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Horner Syndrome After Carotid Sheath Surgery in a Pig: Anatomic Study of Cervical Sympathetic Chain

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Horner Syndrome After Carotid Sheath Surgery in a Pig: Anatomic Study of Cervical Sympathetic Chain Comparative Medicine Vol 61, No 5 Copyright 2011 October 2011 by the American Association for Laboratory Animal Science Pages 453–456 Case Report Horner Syndrome After Carotid Sheath Surgery in a Pig: Anatomic Study of Cervical Sympathetic Chain Peng Ding,1,* Ralph P Tufano,2 Regina Campbell- Malone,1 Wallace Feng,1 Sang Jun Kim,1 and Rebecca Z German1 In an experimental model, iatrogenic Horner syndrome developed after a right carotid sheath surgery in an infant pig (Sus scrofa). Horner syndrome is a classic clinical triad consisting of ipsilateral eyelid ptosis, pupil miosis, and facial anhydrosis. This syndrome results from cervical sympathetic chain (CSC) paresis and usually is acquired in humans. To determine whether the development of Horner syndrome in this situation could be attributed to pig anatomy, we compared the anatomy of the CSC in pigs and humans, by using 10 infant (age, 1 to 3 wk) pig cadavers. The CSC and cranial cervical sympathetic ganglion (CCG) were dissected bilaterally under a surgical microscope. These structures were consistently within the carotid sheaths of the pigs. In contrast, the CSC and CCG are outside the carotid sheath in humans. Awareness of the anatomic variation of the CSC and CCG within the carotid sheath in the pig and the possibility of the same variation in humans may help surgeons to identify and preserve important structures while performing cervical surgery in pigs and humans. Furthermore, this knowledge can aid in the diagnosis and prognosis of schwannoma. Abbreviations: CCG, cranial cervical sympathetic ganglion; CSC, cervical sympathetic chain; NG, nodose ganglion. Horner syndrome is a classic clinical triad consisting of ipsilat- carotid artery, innervates the sphincter of the pupil and Müller eral eyelid ptosis (which is usually mild), pupil miosis, and facial muscle. The other branch follows the external carotid artery (A. anhydrosis (which may or may not be present, depending on the cervicalis externa) to supply other facial areas.19 location of the lesion).This syndrome results from cervical sym- Even though the CSC is located deep in the upper neck, the in- pathetic chain (CSC) paresis and can be congenital or acquired. cidence of iatrogenic Horner syndrome, stemming from surgery, Congenital causes of Horner syndrome account for less than 5% is reported to be 10% to 18.5%15 in humans. Surgeries that can of all cases. Acquired Horner syndrome can be caused by vasa cause iatrogenic Horner syndrome include thyroidectomy, coro- nervorum occlusion, tumor invasion, infection, or trauma or may nary bypass surgery, carotid endarterectomy, spine surgery, and present as an iatrogenic sequela of surgery.17 Horner syndrome cervical sympathectomy or thoracoscopic sympathicotomy.12,15 was characterized first in humans by Friedrich Horner in 1869.11 It Because of the relatively high incidence of iatrogenic Horner syn- has been previously identified in other mammals including guin- drome in patients, the information gained from animal models ea pigs, rats, mice, hamsters, and rabbits after superior cervical can be useful for understanding the specific iatrogenic causes in ganglionectomy.1,14 Only one case of iatrogenic Horner syndrome both animals and humans. Further, data on incidence in animal in pigs (Sus scrofa), which was caused by inflammation after ca- models may be useful in developing models for research of this rotid artery surgery, 10 has been reported previously. problem. In humans, the CSC ascending from thoracic cavity courses in In this study, we report a case of Horner syndrome occurring the prevertebral space posterior to the carotid sheath and anterior after carotid sheath surgery in a pig. In addition to documenting to the longus colli and longus capitis muscles. The CSC has 2 or the problem in the living animal, we performed 20 detailed post- 3 ganglia, with the superior cervical sympathetic ganglion be- mortem evaluations (including the piglet with Horner syndrome) ing the largest. The superior cervical sympathetic ganglion lies to assess the anatomic relationship among the CSC, cranial cervi- adjacent to the second and third cervical vertebrae. The internal cal sympathetic ganglion (CCG; ganglion cervical cranial), and carotid artery (A. cervicalis interna) and sheath lie anterior, and the carotid sheath. longus capitis is posterior.20 The superior cervical sympathetic ganglion has 2 main branches ascending to the face and cranium, Case Report each branch of which includes both postganglionic vasomotor The subject was one of a set of female pigs obtained from Tom and sudomotor fibers. One branch, which follows the internal Morris Farms (Reisterstown, MD) as part of a swallowing study. The pig was 18 d old and weighted 5.44 kg at the time of arrival at Received: 20 Jan 2011. Revision requested: 22 Feb 2011. Accepted: 08 May 2011. our vivarium. The pig was