1
|
Shimizu T, Kosaka H, Yamamoto Y. Cardiac Arrest during Temporary Clipping for Ruptured Internal Carotid Artery Aneurysm: A Case Report. Asian J Neurosurg 2024; 19:787-790. [PMID: 39606299 PMCID: PMC11588596 DOI: 10.1055/s-0044-1788974] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2024] Open
Abstract
Mechanical stimulation of the trigeminal nerve during craniofacial, skull base, or dental surgeries may cause bradycardia, hypotension, or cardiac arrest. This phenomenon is called trigeminal cardiac reflex (TCR). We encountered a rare case of a patient who experienced sinus arrest due to temporary clipping of the intracranial carotid artery during the clipping of a ruptured aneurysm. We discuss possible reasons for the occurrence of TCR in this case. A man in his 30s with no medical history presented with a sudden-onset headache. Computed tomography revealed a subarachnoid hemorrhage in the basal cistern and left Sylvian fissure. Angiography revealed a saccular aneurysm of the left internal carotid-anterior choroidal artery. A left frontotemporal craniotomy and dural incision were performed, followed by a trans-Sylvian approach. Cardiac arrest occurred twice during the temporary clipping of the intracranial carotid artery. After surgery, we performed a cardiac ultrasound echo and a 1-week Holter electrocardiogram. Neither showed abnormalities. No arrhythmia or cardiac events were observed over a one and half-year follow-up period. The cardiac arrest might have been triggered by the stimulation of the trigeminal nerve in the internal carotid artery. The repeated and anatomical features of this case suggest that TCR triggered cardiac arrest. The high probability that cardiac arrest was induced by trigeminal nerve stimulation should be considered during the temporary clipping of the internal carotid artery. However, the predisposing factors and exact underlying mechanisms for these arrhythmias remain unknown and require further investigation.
Collapse
Affiliation(s)
- Toshihiko Shimizu
- Department of Neurosurgery, Matsuyama Shimin Hospital, Matsuyama-city, Ehime, Japan
| | - Hiroshi Kosaka
- Department of Neurosurgery, Matsuyama Shimin Hospital, Matsuyama-city, Ehime, Japan
| | - Yuji Yamamoto
- Department of Neurosurgery, Matsuyama Shimin Hospital, Matsuyama-city, Ehime, Japan
| |
Collapse
|
2
|
Cho SY, Jang BH, Jeon HJ, Kim DJ. Repeated ventricular bigeminy by trigeminocardiac reflex despite atropine administration during superficial upper lip surgery: A case report. World J Clin Cases 2022; 10:11967-11973. [PMID: 36405277 PMCID: PMC9669879 DOI: 10.12998/wjcc.v10.i32.11967] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/02/2022] [Revised: 09/15/2022] [Accepted: 10/18/2022] [Indexed: 11/07/2022] Open
Abstract
BACKGROUND The trigeminocardiac reflex (TCR) is usually caused by an increased parasympathetic tone when pressure or traction is applied to the surrounding tissue of the trigeminal nerve. However, the inexperienced anesthesiologists may have challenges on the management of TCR patients.
CASE SUMMARY This is the case of an 18-year-old woman diagnosed with hemangioma of the upper lip. During the operation, about 1 h after surgery started, a constant 1:1 premature ventricular complex was detected, and blood pressure was decreased when approaching the deeper part with more strong traction for exposure of the part. Although the management of arrhythmias, such as lidocaine and atropine, was injected, arrhythmia induced by surgical stimulation could not be eliminated completely. As the traction repeated, bradycardia was also repeated, despite injecting additional atropine. Therefore, the anesthesiologist and the surgeon decided to perform the operation only to the extent that the vascular tissue was selectively removed only at the site without the reflex.
CONCLUSION With TCR, anesthesiologists should perform appropriate monitoring. In addition to proper drug administration, surgeons should be consulted to cope with stopping the surgery and setting the scope of the surgery even if the site is superficial.
Collapse
Affiliation(s)
- Su-Yeon Cho
- Department of Anesthesiology and Pain Medicine, Chosun University Hospital, Gwangju 61453, South Korea
| | - Bo-Hyun Jang
- Department of Anesthesiology and Pain Medicine, Chosun University Hospital, Gwangju 61453, South Korea
| | - Hye-Jin Jeon
- Department of Anesthesiology and Pain Medicine, Chosun University Hospital, Gwangju 61453, South Korea
| | - Dong-Joon Kim
- Department of Anesthesiology and Pain Medicine, Chosun University Hospital, Gwangju 61453, South Korea
| |
Collapse
|
3
|
Fowler SJ, Featherston M. Recurrent Atrial Tachyarrhythmia Triggered by Percutaneous Balloon Rhizotomy of the Trigeminal Nerve. Anaesth Intensive Care 2019; 32:410-2. [PMID: 15264739 DOI: 10.1177/0310057x0403200318] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022]
Abstract
Stimulation of sensory branches of the trigeminal nerve is known to cause sudden bradycardia (trigeminocardiac reflex). However we report a case where percutaneous balloon rhizotomy of the trigeminal ganglion provoked atrial tachyarrhythmias during two separate treatments. On both occasions the patient was treated with antiarrhythmic drugs and reverted to sinus rhythm within days. Our case demonstrates that surgery involving the trigeminal nerve may cause variable cardiovascular effects that are often clinically significant. Possible mechanisms and management of arrhythmias in this setting are discussed.
