Vol.:(0123456789)1 3 Surgical and Radiologic Anatomy (2021) 43:1243–1248 https://doi.org/10.1007/s00276-020-02642-0 ORIGINAL ARTICLE Anatomical variation and distribution of the vagus nerve in the esophageal hiatus: a cross‑sectional study of post‑mortem cases in Uganda Kamoga Ronald1  · Nakidde Gladys2 · Kintu Mugagga1 · Grace Muwanga1 · Amadi O. Ihunwo3 Received: 16 June 2020 / Accepted: 2 December 2020 / Published online: 2 January 2021 © The Author(s), under exclusive licence to Springer-Verlag France SAS part of Springer Nature 2021 Abstract Purpose Vagus nerve injuries during gastroesophageal surgery may cause significant symptoms due to loss of vagal anti- inflammatory and neuromodulator function. Many previous studies have shown high anatomical variability of the vagus nerve at the esophageal hiatus, but information on its variability in Uganda specifically and Africa in general is scanty. This study provides a reliable and detailed description of the anatomical variation and distribution of the vagus nerve in the esophageal hiatus region of post-mortem cases in Uganda. Methods This was an analytical cross-sectional survey of 67 unclaimed post-mortem cases. Data collection used a pretested data collection form. Data were entered into Epi-Info version 6.0 data base then exported into STATA software 13.0 for analysis. Results The pattern of the anterior vagal trunk structures at the esophageal hiatus was: single trunk [65.7%]; biplexus [20.9%]; triplexus [8.9%] and double-but-not-connected trunks [4.5%]. The pattern of the posterior trunk structures were: single trunk [85.1%]; biplexus 10.4% and triplexus [4.5%]. There was no statistically significant gender difference in the pattern of vagal fibres. There was no major differences in the pattern from comparable British studies. Conclusion The study confirmed high variability in the distribution of the vagus nerve at the esophageal hiatus, unrelated to gender differences. Surgeons must consider and identify variants of vagal innervation when carrying out surgery at the gastroesophageal junction to avoid accidental vagal injuries. Published surgical techniques for preserving vagal function are valid in Uganda. Keywords Vagus nerve · Uganda · Distribution · Variation · Esophageal hiatus Introduction Integrity of the vagus nerve is of great importance for nor- mal gastrointestinal neuromodulatory and anti-inflammatory functions. Many previous studies have demonstrated high anatomical variability of the vagus nerve at the esophageal hiatus and in the abdomen [2, 18]. These variations are highly significant for surgeons to consider during operative procedures at the gastroesophageal junction. Injury to the vagus nerve is known to be a significant risk during gas- trothoracic surgery, particularly commonly performed pro- cedures such as antireflux surgery (ARS) and hiatal hernia repairs. Complication rates have been shown to be common after surgery affecting between 20 and 67% of patients. Inadvertent vagotomy causes significant delayed gastric emptying (gastroparesis) and may cause gastroesophageal reflux. These symptoms may be sufficiently severe to require reoperation, and the reoperation rate is significant [2, 7, 15, 17, 19]. Damage to the hepatic branch of the anterior vagus nerve during Laparoscopic Nissen Fundoplication has been reported to prolong the gallbladder emptying time (GET) increasing the risk of gallstones [5, 12]. In addition, the increasingly valuable technique of vagal nerve stimulation * Kamoga Ronald rkamoga@must.ac.ug 1 Department of Human Anatomy, Faculty of Medicine, Mbarara University of Science and Technology, P.O. Box 1410, Mbarara city, Uganda 2 Departments of Nursing, Bishop Stuart University, P. O. Box 09, Mbarara city, Uganda 3 School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa http://orcid.org/0000-0001-9512-9381 http://crossmark.crossref.org/dialog/?doi=10.1007/s00276-020-02642-0&domain=pdf 1244 Surgical and Radiologic Anatomy (2021) 43:1243–1248 1 3 (VNS) relies on having an intact vagal nerve, and patients who have had vagal nerve damage cannot be treated by VNS. VNS is currently approved for management of intractable epilepsy, severe depression, inflammatory arthritis, and Crohn’s disease [8, 13, 14]. Hundreds of clinical trials are currently underway, to examine the potential use of VNS to manage heart failure, stroke, Alzheimer’s disease, traumatic brain injuries, asthma, diabetes, obesity, post-operative ileus and septic shock among others [3, 4, 