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“Pes anserinus” of the right phrenic nerve innervating the serous membrane of the liver: a case report (anatomical study)
Morphologie, 2004, 88, 203-205 © Masson, Paris, 2004
ORIGINAL ARTICLE
“PES ANSERINUS” OF THE RIGHT PHRENIC NERVE INNERVATING THE SEROUS MEMBRANE OF THE LIVER: A CASE REPORT (ANATOMICAL STUDY)
K. NATSIS (1), G. PARASKEVAS (1), B. PAPAZIOGAS (2), A. AGIABASIS (1)† (1) Department of Anatomy. (2) 2nd Surgical Clinic, Medical School of the Aristotle University of Thessaloniki, Greece.
SUMMARY
RÉSUMÉ
During the preparations of cadavers for educational purposes we followed the course of the right phrenic nerve. On one of them and especially a female cadaver aged 72year-old we found a branch arising from the thoracic portion of the right phrenic and passing through the two layers of the falciform ligament distributed to the upper surface of the serous layer of the liver in the form of “pes anserinus”. As it is known, pain referred from the diaphragmatic peritoneum is classically felt in the shoulder tip but pain from thoracic surfaces supplied by the phrenic nerve is usually located there albeit vaguely. We believe that the above anatomical finding is the explanation of distinct radiating pain from the hepatic region to the right shoulder in some patients. The stimulations is carried through the phrenic nerve to the fourth cervical neurotome from were arise the supraclavicular nerves which are distributed to the shoulder region.
« Pes anserinus » du nerf phrénique droit innervant la membrane séreuse du foie : à propos d’un cas avec étude anatomique
Key words: phrenic nerve. pes anserinus. radiating pain.
Mots-clés : nerf phrénique. pes anserinus. irradiation douloureuse.
INTRODUCTION The right phrenic nerve arises usually from the fourth cervical root and directing at the neck almost vertically is located anteriorly to the anterior scalenus muscle. Consequently, it enters in the mediastinum anteriorly to the root of the right lung, between mediastinal pleura and pericardium and terminates at the diaphragm where it branches off to three motor branches. The posterior phrenic branch after giving off motor branches to the diaphragm, enters in the abdominal cavity through the foramen of the inferior vena cava as a sensory abdominal branch. The right posterior phrenic branch is more developed than the left one and participates in the formation of the hepatic and phrenic plexus, which innervate the liver with multiple thin rami which enter in the liver through its hilus. These two plexuses innervate the internal strucCorrespondence: B. PAPAZIOGAS, Fanariou str. 16, 55133 Kalamaria, Greece. E-mail: [email protected]
Au cours de préparations de cadavres à des fins éducatives, nous avons suivi le trajet du nerf phrénique droit. Dans un cas, le cadavre d’une femme âgée de 72 ans, nous avons observé la présence d’une branche provenant de la portion thoracique du nerf phrénique droit et passant à travers les deux couches du ligament falciforme et se distribuant à la surface séreuse du foie réalisant un aspect de « pes anserinus ». Comme il est bien classique, les douleurs provenant du péritoine diaphragmatique sont ressenties dans l’épaule mais celles provenant des surfaces thoraciques innervées par le nerf phrénique sont plus vagues. Nous pensons que cette donnée anatomique est l’explication de certaines irradiations douloureuses de la région hépatique dans l’épaule droite chez certains patients. Les stimulations sont véhiculées par le nerf phrénique jusqu’au 4e neurotome cervical d’où naissent les nerfs supra-claviculaires qui se distribuent aux épaules.
ture of the liver in combination with branches of the vagus nerve and the sympathetic trunk [1-4]. In our paper we noticed that in a cadaver the right phrenic nerve innervated the coronary ligament through a branch that was distributed to the ligament in the form of “pes anserinus” (goose-foot). That fact may explain the presence of radiating pain in the right shoulder in case of subdiaphragmatic or hepatic abscess or other hepatic lesions.