Collapse
Affiliation(s)
- S J Fowler
- Department of Anaesthesia, Wellington Hospital, Wellington, New Zealand
| | | |
Collapse
|
4
|
Abdel-Hameed Elsayed S, Hegab AF, Youssif Alkatsh SS. Does Surgical Release of TMJ Bony Ankylosis Increase the Risk of Trigeminocardiac Reflex? A Retrospective Cohort Study. J Oral Maxillofac Surg 2018; 77:391-397. [PMID: 30712536 DOI: 10.1016/j.joms.2018.06.006] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/26/2017] [Revised: 06/05/2018] [Accepted: 06/05/2018] [Indexed: 11/25/2022]
Abstract
PURPOSE The exact frequency of the trigeminocardiac (TGC) reflex in temporomandibular joint (TMJ) surgery is still controversial. The purpose of the present report was to estimate the frequency of and identify the risk factors for TGC reflex among patients undergoing operative management of TMJ ankyloses. PATIENTS AND METHODS A retrospective cohort study was conducted of patients who had undergone gap arthroplasty for TMJ ankyloses at Al-Azhar University Hospital, Cairo, Egypt, from 2001 to 2015. The predictor variables were patient demographic data (age and sex), ankylosis type, and surgery type. The outcome variable was the occurrence of the TGC reflex (yes vs no). The data analysis included descriptive statistics and χ2 tests to compare the categorical variables. Binary regression logistic model analysis was performed to identify the associated predictor variable. P values were considered statistically significant at ≤ .05. RESULTS The sample included 55 subjects. The mean ± standard deviation age of the patients was 21.3 ± 9.855 years, and 43.6% were males. The frequency of TGC reflex was 12.7%. The factors associated with an increased risk of TGC reflex were type IV bony ankylosis (P = .012) and the need for repeat surgery (P = .016.). A multivariable binary regression model analysis demonstrated that the recurrence of surgery was the most significant predictor factor affecting the frequency of the TGC reflex. The computed variance ranged from 13 to 25%. However, other variables, including age, gender, side, and ankylosis type, were not associated with reflex onset (odds ratio, 0.028; 95% confidence interval, 0.001 to 0.911; P = .044). CONCLUSIONS Recurrent ankylosis surgery carries a high risk of TGC reflex. Preoperative risk factor identification and close monitoring are crucial to prevent the occurrence of this reflex in susceptible patients. Future research projects should include more variables in the study.
Collapse
Affiliation(s)
- Shadia Abdel-Hameed Elsayed
- Assistant Professor, Department of Oral and Maxillofacial Surgery, Dental College and Hospital, Taibah University, Al-Madinah Al-Munawwarah, Saudi Arabia; and Associate Professor, Department of Oral and Maxillofacial Surgery, Faculty of Dental Medicine, Al-Azhar University (Girls Branch), Cairo, Egypt.
| | - Ayman F Hegab
- Clinical Associate Professor, Department of Oral and Maxillofacial Surgery, Faculty of Dental Medicine, Al-Azhar University, Cairo, Egypt
| | - Saeed Salem Youssif Alkatsh
- Lecturer, Department of Anaesthesia and Intensive Care, Faculty of Medicine for Boys, Al-Azhar University, Cairo, Egypt
| |
Collapse
|
5
|
Nghe MC, Godier A, Shaffii A, Leblanc I, Picard H, Blanc R, Lumbroso-Le Rouic L, Devys JM. Prospective analysis of serious cardiorespiratory events in children during ophthalmic artery chemotherapy for retinoblastoma under a deep standardized anesthesia. Paediatr Anaesth 2018; 28:120-126. [PMID: 29205669 DOI: 10.1111/pan.13294] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 10/31/2017] [Indexed: 11/29/2022]
Abstract
BACKGROUND AND OBJECTIVE Serious adverse cardiorespiratory events complicate super selective ophthalmic artery chemotherapy for retinoblastoma in anesthetized children. Their mechanism remains unclear but may be attributed to an autonomic nervous reflex induced by the catheter close to the ophthalmic artery. Inadequate depth of anesthesia during catheter stimulation might be an aggravating factor. Thus, we tested whether deep general anesthesia reduced the incidence of serious cardiorespiratory events. METHODS Children were prospectively included in this observational study. Standardized deep general anesthesia with sevoflurane, rocuronium, and sufentanil was administered. Sevoflurane MAC was kept between 1.5 and 1.7 and additional sufentanil administered. Serious cardiorespiratory event criteria were predefined and included arterial hypotension, bradycardia, and severe decrease in lung compliance. They were recorded and the factors influencing their occurrence were investigated. RESULTS One hundred fifteen procedures were performed on 32 children. The median MAC of sevoflurane was 1.5 and median BIS value was 44. Serious cardiorespiratory events occurred in 20% of procedures and were mainly severe decrease in lung compliance (83% of events). All of them required active treatment. One procedure was aborted due to cardiorespiratory compromise and required an epinephrine infusion. All severe decreases in lung compliance occurred within 2 minutes after catheter insertion in the ophthalmic artery. No recorded demographic and endovascular characteristics were associated with serious cardiorespiratory events. CONCLUSION Serious cardiorespiratory events occur commonly during super selective ophthalmic artery chemotherapy. Standardized deep anesthesia with analgesia did not appear to be protective. No predictive factors were identified, but these events systematically arose within 2 minutes after ophthalmic artery catheter insertion. Anesthetists and neuroradiologists should be prepared to manage these serious complications and parents should be informed of the risks.