6, 13, 20–22]. This study sought to validate and provide a reliable and detailed description and statistical analysis of the anatomical varia- tion and distribution of the vagus nerve in the esophageal hiatus region in Uganda. Study findings could provide con- firmation of the pattern of vagal innervation, and inform surgeons of anatomical variations to avoid accidental injury to the vagus nerve. Materials and method This was an analytical cross-sectional survey using 67 post- mortems on frozen bodies at Mbarara Regional Referral Hospital, the teaching hospital for Mbarara University of Science and Technology, and Mulago City Mortuary which is the main mortuary for Mulago National Referral hospital located in Kampala, the capital city of Uganda. The bod- ies were of patients who were unclaimed by relatives, the Ugandan legal position being that the bodies become prop- erty of the institution after a fixed period, and available for anatomical teaching and research. The routine post-mortem pathological dissection technique of the participating hospi- tals was used. A midline incision was made extending from the xiphoid process to the symphysis pubis. The incision was extended cranially through the sternum up to the supraster- nal notch. Next, the diaphragm was stripped from the tho- racic and abdominal wall attachments and its attachments to the pericardium and pleural membranes. The esophagus was cut approximately 2 cm superior to the esophageal hiatus. Then, all the abdominal visceral including the diaphragm were stripped and placed on the dissection table. The esoph- ageal hiatus and the stomach were exposed by reflecting the lesser omentum and the left liver lobe laterally. We visually identified, examined and traced the distribution of the ante- rior and posterior vagus nerves noting variations. We used the diaphragmatic constriction (Inferior esophageal “sphinc- ter”) located approximately 2 cm superior to the gastroe- sophageal junction as a landmark [11] to identify patterns and variations by careful dissections and visual identification at this point. Data were collected using a pretested data col- lection form. Specimens were organized and labeled; and data obtained from each were registered on individualized charts. Data collection was done by the first author KR with an experienced mortuary assistant as a research assistant. Every 5th body was dissected by KR together with MG, an experienced anatomist to ensure external quality control. A high-resolution camera (4.3 megapixels) was used to take photographs to capture the entry and exit and the distribution pattern of the vagus nerve through the esophageal hiatus for possible future reference. Data were entered in a database developed in Epi-Info version6.0 and then exported into STATA software 13.0 for analysis. Results General information In this study, 67 adult post-mortem cases (16 females and 52 males) were included (Table 1). Distribution of anterior vagal trunk in esophageal hiatus The most common pattern was single anterior trunk (65.7%) followed by biplexus (20.9%); triplexus (8.9%) and the least common was double-but-not connected (4.5%), (Figs. 1, 2, 3). Distribution of posterior vagal trunk in esophageal hiatus The most common pattern was single posterior trunk (85.1%) followed by biplexus (10.4%) and triplexus Table 1 Distribution of vagus nerve through the diaphragmatic open- ing; double-but-not-connected means two separate trunks; biplexus means two interconnected trunks and triplexus means three intercon- nected trunks Diaphragmatic opening distribution Characteristic N n (%) Structure in hiatus of anterior trunk, n (%) 67  Single 44 (65.7)  Double-but-not-connected 3 (4.5)  Biplexus 14 (20.9)  Triplexus 6 (8.9) Structure in hiatus of posterior trunk, n (%) 67  Single 57 (85.1)  Biplexus 7 (10.4)  Triplexus 3 (4.5) Vagal overall trunks through diaphragm, n (%) 67  2 41 (61.2)  3 14 (20.9)  4 8 (11.9)  5 4 (6.0) 1245Surgical and Radiologic Anatomy (2021) 43:1243–1248 1 3 (4.5%). Generally, 34.3% and 14.9% of anterior and pos- terior trunks respectively were observed to go through esophageal hiatus as one of the many varieties of multi- ple trunk structures such as double trunks not connected, biplexus and triplexus. The number of trunks through the diaphragm ranged between 2 and 5 with 2 occurring most frequently (61.2%) and 5 least frequent (6%), (Fig. 4). Distribution of the vagus nerve in the esophageal region across gender There was no statistically significant (p > 