OUR CASE During the anatomical courses which took place at the Dissection Room of our Department of Anatomy we have found in a female cadaver aged 72-yearold a branch arising from the thoracic portion of the right phrenic nerve and directing anterior to the pericardium penetrated the sternocostal part of the diaphragm passed through the two layers of the falciform ligament and distributed to the upper surface of the serous layer of the liver in the form of “pes
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anserinus” (figure 1). After dissection of the anterior abdominal wall through insicion which have done along the right costal arch and anterior median line we prepared the antero-superior surface of the liver in which we noticed the presence of the just mentioned finding. We study the antero-superior surface in 28 cadavers and we found the existence of such nerval formation in one cadaver. Because of the too small size specimen we couldn’t exclude any specific incidence of that nerval formation in the general population so we present that finding as a case report.
DISCUSSION The abdominal branch of the right phrenic nerve enters in the celiac plexus connecting with the right semilunar ganglion. Rami from the right celiac plexus supply the right suprarenal gland, the inferior vena cava, the hepatic falciform and coronary ligaments and possibly via connection with celiac and hepatic plexuses the gallbladder. Also, on the right, at the junction of the celiac plexuses the right abdominal branch connects with a small phrenic ganglion [4, 5]. It may be noticed that the abdominal branch of the left phrenic nerve, which is thinner than the right one communicates with the phrenic ganglion [6]. The rami of the terminal branches of the right phrenic nerve which are distributed to the falciform ligament and the superior surface of the hepatic peritoneum have been described firstly by Luschka. The presence of these thin rami couldn’t be identified by Ramstrom after relative microscopic studies [7]. It is known that in various hepatic diseases the pain is radiating to the right shoulder. Especially, Andreoli et al. [8] found that subdiaphragmatic or hepatic abscess pain radiates to the tip of the right
FIG. 1. — The “pes anserinus” (with arrows) of the right phrenic nerve is distinguished between the two layers of the falciform ligament of the liver (D: diaphragm, F: falciform ligament, L: liver). FIG. 1. — Le « pes anserinus » (flèches) du nerf phrénique est observable entre les deux couches du ligament falciforme du foie (D : diaphragme, F : ligament falciforme, L : foie).
shoulder. For the explanation of that pain many theories have been stated, the most important of which is Mackenzie’s theory that has not however been proved anatomically. According to that theory splachnic lesions cause pain which doesn’t locate to the corresponding region but to distant regions through a mechanism of reflex. That theory explains the presence of abdominal pain in some cases but: a) it is found no anatomical relationship between afferent splachnic and efferent splachnic nerval trunks and b) the pain isn’t always radiating, but frequently is located to the affected organ. There is an opinion according to which various sensory nerval tracts exist that “connect” the viscera with the spinal cord which transmit the abdominal pain. One of these tracts is the phrenic nerve that receives stimuli from the capsule of Glisson, the hepatic ligaments, the tendinous portion of the diaphragm, the splenic capsule and the pericardium. The somatic pain which is caused by the irritation of peritoneum is located to distant region, such as in case of peritoneal irritation of the tendinous portion of the diaphragm, in which the pain is radiated to the shoulder, because the stimuli is transmitted to fourth cervical neutotome via the phrenic nerve; to the same neurotome end the supraclavicular nerves, which are the sensory nerves of the shoulder [9]. When the sensory endings of the phrenic nerve have been irritated it is caused pain at the tip of the shoulder (acromion) as the supraclavicular nerves that innervate that region are formatted by the C2C4 roots [10, 11]. According to Mc Minn [12] pains referred from the diaphragmatic peritoneum is classically felt in the shoulder tip but pain from thoracic surfaces supplied by the phrenic nerve is usually located there albeit vaguely. That radiating pain may be appeared only in case of irritation of the peritoneum of the inferior surface of the diaphragm. Shoulder pain may be caused by disturbance of the serous membranes that cover the diaphragm’s surfaces, the pleura superiorly and peritoneum inferiorly, which are innervated by phrenic nerve. It has been reported that shoulder pain may be appeared after thoracotomy because of irritation of the pleural endings of the phrenic nerve [13] and after presentation of pneumonia [14] and lung cancer [15] because of intrathoracic involvement of the phrenic nerve. If the disturbance is anteriorly then the pain is radiated to the supraclavicular region, while when the disturbance is posteriorly then the pain is radiated to the acromion. It is impossible from the exact location of the shoulder pain to conclude if the pain is referring to the superior or inferior surface of the diaphragm [16]. We think that our finding is possible to explain the appearance of the right shoulder pain in some individuals in case of hepatic lesions, in specific sites of shoulder and supraclavicular region, because the “goose-foot” (pes anserinus) distribution of the right phrenic nerve is not a constant finding. It is a subject of further research to find the possible correlation between the presence of that finding and the exact location of the shoulder pain.