Collapse
Affiliation(s)
- Marie-Claire Nghe
- Department of Anesthesiology and Intensive Care, Foundation Adolphe de Rothschild, Paris, France
| | - Anne Godier
- Department of Anesthesiology and Intensive Care, Foundation Adolphe de Rothschild, Paris, France.,INSERM UMR-S1140, Paris Descartes University, Paris, France
| | - Anoushée Shaffii
- Department of Anesthesiology and Intensive Care, Foundation Adolphe de Rothschild, Paris, France
| | - Isabelle Leblanc
- Department of Anesthesiology and Intensive Care, Foundation Adolphe de Rothschild, Paris, France
| | - Hervé Picard
- Clinical Research Unit, Foundation Adolphe de Rothschild, Paris, France
| | - Raphaël Blanc
- Department of Interventional Neuroradiology, Foundation Adolphe de Rothschild, Paris, France
| | | | - Jean-Michel Devys
- Department of Anesthesiology and Intensive Care, Foundation Adolphe de Rothschild, Paris, France
| |
Collapse
|
6
|
Sandu N, Chowdhury T, Meuwly C, Schaller B. Trigeminocardiac reflex in cerebrovascular surgery: a review and an attempt of a predictive analysis. Expert Rev Cardiovasc Ther 2017; 15:203-209. [DOI: 10.1080/14779072.2017.1286983] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 10/20/2022]
Affiliation(s)
- Nora Sandu
- Department of Research, University of Southampton, Southampton, UK
| | - Tumul Chowdhury
- Department of Anesthesiology and Perioperative Medicine, University of Manitoba (UOM)/Winnipeg Regional Health Authority (WRHA), Winnipeg, Manitoba, Canada
| | | | - Bernhard Schaller
- Department of Research, University of Southampton, Southampton, UK
- Department of Pathology, University of Buenos Aires, Buenos Aires, Argentina
| |
Collapse
|
7
|
Meuwly C, Golanov E, Chowdhury T, Erne P, Schaller B. Trigeminal cardiac reflex: new thinking model about the definition based on a literature review. Medicine (Baltimore) 2015; 94:e484. [PMID: 25654391 PMCID: PMC4602726 DOI: 10.1097/md.0000000000000484] [Citation(s) in RCA: 95] [Impact Index Per Article: 9.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/02/2022] Open
Abstract
Trigeminocardiac reflex (TCR) is a brainstem reflex that manifests as sudden onset of hemodynamic perturbation in blood pressure (MABP) and heart rate (HR), as apnea and as gastric hypermotility during stimulation of any branches of the trigeminal nerve. The molecular and clinical knowledge about the TCR is in a constant growth since 1999, what implies a current need of a review about its definition in this changing context. Relevant literature was identified through searching in PubMed (MEDLINE) and Google scholar database for the terms TCR, oculocardiac reflex, diving reflex, vasovagale response. The definition of the TCR varies in clinical as well as in research studies. The main difference applies the required change of MABP and sometimes also HR, which most varies between 10% and 20%. Due to this definition problem, we defined, related to actual literature, 2 major (plausibility, reversibility) and 2 minor criteria (repetition, prevention) for a more proper identification of the TCR in a clinical or research setting. Latest research implies that there is a need for a more extended classification with 2 additional subgroups, considering also the diving reflex and the brainstem reflex. In this review, we highlighted criteria for proper definition and classification of the TCR in the light of increased knowledge and present a thinking model to overcome this complexity. Further we separately discussed the role of HR and MABP and their variation in this context. As another subtopic we gave attention to is the chronic TCR; a variant that is rarely seen in clinical medicine.
Collapse
Affiliation(s)
- C Meuwly
- From the University of Basel, Switzerland (CM); The Houston Methodist Research Institute, Houston, Texas, USA (EG); Department of Anesthesia and Perioperative Medicine. University of Manitoba, Winnipeg, Canada (TC); Cardiology, St Anna Clinic, Luzern, Switzerland and University of Basel, Switzerland (PE); Department of Research, University of Southampton, United Kingdom (BS); and Academic Editor, Medicine (BS)
| | | | | | | | | |
Collapse
|
8
|
Rossi R, Lodise M, Lancia M, Bacci M, De-Giorgio F, Cascini F. Trigemino-Cardiac Reflex as Lethal Mechanism in a Suicidal Fire Death Case. J Forensic Sci 2014; 59:833-5. [DOI: 10.1111/1556-4029.12408] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/20/2012] [Revised: 02/04/2013] [Accepted: 04/21/2013] [Indexed: 11/28/2022]
Affiliation(s)
- Riccardo Rossi
- Institute of Legal Medicine; Catholic University of the Sacred Heart; Largo Francesco Vito, 1 00168 Rome Italy
| | - Maria Lodise
- Institute of Legal Medicine; Catholic University of the Sacred Heart; Largo Francesco Vito, 1 00168 Rome Italy
| | - Massimo Lancia
- Section of Legal Medicine; University of Perugia; via del Giochetto, snc 06126 Perugia Italy
| | - Mauro Bacci
- Section of Legal Medicine; University of Perugia; via del Giochetto, snc 06126 Perugia Italy
| | - Fabio De-Giorgio
- Institute of Legal Medicine; Catholic University of the Sacred Heart; Largo Francesco Vito, 1 00168 Rome Italy
| | - Fidelia Cascini
- Institute of Legal Medicine; Catholic University of the Sacred Heart; Largo Francesco Vito, 1 00168 Rome Italy
| |
Collapse
|
9
|
Phillips TJ, McGuirk SP, Chahal HK, Kingston J, Robertson F, Brew S, Roebuck D, Hungerford JL, Herod J. Autonomic cardio-respiratory reflex reactions and superselective ophthalmic arterial chemotherapy for retinoblastoma. Paediatr Anaesth 2013; 23:940-5. [PMID: 23668238 DOI: 10.1111/pan.12162] [Citation(s) in RCA: 25] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 03/03/2013] [Indexed: 01/22/2023]
Abstract
OBJECTIVE To describe our experience with superselective ophthalmic artery chemotherapy (SOAC) in retinoblastoma and to report the serious adverse cardio-respiratory reactions we have observed. METHODS SOAC was performed using a standardized protocol for general anesthesia, ophthalmic artery catheterization, and pulsed infusion of melphalan. Adverse reactions were defined as those in which the patient required active treatment to maintain cardio-respiratory stability. RESULTS Between December 2008 and May 2012, 54 eyes in 52 patients were treated. 143 catheterization procedures were performed, with a technical success rate of 93% (n = 133). There were no deaths or major complications. Adverse cardio-respiratory reactions developed during 35 procedures (24%; 95% CI, 18-32%). All reactions occurred during second or subsequent catheterization procedures (39%; 95% CI, .29-49%) and were characterized by hypoxia, reduced lung compliance, systemic hypotension and bradycardia. Adverse events were successfully treated in all patients. One procedure was abandoned due to prolonged hemodynamic instability. CONCLUSION Adverse cardio-respiratory reactions are commonly observed in SOAC for retinoblastoma. We believe that the adverse clinical signs represent an autonomic reflex response, akin to the trigemino-cardiac or oculo-respiratory reflexes, and all patients should be considered at-risk. Reactions occur only during second or subsequent procedures and can be life-threatening. The routine use of intravenous atropine does not seem to have altered the incidence or severity of these reactions. Anesthetists and interventional neuroradiologists involved in SOAC must be vigilant to ensure adverse reactions, when they develop, are treated quickly and effectively.