housed in a separate indoor cage and Departments of 1Physical Medicine and Rehabilitation and 2Otolaryngology-Head and environmental conditions were maintained as recommended in Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland. the Guide for the Care and Use of Laboratory Animals.9 It was fed 5 *Corresponding author. Email: [email protected] 453 Vol 61, No 5 Comparative Medicine October 2011 times daily with a milk replacement formula (Solustart pig milk replacer, Land O Lakes, St Paul, MN). Fresh water was provided ad libitum. Vital signs were tested daily by the veterinarian and indicated that the pig was healthy prior to surgery. All procedures on the living pig were approved by the Johns Hopkins IACUC (protocol number, SW07M14). For surgery, anesthesia was induced with inhaled isoflurane at 5% by face mask. The pig was intubated, and anesthesia was maintained with 3.5% to 5% isoflurane in 100% 2O as a carrier gas. The isoflurane level was adjusted to maintain anesthesia with stable hemodynamics. Heart rate, aortic blood pressure, respira- tory rate, and electrocardiographic data were continuously moni- tored throughout the procedure. Under sterile conditions, we performed the anterior approach to expose the cranial laryngeal nerve (N. laryngeus cranialis) in the lateral thyrohyoid membrane (membrana thyrohyoidea). We traced this nerve laterally to the ca- rotid sheath, which we opened. The right nodose ganglion (NG; ganglion distal) and its branch, the cranial laryngeal nerve, were exposed at the thyrohyoid membrane level within the sheath. During further dissection of the cervical vagus nerve (N. vagus cervicalis) caudally, we found another nerve medial and parallel to the cervical vagus nerve tracing between the cervical vagus nerve Figure 1. Horner syndrome in the pig. (A) Right side ptosis. (B) Left and internal jugular vein (V. jugulari interna) within the sheath. side normal eyelid. (C) Horner syndrome pig. (D) Right carotid sheath This nerve was injured inadvertently by the microforceps tips structures postmortem. Cervical sympathetic chain (CSC) was located during the phase of the dissection. Within 12 h after surgery, the medial and dorsal to the cervical vagus nerve (CV) and nodose ganglion pig presented with a drooping right upper eyelid. Ophthalmo- (NG). The start of the cranial laryngeal nerve (CLN) from the NG had logic examination revealed 3 mm of ptosis and 1 mm of miosis been ligated with a black suture during the surgery. CCA, common ca- on the right side (Figure 1). Analgesics and antibiotics were ad- rotid artery; CLA, cranial laryngeal artery; H, hyoid bone; TC, thyroid ministered after surgery to decrease the pain and infective risk. cartilage; TM, thyrohyoid membrane. We delivered buprenorphine (0.01 mg/kg IM twice daily) at 0800 and 1700 and meloxicam (0.4 mg/kg IM daily) and amoxicillin Results (20 mg/kg IM daily) at 1700. The pig showed no distress or pain The basic arrangement of the carotid sheath was constant in after surgery. all dissected pigs. In all 20 cases, the CSC lay within the carotid At 3 d after surgery, no recovery had occurred and the pig sheath. The CSC ascended between the cervical vagus nerve and was euthanized by intracardiac injection of sodium pentobarbi- the internal jugular vein, arriving at the CCG which was cranial, tal (greater than 200 mg/kg) under deep isoflurane anesthesia. dorsal, and medial to the NG. For all 20 specimens, the CCG was Postmortem evaluation confirmed that the nerve injured during located on the ventral and medial surface of the internal carotid surgery was the CSC caudal to the CCG within the carotid sheath. artery adjacent to the bifurcation of the common carotid artery On the basis of the physical examination and anatomic findings, (A. cervicalis profunda) at the level of the first and second cervi- the diagnosis of Horner syndrome was indicated and classified as cal vertebrae. The CCG was fusiform or flattened triangular in a preganglionic lesion. shape and reddish or gray in color. The CCG was larger than the NG. In all 20 dissections, the NG was reddish in color and ovoid Materials and Methods in shape. The CCG had 2 main branches traveling cranially: one Materials. The cadaver study included 10 pig specimens (age, with the internal carotid artery for innervations of the face, and 1 to 3 wk) obtained from Tom Morris Farms (Reisterstown, MD). the other traveling with the external carotid artery. Within the All dissections involved recently euthanized animals. All dissec- carotid sheath, from cranial to caudal direction between the skull tions within and related to the carotid sheath were done by using base and thyrohyoid membrane level, there were the CCG, the bi- microdissection surgical tools and a surgical microscope (OPMI furcation of the common carotid artery, and the NG. From ventral CS-NC, Carl Zeiss, Oberkochen, Germany). Photos were taken to dorsal direction, there were the common carotid artery and cra- with a digital camera (Coolpix 8700, Nikon, Melville, NY) con- nial laryngeal artery, the NG and cranial laryngeal nerve, the CSC nected to the surgical microscope.
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