Right phrenic nerve innervating serous membrane of the liver
205
CONCLUSION
[7] Sklavounos G. Textbook of Human Anatomy, volume 3, 2nd edition, Ed. P. Sakellariou, Athens, 1913, 634-637.
The presence of “pes anserinus” distribution of the right phrenic nerve innervating the serous membrane of the liver may present the anatomical basis for the clinical observation that in some patients the pain caused by subdiaphragmatic diseases radiates in specific sites of the shoulder and supraclavicular region.
[8] Andreoli T, Carpenter C, Plum F, Smith L. Cecil Essentials of Medicine, WB. Saunders Co, Philadelphia, 1989, 419-420.
RÉFÉRENCES
[9] Krikelis GN. Clinical examination and diagnosis, 4 th edition, ed. G.K. Parisianos, Athens, 1989, 473-476. [10] Plessis D. A synopsis of surgical anatomy. 11 th edition, J Wright and Sons Ltd, Bristol, 1975, 88-89. [11] Braunwald E, Isselbacher K, Petersdorf R, Wilson J, Martin J, Fanci A. Harrison’s. Principles of Internal Medicine, 11th edition, Mc Graw-Hill Book Company, 1967, 14.
[1] Hollinshead HW. Textbook of Anatomy, 4 th edition, Harper and Row, Philadelphia, 1985, 519.
[12] McMinn R. Last’s Anatomy, Regional and Applied, 8th edition, Churchill Livingstone, Edinburgh, 1990, 261262.
[2] Moore KL. Clinically Oriented Anatomy, 3 rd edition, Williams and Wilkins, Baltimore, 1992, 80.
[13] Scawn N, Pennefather S, Soorae A, Wang J, Russel G. Ipsilateral shoulder pain after thoracotom ywith epidural analgesia: the influence of phrenic nerve infiltration with lidocaine. Anesth Analg 2001; 93: 260-264.
[3] Williams P, Warwick R, Dyson M, Bannister L. Gray’s Anatomy, 38th edition, Churchill Livingstone, London, 1995, 1129-1130. [4] Romanes G. Cunningham’s Textbook of Anatomy. 12th Edition, Oxford University Press, Oxford, 1991, 773.
[14] Petchkrua W, Harris S. Shoulder pain as an unusual presentation of pneumonia in a stroke patient: a case report. Arch Phys Med Rehabil 2000; 81: 827-829.
[5] Savas A. Textbook of Human Anatomy, Volume 4, Ed. Spyropoulou, Thessaloniki, 1968, 486.
[15] Khaw P, Ball D. Relief of non-metastatic shoulder pain with mediastinal radiotherapy in patients with lung cancer. Lung Cancer 2000; 28: 51-54.
[6] Sklavounos G. Textbook of Human Anatomy, volume 3, 3rd edition, Ed. N. Tarousopoulou, Athens, 1928, 270-271.