Collapse
Affiliation(s)
- Trudie J Phillips
- Department of Anaesthesia, Great Ormond Street Hospital For Children NHS Foundation Trust, London, UK
| | | | | | | | | | | | | | | | | |
Collapse
|
10
|
Abstract
Heart rate, blood pressure, and vascular tone, as well as ventilator drive, respiratory rate, and breathing pattern, are, at least in part, under the control of specific reflexes. These reflexes are mediated by a complex network of baroreceptors and chemoreceptors in the arterial system of the carotids, aorta, and left heart, including receptors in the left atrium, the ventricle, and the coronary arteries; irritants in the upper airways and stretch receptors in the lower airways; juxtacapillary-located nonmyelinated fibers in the alveoli and in the bronchial arterial system; and muscle spindles that evoke changes in the membrane potential upon alteration of sarcolemmal tension. Some of these reflexes, usually named after the first individual to describe them, have spread as eponyms into propaedeutic education and clinical work. Because these euphonic eponyms are enigmatic to most clinicians today, this article is intended to provide a short overview of these reflexes, including the historical context of their describers. As evidenced by their clinical implications, the eponyms discussed are revealed to be more than curiosities taught during undergraduate medical education.
Collapse
Affiliation(s)
- Mattia Arrigo
- Cardiosurgical Intensive Care Unit, University Hospital Zurich, Zurich, Switzerland.
| | | |
Collapse
|
11
|
Bhargava D, Thomas S, Chakravorty N, Dutt A. Trigeminocardiac Reflex: A Reappraisal with Relevance to Maxillofacial Surgery. J Maxillofac Oral Surg 2013. [PMID: 26224999 DOI: 10.1007/s12663-013-0541-4] [Citation(s) in RCA: 20] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/07/2023] Open
Abstract
PURPOSE The purpose of this paper was to undertake a review of literature on trigeminocardiac reflex in oral and maxillofacial online data-base and discuss the pathophysiology, risk factor assessment, presentation of the reflex, prevention, management with emphasis on the role of the attending anaesthetist and the maxillofacial surgeon. MATERIALS AND METHODS The available literature relevant to oral and maxillofacial surgery in online data-base of the United States National Library of Medicine: Pubmed (http://www.ncbi.nlm.nih.gov/pubmed/) was searched. The inclusion criterion was to review published clinical papers, abstracts and evidence based reviews on trigeminocardiac reflex relevant to oral and maxillofacial surgery. RESULTS Sixty-five articles were found with the search term "trigeminocardiac reflex" in the literature searched. Eighteen articles met the inclusion criteria for this study. The relevant data was extracted, tabulated and reviewed to draw evidence based conclusions for the management of trigeminocardiac reflex. CONCLUSIONS Conclusions were drawn and discussed based on the reviewed maxillofacial literature with emphasis on the anaesthetist's and the surgeon's role in the management of this detrimental event in maxillofacial surgical practice.
