic GB stones because of pathological conditions resulting in progressive dilatation of the CD due to the passage and impaction of gallstones or destruction of the CD, as in Mirizzi syndrome [23]. Hence, it is imperative to exercise caution to prevent misinterpretation of the short CD for the CBD during surgical procedures. A short CD is referred to as a “stone pathological dilatation,” and in the present study, it was not considered to be a laparoscopic variant. A long CD causes an increase in CD resistance and leads to impaired emptying of the GB; therefore, it is claimed to be one of the etiologic factors for gallstone formation [23].

In this study, the sole focus was on the CD length. CDs measuring >5 cm in length were considered long. A long, thin, and low-inserted CD of a parallel course fused with the CBD or CHD is of great surgical concern regardless of its lateral or medial insertion. It is usually mistaken for the bile ducts and carries a high risk of iatrogenic injury to the main biliary ducts.

Of the 26 variations in this study, the reported incidence of long and thin CD with low insertion rates was observed in four patients (15.4%) (Fig. 6). This result is probably similar to those reported in other laparoscopic CD length variation studies.

Figure 6. Lateral laparoscopic view of a long and thin cystic duct (CD) running parallel to the common bile duct after separation. GB, gallbladder.

The SVD is another uncommon anatomical and laparoscopic biliary ductal variant. A thin, small, accessory duct originates from the extra- or intra-right hepatic duct and traverses the GB fossa. It was barely detected during the separation of the lower part of the GB from the cystic bed. Therefore, the occurrence of surgical injury to these ducts is nearly certain, leading to severe complications such as bile leakage [25].

In numerous studies, subvesical (accessory) ducts have various terms and types, such as supravesical, cholecystohepatic, cystohepatic, and Luschka ducts [24–27]. In contrast, the SVD was initially incorrectly referred to as the “ducts of Luschka.” The ducts of Luschka do not open into the GB, and they differ from the three aberrant bile ducts, which drain part of the right lobe into the CD or GB [25,27,28].

Preoperative diagnosis of SVDs is unusual and necessitates preoperative magnetic resonance imaging and cholangiography. However, these investigations are expensive, not routinely performed, and are unavailable under our conditions. The diagnosis is usually made intraoperatively by raising the index of suspicion and carefully separating the GB from the liver bed. Injury to these ducts can lead to bile leakage and postoperative peritonitis.

Several studies have indicated that the combined incidence of cystohepatic and cholecystohepatic ducts varies from 0.2% to 2.3% [29]. Iida et al. [28] found that in their study of 2,107 patients who underwent cholecystectomy, only eight (0.83%) patients were diagnosed with SVDs. In this study, SVDs were found in three patients, and the incidence was 0.8%. Two patients were diagnosed with SVDs during surgery (Fig. 7). The third patient was a young woman who came back 3 days later with signs of peritonitis and underwent a late laparotomy, which revealed a focal leakage of bile from the GB bed due to missed SVDs.

Figure 7. Two different cases of subvesical duct (SVD). (A) Intact SVD at the liver-gallbladder bed. (B) Partially divided SVD after separation and division of th cystic duct (CD).

The two most serious complications of LC are intraoperative bleeding and bile leakage due to iatrogenic injury. Therefore, with precise surgical techniques, clear visualization of anatomical landmarks, and meticulous tissue dissection, this risk can be minimized [2,26].

In LC, adequate upward retraction of the grasped GB fundus gives a different view of the hepatocystic area (medial, lateral, anterior, and posterior), thus introducing the term “laparoscopic anatomy” [11]. The term of “critical view of safety (CVS)” use to described as the most important step in avoiding bile duct injury during a procedure. A CVS is that a fixed anatomical landmark helps the surgeon identify and stay in the safe zone of dissection [9]. It is imperative to identify the CVS and provide clues as to where to safely commence the dissection.

Although Calot’s triangle is an important area containing CA and CD, it is considered a constrained area. To identify potential anatomical variations, a larger window of the hepatocystic region and beyond is required. The literature suggests that the safe zone of dissection is limited to the hepatocystic triangle, which anatomically contains the CHD on the medial side, the CD caudally, and the liver under the surface cranially [9]. However, it is important to remember that the safe zone of dissection is not always a safe zone. It could contain numerous anatomical variants, such as the RHA in Moynihan’s hump, DCAs, and accessory SVDs, which are vulnerable to iatrogenic injury. During dissection of this zone, bile duct injury can occur because of missed identification of the fused, long, and thin CD with the bile ducts. Additionally, inflammation in this zone makes dissection difficult and increases the risk of iatrogenic injury.

In severe chronic cholecystitis, the region beyond the CD (infundibulo-visceral zone) may represent a region of severe adhesion of the GB infundibulum to the duodenum or small intestine. Occasionally, this can lead to cysto-visceral fistulization, which can render LC hazardous. In addition, the CA passes through this zone, hooking the CD posteriorly before entering the hepatocystic triangle. This region should be meticulously dissected in an uncertain setting to prevent visceral injury and bleeding.

Intraoperative cholangiography, laparoscopic ultrasonography, indocyanine green in local pathology, and a fibrosed hepatocystic triangle are effective measures to identify the CD, CBD, and biliary vasculature before clipping and dividing. In limited-resources conditions, cholangiography, indocyanine green, laparoscopic ultrasonography, and hepatobiliary surgery are usually not available. In these circumstances, the antegrade (“dome-down” or fundus first) technique, often advocated for cholecystitis with a frozen hepatocystic triangle, would be beneficial [30]. Otherwise, partial cholecystectomy could be a wise decision.

Moreover, enhanced equipment, improved hand and eye coordination, and a thorough understanding of biliary anatomy can make LC more successful and be performed safely at the 100% level [19].

In conclusion, biliary vascular variations are more common than biliary ductal variations. It is reasonable to anticipate anatomical variations in any zone of dissection in LC. The LC procedure is not effortless; however, it is still a viable option if surgeons are aware of the anatomical variations and the alterations caused by pathological processes.

Ethics statement

We conducted this study in compliance with the principles of the Declaration of the International Conference of Harmonization-Good Clinical Practice Guidelines. The study’s protocol was reviewed and approved by the Research and Ethics Committee in the Postgraduate Studies and Scientific Research Department, Faculty of Medicine and Health Sciences, University of Aden, Yemen (REC-191-2024). Prior to the operation, all patients who participated in the study provided written informed consent including information about the purpose of the study, stating that this is an informational study and not experimental research and that images taken during surgery will be anonymized. Each adult patient has to sign this written and dated consent form personally, while for children under 18 years old, the consent form has to be signed by one of the parents or by the adult person directly responsible for the child.

Authors’ contributions

Conceptualization: MGMH

Data curation, Project administration: MGMH, NAHS

Formal analysis: SAS

Investigation: All authors

Methodology: NAHS

Visualization: MGMH, NAHS, PU

Writing–original draft: MGMH, NAHS

Writing–review & editing: MGMH, NAHS

All authors read and approved the final manuscript.

Conflict of interest

All authors have no conflicts of interest to declare.

Funding/support

None.

Data availability

The data presented in this study are available upon reasonable request to the corresponding author.