[16] Glockner SM. Shoulder pain: a diagnostic dilemma. Am Fam Physician 1995; 51: 1677-1687.
ORIGINAL ARTICLE
“PES ANSERINUS” OF THE RIGHT PHRENIC NERVE INNERVATING THE SEROUS MEMBRANE OF THE LIVER: A CASE REPORT (ANATOMICAL STUDY)
K. NATSIS (1), G. PARASKEVAS (1), B. PAPAZIOGAS (2), A. AGIABASIS (1)† (1) Department of Anatomy. (2) 2nd Surgical Clinic, Medical School of the Aristotle University of Thessaloniki, Greece.
SUMMARY
RÉSUMÉ
During the preparations of cadavers for educational purposes we followed the course of the right phrenic nerve. On one of them and especially a female cadaver aged 72year-old we found a branch arising from the thoracic portion of the right phrenic and passing through the two layers of the falciform ligament distributed to the upper surface of the serous layer of the liver in the form of “pes anserinus”. As it is known, pain referred from the diaphragmatic peritoneum is classically felt in the shoulder tip but pain from thoracic surfaces supplied by the phrenic nerve is usually located there albeit vaguely. We believe that the above anatomical finding is the explanation of distinct radiating pain from the hepatic region to the right shoulder in some patients. The stimulations is carried through the phrenic nerve to the fourth cervical neurotome from were arise the supraclavicular nerves which are distributed to the shoulder region.
« Pes anserinus » du nerf phrénique droit innervant la membrane séreuse du foie : à propos d’un cas avec étude anatomique
Key words: phrenic nerve. pes anserinus. radiating pain.
Mots-clés : nerf phrénique. pes anserinus. irradiation douloureuse.
INTRODUCTION The right phrenic nerve arises usually from the fourth cervical root and directing at the neck almost vertically is located anteriorly to the anterior scalenus muscle. Consequently, it enters in the mediastinum anteriorly to the root of the right lung, between mediastinal pleura and pericardium and terminates at the diaphragm where it branches off to three motor branches. The posterior phrenic branch after giving off motor branches to the diaphragm, enters in the abdominal cavity through the foramen of the inferior vena cava as a sensory abdominal branch. The right posterior phrenic branch is more developed than the left one and participates in the formation of the hepatic and phrenic plexus, which innervate the liver with multiple thin rami which enter in the liver through its hilus. These two plexuses innervate the internal strucCorrespondence: B. PAPAZIOGAS, Fanariou str. 16, 55133 Kalamaria, Greece. E-mail: [email protected]
Au cours de préparations de cadavres à des fins éducatives, nous avons suivi le trajet du nerf phrénique droit. Dans un cas, le cadavre d’une femme âgée de 72 ans, nous avons observé la présence d’une branche provenant de la portion thoracique du nerf phrénique droit et passant à travers les deux couches du ligament falciforme et se distribuant à la surface séreuse du foie réalisant un aspect de « pes anserinus ». Comme il est bien classique, les douleurs provenant du péritoine diaphragmatique sont ressenties dans l’épaule mais celles provenant des surfaces thoraciques innervées par le nerf phrénique sont plus vagues. Nous pensons que cette donnée anatomique est l’explication de certaines irradiations douloureuses de la région hépatique dans l’épaule droite chez certains patients. Les stimulations sont véhiculées par le nerf phrénique jusqu’au 4e neurotome cervical d’où naissent les nerfs supra-claviculaires qui se distribuent aux épaules.
ture of the liver in combination with branches of the vagus nerve and the sympathetic trunk [1-4]. In our paper we noticed that in a cadaver the right phrenic nerve innervated the coronary ligament through a branch that was distributed to the ligament in the form of “pes anserinus” (goose-foot). That fact may explain the presence of radiating pain in the right shoulder in case of subdiaphragmatic or hepatic abscess or other hepatic lesions.