Collapse
Affiliation(s)
- Darpan Bhargava
- Department of Oral and Maxillofacial Surgery, Peoples College of Dental Sciences and Research Center, Peoples University, Bhanpur, Bhopal, M.P. India
| | - Shaji Thomas
- Department of Oral and Maxillofacial Surgery, Peoples College of Dental Sciences and Research Center, Peoples University, Bhanpur, Bhopal, M.P. India
| | - Nupur Chakravorty
- Department of Anesthesiology, L.N Medical College and Research Center and J.K Hospital, J.K Town, Sarvdharm C-Sector, Kolar Road, Bhopal, M.P. India
| | - Ashutosh Dutt
- Department of Oral and Maxillofacial Surgery, Peoples College of Dental Sciences and Research Center, Peoples University, Bhanpur, Bhopal, M.P. India
| |
Collapse
|
12
|
Trigeminocardiac reflex: a predictable event with unpredictable aspects. World Neurosurg 2012; 76:407-8. [PMID: 22152566 DOI: 10.1016/j.wneu.2011.03.005] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/24/2011] [Accepted: 03/02/2011] [Indexed: 11/22/2022]
|
13
|
Yorgancilar E, Gun R, Yildirim M, Bakir S, Akkus Z, Topcu I. Determination of trigeminocardiac reflex during rhinoplasty. Int J Oral Maxillofac Surg 2012; 41:389-93. [PMID: 22240287 DOI: 10.1016/j.ijom.2011.12.025] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/07/2011] [Revised: 10/14/2011] [Accepted: 12/09/2011] [Indexed: 11/19/2022]
Abstract
In most rhinoplasty procedures, osteotomies are usually required. The osteotomy areas are innervated by sensory branches of the trigeminal nerve. The trigeminocardiac reflex (TCR) is clinically defined as the sudden onset of parasympathetic activity during stimulation of the trigeminal nerve. When an osteotomy is performed or external pressure is applied over the nasal bone, the infraorbital nerve may send signals via this nerve. The aim of this prospective study is to determine the blood pressure changes and occurrence of TCR during rhinoplasty. one hundred and eight patients were enrolled into the study. Lidocaine and adrenaline combination (LAC) was injected only into the left lateral osteotomy sites. All patients underwent median, right-side, then left-side lateral osteotomies and nasal pyramid infracture. The haemodynamic changes were recorded. A 10% or more decrease in the heart rate from baseline was considered a TCR. TCR was detected in nine patients following lateral osteotomies and nasal pyramid infracture procedures (8.3%). The authors determined that LAC injection prior to osteotomy did not prevent TCR. Manipulation at or near the infraorbital nerve during rhinoplasty may cause TCR, even if local anaesthetic infiltration is used.
Collapse
Affiliation(s)
- E Yorgancilar
- Department of Otorhinolaryngology and Head and Neck Surgery, Dicle University School of Medicine, Diyarbakir, Turkey.
| | | | | | | | | | | |
Collapse
|
14
|
Vasudev S, Reddy KS. Trigemino-cardiac reflex during orbital floor reconstruction: a case report and review. J Maxillofac Oral Surg 2011; 14:32-7. [PMID: 25861181 DOI: 10.1007/s12663-011-0271-4] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/14/2010] [Accepted: 08/02/2011] [Indexed: 11/24/2022] Open
Abstract
Trigemino-cardiac reflex is occurrence of hypotension and bradycardia upon surgical manipulation of areas supplied by the trigeminal nerve, and has been reported during craniofacial maxillofacial and ocular surgeries. Communication between the anaesthetic and surgical team is essential, and cessation of the precipitating stimulus is the first and most important therapeutic step. We report a case of immediate, reproducible, and reflexive response of Bradycardia and dysrhythmia upon manipulation of orbital fracture during orbital floor reconstruction in a 65-year-old man. Upon recognition of the reproducible relationship between falcine stimulation and increased vagal tone, the patient was given atropine in an effort to block cholinergic hyperactivity. After atropine administration, no further dysrhythmias occurred and surgery was carried uneventfully.
Collapse
Affiliation(s)
- Sunil Vasudev
- Department of Oral & Maxillofacial Surgery, DAPMRV Dental College & Hospital, JP Nagar 1st Phase, Bangalore, India
| | - K Sudhakara Reddy
- Department of Oral & Maxillofacial Surgery, Sri Rajiv Gandhi College of Dental Sciences, Bangalore, India
| |
Collapse
|
15
|
Trigeminocardiac reflex, bilateral sagittal split ramus osteotomy, Gow-Gates block: a randomized controlled clinical trial. J Oral Maxillofac Surg 2011; 69:2316-20. [PMID: 21511380 DOI: 10.1016/j.joms.2011.01.026] [Citation(s) in RCA: 21] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/21/2010] [Revised: 01/15/2011] [Accepted: 01/20/2011] [Indexed: 10/18/2022]
Abstract
PURPOSE The behavior of trigeminocardiac reflex (TCR) during maxillofacial surgeries has not yet been sufficiently studied and knowledge of its behavior is limited to some case reports. The present study aimed to assess the occurrence of TCR in bilateral sagittal split ramus osteotomy and to determine the possible effect of Gow-Gates block on its incidence. MATERIALS AND METHODS Twenty candidates for bilateral sagittal split ramus osteotomy (included were American Society of Anesthesiologists I Class III patients with a prognathism of 3 to 5 mm) were given routine general anesthesia after at least 12 hours of fasting. All patients received Gow-Gates mandibular nerve block on 1 random side (case ramus; the other side was used as the control) after induction of general anesthesia before surgery. Pulse rate was recorded at baseline, soft tissue cutting, bone cutting, sagittal splitting, setback manipulation, and recovery. Mean pulse rate values were compared statistically using t test for the 2 sides in patients. RESULTS No statistically significant differences were found between the blocked and control sides except during ramus sagittal splitting and setback manipulation (P < .0001), when a significantly decreased pulse rate was recorded for the control ramus compared with the blocked ramus. CONCLUSIONS The present study provides further evidence for the complex neurophysiologic mechanism and probable prevention of peripheral TCR. The results of the present study should be further validated through future studies but already provide strong evidence that peripheral and central TCR may act differently based on slightly different pathways.