0.05) variation across gender. The observed difference was absence of posterior vagus biplexus among all female participants (Table 2). Discussion and conclusion The study found a single posterior and a single anterior trunk as the most common pattern through the esophageal hiatus. The proportion of participants with single anterior trunk was 65.7%, with gender-specific proportions of 66.7% males and 62.5% females. The proportion of participants with single posterior trunks was 85.1%, with gender-spe- cific percentages of 82.4% males and 93% females. Multiple trunks were also observed: 34.3% of cadavers had multiple anterior trunks, and 14.9% of the cadavers had multiple pos- terior trunks. The study did not find statistically significant (P > 0.05) difference of the vagus nerve in the esophageal region when analyzed by gender. Our study result of 65.7% single anterior trunk was close to the 67% reported by Mitchell [10] in the United Kingdom; 67% by Ruckley et al. [16] in Scotland and 58% by Mackay and Andrews [9] in the United States of America (USA). However, it was considerably higher than 13% reported by Baccaro et al. [2] in Argentina. The latter study had a very small sample size of 15 specimens compared to 67 speci- mens utilized in our study which may explain their very different result. Similarly, in our study, 85.1% of cases cadavers had a single posterior trunk through the esophageal hiatus. This finding was close to the 95% reported by Ruckley et al. [16] in Scotland, but higher than 60% observed by Alden [1] and 53% by Mitchell [10] elsewhere in the United Kingdom. Multiple structures (double unconnected trunks, biplex- uses and triplexuses) through the diaphragm were identified in this study, 34.3% in the anterior trunk, and 14.9% in the posterior trunk. Baccaro et al. [2] in Argentina reported 87% presence of multiple structures of the anterior trunk, while Alden [1] in the USA reported 78% multiple structures in the anterior trunk, and 20% multiple structures in the posterior trunk. These studies and our findings confirm findings that multiple structures are commoner in the anterior trunk than the posterior trunk. We noted that multiple vagal trunks were rarer in the female group in our study and a triplexus struc- ture totally absent, although the numbers were too small to allow valid statistical sub analysis. There was a difference between the proportion of multiple structures between our study (34.3%) and the studies by Baccaro et al. [2] and Alden [1]. Our study and the two studies had very different sample Fig. 1 2 vagal trunks through diaphragm; A single anterior trunk marked with single arrow pointing to the left and a single posterior trunk marked by double arrows pointing to the left Fig. 2 3 vagal trunks through esophageal hiatus: an anterior biplexus marked by arrows pointing downward and a single posterior trunk marked by arrows pointing upwards 1246 Surgical and Radiologic Anatomy (2021) 43:1243–1248 1 3 sizes. The sample size was 67 in our study, while it was 15 for Baccaro et al. and 50 for Alden. The other possible expla- nation for the difference in the incidence of multiple vagal trunks could be differences in dissection and observation skills. The current study did not find statistically significant gender variations, and we were unable to find any previous studies that compared vagus nerve variations in esophageal hiatus across gender. In summary, we would comment that, it is crucial for antireflux; hiatal hernia repair and surgical peptic Ulcer Disease (PUD) surgeons to have consideration for vari- ations. It is particularly important for surgeons to recog- nize that, multiple vagal structures may exist in the hiatal area. Identification of single anterior and posterior trunks at operation is insufficient to avoid the possibility of producing injuries to vagal fibres, with possible life threatening com- plications resulting from the parasympathetic denervation of many vital organs distal to the esophageal hiatus [12, 17]. Conclusions There is high variability in the distribution of the vagus nerve in the esophageal hiatus that is not related to gen- der differences. Surgeons must consider and identify vari- ants of vagal innervation when carrying out surgery at the Fig. 3 Structural varieties of the anterior vagus nerve through the esophageal hiatus; (i) Single trunk (a), 65.7%; (ii) Biplexus (b), 20.9%; (iii) Triplexus (c), 8.9% and (iv) Double-but-not connected; (d), 4.5%; h is the hepatic branch of the