OUR CASE During the anatomical courses which took place at the Dissection Room of our Department of Anatomy we have found in a female cadaver aged 72-yearold a branch arising from the thoracic portion of the right phrenic nerve and directing anterior to the pericardium penetrated the sternocostal part of the diaphragm passed through the two layers of the falciform ligament and distributed to the upper surface of the serous layer of the liver in the form of “pes
204
K. NATSIS et al.
anserinus” (figure 1). After dissection of the anterior abdominal wall through insicion which have done along the right costal arch and anterior median line we prepared the antero-superior surface of the liver in which we noticed the presence of the just mentioned finding. We study the antero-superior surface in 28 cadavers and we found the existence of such nerval formation in one cadaver. Because of the too small size specimen we couldn’t exclude any specific incidence of that nerval formation in the general population so we present that finding as a case report.
DISCUSSION The abdominal branch of the right phrenic nerve enters in the celiac plexus connecting with the right semilunar ganglion. Rami from the right celiac plexus supply the right suprarenal gland, the inferior vena cava, the hepatic falciform and coronary ligaments and possibly via connection with celiac and hepatic plexuses the gallbladder. Also, on the right, at the junction of the celiac plexuses the right abdominal branch connects with a small phrenic ganglion [4, 5]. It may be noticed that the abdominal branch of the left phrenic nerve, which is thinner than the right one communicates with the phrenic ganglion [6]. The rami of the terminal branches of the right phrenic nerve which are distributed to the falciform ligament and the superior surface of the hepatic peritoneum have been described firstly by Luschka. The presence of these thin rami couldn’t be identified by Ramstrom after relative microscopic studies [7]. It is known that in various hepatic diseases the pain is radiating to the right shoulder. Especially, Andreoli et al. [8] found that subdiaphragmatic or hepatic abscess pain radiates to the tip of the right
FIG. 1. — The “pes anserinus” (with arrows) of the right phrenic nerve is distinguished between the two layers of the falciform ligament of the liver (D: diaphragm, F: falciform ligament, L: liver). FIG. 1. — Le « pes anserinus » (flèches) du nerf phrénique est observable entre les deux couches du ligament falciforme du foie (D : diaphragme, F : ligament falciforme, L : foie).
shoulder. For the explanation of that pain many theories have been stated, the most important of which is Mackenzie’s theory that has not however been proved anatomically. According to that theory splachnic lesions cause pain which doesn’t locate to the corresponding region but to distant regions through a mechanism of reflex. That theory explains the presence of abdominal pain in some cases but: a) it is found no anatomical relationship between afferent splachnic and efferent splachnic nerval trunks and b) the pain isn’t always radiating, but frequently is located to the affected organ. There is an opinion according to which various sensory nerval tracts exist that “connect” the viscera with the spinal cord which transmit the abdominal pain. One of these tracts is the phrenic nerve that receives stimuli from the capsule of Glisson, the hepatic ligaments, the tendinous portion of the diaphragm, the splenic capsule and the pericardium. The somatic pain which is caused by the irritation of peritoneum is located to distant region, such as in case of peritoneal irritation of the tendinous portion of the diaphragm, in which the pain is radiated to the shoulder, because the stimuli is transmitted to fourth cervical neutotome via the phrenic nerve; to the same neurotome end the supraclavicular nerves, which are the sensory nerves of the shoulder [9]. When the sensory endings of the phrenic nerve have been irritated it is caused pain at the tip of the shoulder (acromion) as the supraclavicular nerves that innervate that region are formatted by the C2C4 roots [10, 11]. According to Mc Minn [12] pains referred from the diaphragmatic peritoneum is classically felt in the shoulder tip but pain from thoracic surfaces supplied by the phrenic nerve is usually located there albeit vaguely. That radiating pain may be appeared only in case of irritation of the peritoneum of the inferior surface of the diaphragm. Shoulder pain may be caused by disturbance of the serous membranes that cover the diaphragm’s surfaces, the pleura superiorly and peritoneum inferiorly, which are innervated by phrenic nerve. It has been reported that shoulder pain may be appeared after thoracotomy because of irritation of the pleural endings of the phrenic nerve [13] and after presentation of pneumonia [14] and lung cancer [15] because of intrathoracic involvement of the phrenic nerve. If the disturbance is anteriorly then the pain is radiated to the supraclavicular region, while when the disturbance is posteriorly then the pain is radiated to the acromion. It is impossible from the exact location of the shoulder pain to conclude if the pain is referring to the superior or inferior surface of the diaphragm [16]. We think that our finding is possible to explain the appearance of the right shoulder pain in some individuals in case of hepatic lesions, in specific sites of shoulder and supraclavicular region, because the “goose-foot” (pes anserinus) distribution of the right phrenic nerve is not a constant finding. It is a subject of further research to find the possible correlation between the presence of that finding and the exact location of the shoulder pain.