Collapse
|
16
|
Ong C, Ong M, Le K, Power M, Wang L, Lam D, Parkinson R, Wenderoth J. The trigeminocardiac reflex in Onyx embolisation of intracranial dural arteriovenous fistula. J Clin Neurosci 2010; 17:1267-70. [DOI: 10.1016/j.jocn.2010.01.041] [Citation(s) in RCA: 12] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2009] [Accepted: 01/05/2010] [Indexed: 10/19/2022]
|
17
|
Lv X, Li Y, Jiang C, Wu Z. The incidence of trigeminocardiac reflex in endovascular treatment of dural arteriovenous fistula with onyx. Interv Neuroradiol 2010; 16:59-63. [PMID: 20377980 PMCID: PMC3277960 DOI: 10.1177/159101991001600107] [Citation(s) in RCA: 40] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/29/2009] [Accepted: 02/20/2010] [Indexed: 02/05/2023] Open
Abstract
This paper reports the incidence of tri-geminocardiac reflex (TCR) in endovascular treatment of dural arteriovenous fistulas (DAVFs) with Onyx. The consecutive case histories of 45 patients with DAVFs, treated with Onyx transarterially and transvenously, from February 2005 to February 2008 at Beijing Tiantan Hospital, China, were retrospectively reviewed. The time period was limited as the anesthetic and intravascular procedure was performed under the same standardized anesthetic protocol and by the same team. The TCR rate was subsequently calculated. Of the 45 patients, five showed evidence of TCR during transarterial Onyx injection and transvenous DMSO injection. Their HR fell 50% during intravascular procedures compared with levels immediately before the stimulus. However, blood pressure values were stable in all cases. The TCR rate for all patients was 11.1% (95% CI, 4 to 24%), 7.7% (95% CI, 2 to 21%) in patients treated intraarterially and 33.3% (4 to 78%) in patients treated intravenously. Once HR has fallen, intravenous atropine is indicated to block the depressor response and prevention further TCR episodes. TCR may occur due to chemical stimulus of DMSO and Onyx cast formation under a standardized anesthetic protocol and should be blunted by atropine.
Collapse
Affiliation(s)
- X Lv
- Beijing Neurosurgical Institute, Beijing Tiantan Hospital, Capital Medical University; Beijing, China.
| | | | | | | |
Collapse
|
18
|
Bohluli B, Ashtiani AK, Khayampoor A, Sadr-Eshkevari P. Trigeminocardiac reflex: A MaxFax literature review. ACTA ACUST UNITED AC 2009; 108:184-8. [DOI: 10.1016/j.tripleo.2009.03.050] [Citation(s) in RCA: 38] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/01/2009] [Revised: 03/10/2009] [Accepted: 03/20/2009] [Indexed: 11/25/2022]
Affiliation(s)
- Behnam Bohluli
- Oral and Maxillofacial Surgery, School of Dental Medicine, Azad University of Tehran, Tehran, Iran
| | | | | | | |
Collapse
|
19
|
Meng Q, Yang Y, Zhou M, Li X. Trigemino-cardiac reflex: the trigeminal depressor responses during skull base surgery. Clin Neurol Neurosurg 2008; 110:662-6. [PMID: 18514393 DOI: 10.1016/j.clineuro.2008.03.018] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/07/2007] [Revised: 03/16/2008] [Accepted: 03/26/2008] [Indexed: 10/22/2022]
Abstract
OBJECTIVE To observe and analyze the occurrence and management of the trigemino-cardiac reflex (TCR) defined as the phenomenon of abrupt drops in heart rate (HR) and blood pressure during skull base surgery. METHOD One hundred patients underwent skull base surgery for various lesions were recruited and great attention was paid to heart rate and blood pressure throughout the surgical procedure to screen intraoperative TCR. RESULT Twelve patients had TCR intro-operatively, all patients showed abrupt drops in HR of 38% from a mean of 78 beats/min to a mean of 49 beats/min, mean arterial blood pressure (MABP) decreased 33% from a mean of 93 mmHg to a mean of 60 mmHg, respectively. TCR was resolved spontaneously in eight patients, but had to be offset by intraoperative administration of relatively higher dose atropine in another four patients. CONCLUSION (1) Manipulation at or near the trigeminal nerve during the skull base surgery may cause TCR, even if premedication with anticholinergic drug is used; (2) cessation of irritation from surgical manipulation to disrupt the reflex is the most important step to offset TCR; (3) continuous, especially repeated TCR in some rare cases occasionally necessitates the administration of high dose atropine.
Collapse
Affiliation(s)
- Qingli Meng
- Department of Neurosurgery, Qilu Hospital, Shandong University, Jinan, Shandong, PR China
| | | | | | | |
Collapse
|
20
|
Kim JY, Park JS, Baek DJ, Lee SI, Kim KT, Choe WJ, Kim JW. Asystole via Trigeminocardiac Reflex during Skin Flap Elevation in a Patient Undergoing Craniotomy for Cerebral Aneurysm Clipping - A case report -. Korean J Anesthesiol 2008. [DOI: 10.4097/kjae.2008.54.2.220] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/10/2022] Open
Affiliation(s)
- Ji Yeon Kim
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| | - Jang Su Park
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| | - Dong Jin Baek
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| | - Sang Il Lee
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| | - Kyung Tae Kim
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| | - Won Joo Choe
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| | - Jung Won Kim
- Department of Anesthesiology and Pain Medicine, Ilsan Paik Hospital, Inje University Collge of Medicine, Goyang, Korea
| |
Collapse
|
21
|
|
22
|
Schaller BJ, Weigel D, Filis A, Buchfelder M. Trigemino-cardiac reflex during transsphenoidal surgery for pituitary adenomas: Methodological description of a prospective skull base study protocol. Brain Res 2007; 1149:69-75. [PMID: 17428450 DOI: 10.1016/j.brainres.2005.08.060] [Citation(s) in RCA: 24] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/12/2005] [Revised: 08/22/2005] [Accepted: 08/31/2005] [Indexed: 12/21/2022]
Abstract
A systematic clinical neuroscience protocol is described for the use to examine the trigemino-cardiac reflex (TCR) response in humans. Target neurosurgical conditions are operations that require manipulations around the peripheral and central part of the trigeminal nerve and its branches, e.g. the cerebellopontine angle or the sellar region. To assess the hemodynamic and cardiac responses of patients after TCR initiation, anesthetic monitoring has been applied. The TCR is defined as a drop of more than 20% of the heart rate and the mean arterial blood pressure compared with the baseline values before the stimulus and coinciding with the surgical manipulation at or around any branches of the trigeminal nerve. By help of illustrative cases, we present for the first time preliminary results regarding the differentiation of the TCR in a central and a peripheral induction during transsphenoidal surgery of pituitary adenomas. Based on these results, we can conclude that we have developed a battery of preoperative examination procedures based on event-related diagnostics that was useful to differentiate different subgroups of TCR during transsphenoidal surgery. The presented protocol can be performed directly pre-, intra- and postoperatively and applied for assessment of TCR even in patients with known risk factors.