anterior vagus nerve; g is the gastric branch of anterior vagus (of Laterjet); e is the diaphragm 1247Surgical and Radiologic Anatomy (2021) 43:1243–1248 1 3 gastroesophageal junction to avoid accidental vagal inju- ries. Published surgical techniques for preserving vagal function are valid in any part of the world. Acknowledgements We wish to thank Prof. Celestino Obua for research skills mentorship, and for securing the funding we used from the Makerere-Sweden Research Cooperation (SIDA). We also thank Dr Atwine Daniel who contributed invaluable insight in proposal development and data analysis. We also acknowledge the Director of Health services, Uganda Police, Dr Moses Byaruhanga and Dr. Samuel Kalungi, a senior pathologist, whose contribution in data collection made this research possible. Author contributions RK: Project development, data collection or management, data analysis, manuscript writing/editing. GN: project development, data collection or management, manuscript writing/edit- ing. MK: manuscript writing/editing. GM: project development, data collection, manuscript writing/editing. IOA: data analysis, manuscript writing/editing. Funding The work was supported by Makerere-Sweden Research Cooperation (Makerere University SIDA-program) as part of the pro- ject titled Makerere-SIDA PHASE IV 2015/2020 under Grant Agree- ment No. [DRGT 377]. Availability of data and materials The full dataset generated and ana- lyzed during the current study are not publicly available for ethical reasons. However, deidentified data can be made available from the corresponding author on reasonable request. Compliance with ethical standards Conflict of interest All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials dis- cussed in this manuscript. Consent to participate Informed consent was waived because researchers only accessed unclaimed bodies that had no identified living relative(s) or legal representatives. Administrative permission Fig. 4 Structural varieties of the posterior vagus nerve through esophageal hiatus: (i) Single trunk (a), 65.7%; (ii) Biplexus (b), 20.9%; (iii) Tri- plexus (c), 8.9%; g is the gastric branch of posterior vagus; and t is celiac branch of posterior vagus; d is the diaphragm Table 2 Distribution of the vagus nerve in the esophageal hiatus across gender; Double- but-not-connected means two separate trunks; biplexus means two interconnected trunks and triplexus means three interconnected trunks Characteristic N Overall n (%) Gender p value Male n (%) Female n (%) Structure in hiatus of anterior trunk, n (%) 67 0.873  Single 44 (65.7) 34 (66.7) 10 (62.5)  Double-but-not-connected 3 (4.5) 2 (3.9) 1 (6.2)  Biplexus 14 (20.9) 10 (19.6) 4 (25.0)  Triplexus 6 (8.9) 5 (9.8) 1 (6.3) Structure in hiatus of posterior trunk, n (%) 67 0.295  Single 57 (85.1) 42 (82.4) 15 (93.7)  Biplexus 7 (10.4) 7 (13.7) 0 (0.00)  Triplexus 3 (4.5) 2 (3.9) 1 (6.3) Overall vagal trunks through diaphragm, n (%) 67 0.942  2 41 (61.2) 31 (60.8) 10 (62.5)  3 14 (20.9) 10 (19.6) 4 (25.0)  4 8 (11.9) 7 (13.7) 1 (6.2)  5 4 (6.0) 3 (5.9) 1 (6.2) 1248 Surgical and Radiologic Anatomy (2021) 43:1243–1248 1 3 was received from the Uganda police authorities, the custodians of all unclaimed bodies, before data collection. 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Neu- ral Regener Res. https ://doi.org/10.4103/1673-5374.14178 3 Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. https://doi.org/10.4172/2161-0940.1000121 https://doi.org/10.1111/all.13790 https://doi.org/10.1371/journal.pone.0087785 https://doi.org/10.1371/journal.pone.0087785 https://doi.org/10.3389/fnins.2019.00280 https://doi.org/10.3389/fnins.2019.00280 https://doi.org/10.1007/s00464-018-6562-9 https://doi.org/10.1016/j.berh.2014.10.015 https://doi.org/10.1007/s00268-013-1958-0 https://doi.org/10.1073/pnas.1919040116 https://doi.org/10.2147/JIR.S163248 https://doi.org/10.1038/ajg.2016.42 https://doi.org/10.1038/ajg.2016.42 https://doi.org/10.1113/EP087351 https://doi.org/10.4103/1673-5374.141783 Anatomical variation and distribution of the vagus nerve in the esophageal hiatus: a cross-sectional study of post-mortem cases in Uganda Abstract Purpose Methods Results Conclusion Introduction Materials and method Results General information Distribution of anterior vagal trunk in esophageal hiatus Distribution of posterior vagal trunk in esophageal hiatus Distribution of the vagus nerve in the esophageal region across gender Discussion and conclusion Conclusions Acknowledgements References