Right phrenic nerve innervating serous membrane of the liver
205
CONCLUSION
[7] Sklavounos G. Textbook of Human Anatomy, volume 3, 2nd edition, Ed. P. Sakellariou, Athens, 1913, 634-637.
The presence of “pes anserinus” distribution of the right phrenic nerve innervating the serous membrane of the liver may present the anatomical basis for the clinical observation that in some patients the pain caused by subdiaphragmatic diseases radiates in specific sites of the shoulder and supraclavicular region.
[8] Andreoli T, Carpenter C, Plum F, Smith L. Cecil Essentials of Medicine, WB. Saunders Co, Philadelphia, 1989, 419-420.
RÉFÉRENCES
[9] Krikelis GN. Clinical examination and diagnosis, 4 th edition, ed. G.K. Parisianos, Athens, 1989, 473-476. [10] Plessis D. A synopsis of surgical anatomy. 11 th edition, J Wright and Sons Ltd, Bristol, 1975, 88-89. [11] Braunwald E, Isselbacher K, Petersdorf R, Wilson J, Martin J, Fanci A. Harrison’s. Principles of Internal Medicine, 11th edition, Mc Graw-Hill Book Company, 1967, 14.
[1] Hollinshead HW. Textbook of Anatomy, 4 th edition, Harper and Row, Philadelphia, 1985, 519.
[12] McMinn R. Last’s Anatomy, Regional and Applied, 8th edition, Churchill Livingstone, Edinburgh, 1990, 261262.
[2] Moore KL. Clinically Oriented Anatomy, 3 rd edition, Williams and Wilkins, Baltimore, 1992, 80.
[13] Scawn N, Pennefather S, Soorae A, Wang J, Russel G. Ipsilateral shoulder pain after thoracotom ywith epidural analgesia: the influence of phrenic nerve infiltration with lidocaine. Anesth Analg 2001; 93: 260-264.
[3] Williams P, Warwick R, Dyson M, Bannister L. Gray’s Anatomy, 38th edition, Churchill Livingstone, London, 1995, 1129-1130. [4] Romanes G. Cunningham’s Textbook of Anatomy. 12th Edition, Oxford University Press, Oxford, 1991, 773.
[14] Petchkrua W, Harris S. Shoulder pain as an unusual presentation of pneumonia in a stroke patient: a case report. Arch Phys Med Rehabil 2000; 81: 827-829.
[5] Savas A. Textbook of Human Anatomy, Volume 4, Ed. Spyropoulou, Thessaloniki, 1968, 486.
[15] Khaw P, Ball D. Relief of non-metastatic shoulder pain with mediastinal radiotherapy in patients with lung cancer. Lung Cancer 2000; 28: 51-54.
[6] Sklavounos G. Textbook of Human Anatomy, volume 3, 3rd edition, Ed. N. Tarousopoulou, Athens, 1928, 270-271.
[16] Glockner SM. Shoulder pain: a diagnostic dilemma. Am Fam Physician 1995; 51: 1677-1687.