Collapse
Affiliation(s)
- B J Schaller
- Department of Neurosurgery, University of Göttingen, Germany.
| | | | | | | |
Collapse
|
23
|
|
24
|
Schaller B. Trigemino-cardiac reflex during transsphenoidal surgery for pituitary adenomas. Clin Neurol Neurosurg 2005; 107:468-74. [PMID: 16202819 DOI: 10.1016/j.clineuro.2004.12.004] [Citation(s) in RCA: 71] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2004] [Revised: 11/29/2004] [Accepted: 12/02/2004] [Indexed: 11/30/2022]
Abstract
BACKGROUND The trigemino-cardiac reflex (TCR) is a well-recognized phenomenon consisting of bradycardia, arterial hypotension, apnea, and gastric hypermotility. It occurs during ocular surgery or other manipulations around the orbit and can also be elicited by stimulation of the central part of the trigeminal nerve during surgery for processes of the cerebellopontine angle. The present retrospective study was conducted to determine if TCR occurs during transsphenoidal surgery in the same way. METHODS TCR was defined as a drop in mean arterial blood pressure (MABP) and the heart rate (HR) of more than 20% to the baseline values before the stimulus and coinciding with manipulation of the trigeminal nerve. Pre-, intra-, and postoperative HR and MABP were retrospectively reviewed in 117 patients who underwent resection of pituitary adenomas near the trigeminal nerve at the cavernous sinus in the supine position. Tumor invasiveness was classified according to the modified Hardy criteria. RESULTS Of the 117 patients with immunohistochemically and/or electromicroscopically proven pituitary adenoma, 12 (10%) patients demonstrated intraoperative evidence of TCR according to the strict inclusion criteria. In these 12 patients, the HR and MABP decreased by a mean of 43 and 54%, respectively, from the preoperative mean levels during microsurgical manipulation near the cavernous sinus and returned to physiological levels within 10 min after cessation of this surgical maneuver. The percentage of invasive adenomas (grade III-IV) was significantly higher in the TCR subgroup than in the non-TCR subgroup (83% versus 22%). CONCLUSION The present results give evidence for the first time that TCR may occur during transsphenoidal surgery in the supine position for resection of pituitary adenomas near the cavernous sinus, leading to a significant decrease in HR and MABP under a standardized anesthetic protocol.
Collapse
Affiliation(s)
- Bernhard Schaller
- Department of Neuroscience, Karolinska Institute, Retzius väg 8, S-17177 Stockholm, Sweden
| |
Collapse
|
25
|
Bauer DF, Youkilis A, Schenck C, Turner CR, Thompson BG. The falcine trigeminocardiac reflex: case report and review of the literature. ACTA ACUST UNITED AC 2005; 63:143-8. [PMID: 15680656 DOI: 10.1016/j.surneu.2004.03.022] [Citation(s) in RCA: 47] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/20/2003] [Accepted: 03/25/2004] [Indexed: 10/25/2022]
Abstract
BACKGROUND Trigeminocardiac reflex (TCR), the reproducible hypotension and bradycardia upon stimulation of the trigeminal nerve, has been reported during craniofacial surgery and during surgery within the cerebellopontine angle, petrosal sinus, orbit, and trigeminal ganglion. Whereas the falx cerebri is known to be innervated by the nervus tentorii, a recurrent branch of V1, there have been no reports to date of this response upon mechanical stimulation of the falx. CASE DESCRIPTION We report a case of immediate, reproducible, and reflexive response of asystole upon stimulation of the falx cerebri during operative resection of a parafalcine meningioma in a 53-year-old woman. Upon recognition of the reproducible relationship between falcine stimulation and increased vagal tone, the patient was given glycopyrrolate in an effort to block cholinergic hyperactivity. After glycopyrrolate was given, no further dysrhythmias occurred. CONCLUSION In this patient, mechanical stimulation of the falx likely resulted in the hyperactivity of the trigeminal ganglion, thereby triggering TCR. The dorsal region of the spinal trigeminal tract includes neurons from hypoglossal and vagus nerves, and projections have been seen between the vagus and trigeminal nuclei. The vagus provides parasympathetic innervation to the heart, vascular smooth muscle, and abdominal viscera. Vagal stimulation via these connections after trigeminal nerve activation likely accounts for the reflexive response of asystole seen in this patient. This is confirmed by the observation that the reflex was inhibited by the anticholinergic effects of glycopyrrolate. Awareness of TCR allows for early detection and appropriate treatment.
Collapse
Affiliation(s)
- David F Bauer
- University of Michigan Medical School, Ann Arbor, MI 48109, USA
| | | | | | | | | |
Collapse
|
26
|
Cha ST, Eby JB, Katzen JT, Shahinian HK. Trigeminocardiac reflex: a unique case of recurrent asystole during bilateral trigeminal sensory root rhizotomy. J Craniomaxillofac Surg 2002; 30:108-11. [PMID: 12069514 DOI: 10.1054/jcms.2001.0264] [Citation(s) in RCA: 51] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022] Open
Abstract
BACKGROUND The trigeminocardiac reflex is the sudden-onset of dysrhythmia and hypotension during manipulation of any of the branches of the trigeminal nerve. The trigeminal nerve and cardioinhibitory vagus nerve constitute the afferent and efferent pathways in the reflex arc. The trigeminocardiac reflex has been reported to occur during craniofacial surgery, balloon-compression rhizolysis of the trigeminal ganglion, and tumour resection in the cerebellopontine angle. PATIENT & METHOD A 2-year-old male patient with haemangioma near the sella turcica underwent rhizotomies of both sides of the dorsal sensory roots, of the trigeminal nerves for palliation of intractable trigeminal pain. RESULTS In this report, we experienced two unexpected episodes of asystole after transection of the sensory roots of the trigeminal nerves. CONCLUSION Sectioning of the intracranial dorsal sensory root of the trigeminal nerve provides clear evidence of the central role of the trigeminal nerve as the afferent pathway of the trigeminocardiac reflex arc.
Collapse
Affiliation(s)
- S T Cha
- Division of Skull Base Surgery, Los Angeles, CA 90048, USA
| | | | | | | |
Collapse
|
27
|
Schaller B, Probst R, Strebel S, Gratzl O. Trigeminocardiac reflex during surgery in the cerebellopontine angle. J Neurosurg 1999; 90:215-20. [PMID: 9950491 DOI: 10.3171/jns.1999.90.2.0215] [Citation(s) in RCA: 171] [Impact Index Per Article: 6.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/06/2022]
Abstract
OBJECT In different experimental studies authors have analyzed the autonomic responses elicited by the electrical, mechanical, or chemical stimulation of the trigeminal nerve system. The trigeminocardiac reflex (TCR) is a well-recognized phenomenon that consists of bradycardia, arterial hypotension, apnea, and gastric hypermotility. It occurs during ocular surgery and during other manipulations in and around the orbit. Thus far, it has not been shown that central stimulation of the trigeminal nerve can also cause this reflex. METHODS The TCR was defined as clinical hypotension with a drop in mean arterial blood pressure (MABP) of more than 20% and bradycardia lower than 60 beats/minute. Pre-, intra-, and postoperative heart rate (HR) and MABP were reviewed retrospectively in 125 patients who underwent surgery for tumors of the cerebellopontine angle (CPA), and they were divided into two groups on the basis of the occurrence of the TCR during surgery. Of the 125 patients, 14 (11%) showed evidence of the TCR during dissection of the tumor near the trigeminal nerve at the brainstem. Their HRs fell 38% and their MABPs fell 48% during operative procedures as compared with preoperative levels. After cessation of manipulation, the HRs and the MABPs returned to preoperative levels. Risk factors for the occurrence of the TCR were compared with results from the literature. CONCLUSIONS The authors' results show the possibility of occurrence of a TCR during manipulation of the central part of the trigeminal nerve when performing surgery in the CPA.
Collapse
Affiliation(s)
- B Schaller
- Department of Neurological Surgery, University Hospitals Basel, Switzerland
| | | | | | | |
Collapse
|
28
|
Schall B, Probst R, Strebel S, Fuhr P, Gratzl O. Trigeminocardiac reflex during surgery in the cerebellopontine angle. Neurosurg Focus 1998. [DOI: 10.3171/foc.1998.5.3.10] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/06/2022]
Abstract
In different experimental studies authors have analyzed the autonomic responses elicited by the electrical, mechanical, or chemical stimulation of the trigeminal nerve system. The trigeminocardiac reflex (TCR) is a well-recognized phenomenon that consists of bradycardia, arterial hypotension, apnea, and gastric hypermotility. It occurs during ocular surgery and during other manipulations in and around the orbit. Thus far, it has not been shown that central stimulation of the trigeminal nerve can also cause this reflex.
The TCR was defined as clinical hypotension with a drop in mean arterial blood pressure (MABP) of more than 20% and bradycardia lower than 60 beats/minute. Pre-, intra-, and postoperative heart rate (HR) and blood pressure were reviewed retrospectively in 125 patients who underwent surgery for tumors of the cerebellopontine angle (CPA), and they were divided into a TCR group and a non-TCR group. Of the 125 patients, 14 (11%) showed evidence of TCR during dissection of the tumor near the trigeminal nerve at the brainstem. Their HR fell 38% and their MABP fell 48% during operative procedures as compared with preoperative levels. After cessation of manipulation, the HR and the MABP returned to preoperative levels. Risk factors for the occurrence of TCR were compared with results from the literature.
The authors' results show the possibility of occurrence of a TCR during manipulation of the central part of the trigeminal nerve when performing surgery in the CPA.
Collapse
|
29
|
Blanc VF. Atropine and succinylcholine: beliefs and controversies in paediatric anaesthesia. Can J Anaesth 1995; 42:1-7. [PMID: 7889577 DOI: 10.1007/bf03010562] [Citation(s) in RCA: 16] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/27/2023] Open
|
30
|
Carrero EJ, Chabás E, Nalda MA. The trigeminal-cardiac reflex in paediatric surgery. Anaesthesia 1994; 49:741. [PMID: 7943726 DOI: 10.1111/j.1365-2044.1994.tb04430.x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/28/2023]
|
31
|
|