History of the Trigeminocardiac Reflex

An Odyssey

Gelarah Vahdati1, Arezoo Rajaee2, Seyed Aliakbar Vahdati3 and Pooyan Sadr-Eshkevari4,    1Excel Diagnostics and Nuclear Oncology Center, Houston, TX, USA,    2Department of Maternal Fetal Medicine, Obstetrics and Gynecology, University of California, Los Angeles (UCLA), CA, USA,    3Private Practice Dentist, CA, USA,    4Professional Program for International Dentists, University of California, Los Angeles (UCLA), CA, USA

Rome ne s’est pas faite en un jour,1 and neither was our current understanding of the trigeminocardiac reflex. This understanding is based on a series of meticulous observations and experiments over the past two centuries, but predominantly in the last two decades. The journey extends from the initial explanation of the respiration reflexes in the mid-nineteenth century to the clinical and physiological definitions of the phenomenon in the twenty-first century. The history of the trigeminocardiac reflex sheds light on the importance of this phenomenon for everyone involved in the treatment of patients by means of neurosurgery, craniomaxillofacial surgery, facial plastic surgery, and ophthalmology. This chapter presents an in-depth treatment of the history of the trigeminocardiac reflex.

Keywords

History; oculocardiac reflex; trigeminal nerve; trigeminocardiac reflex; trigeminal ganglion

Outline

The trigeminocardiac reflex (TCR) is described as the sudden development of cardiac arrhythmia, including cardiac arrest, arterial hypotension, apnea, and gastric hypermobility. Ewald Hering’s laboratory at the Emperor Joseph’s Military Academy in Vienna in 1869 should be considered the birthplace and date, respectively, of the TCR, even though that term was not used to refer to the phenomenon until a century later.1 Florian Kratschmer (1843–1922), a graduate of medicine from the Joseph’s Academy, was a 27-year-old fresh graduate when he started working for a single year in Hering’s laboratory in Vienna as a research assistant. Soon after this 1 year of physiological research, he pursued a career as a military physician, becoming head of a laboratory for public health.2 He became the renowned and respected specialist in hygiene and, in 1903, became the first military physician to be titled Professor of Hygiene at the University of Vienna.3 He published only one paper in respiratory physiology, but it established and detailed the mechanisms and importance of respiratory and cardiovascular reflexes from the nose and larynx. He applied “natural stimuli” such as cold air, tobacco smoke, carbon dioxide, ammonia, and chloroform to different parts of the upper airway of cats and rabbits, recorded a variety of responses, and established their nervous pathways by nerve sections. He described the glottal closure reflex on nasal and laryngeal stimulation; the cardiovascular responses with the same stimuli; and the respiratory, cardiovascular, and glottal components of the diving reflex. He was the first to describe cardiac arrhythmias on upper airway stimulation.1–5 In his seminal article, he stated, “we notice yet another striking phenomenon in the appended curve sections. Despite the considerable slowing of the heart beats, such as one perceives only, perhaps, after excitation of the peripheral ends of the Vagi, the blood pressure remains more or less at the same height, or even rises”.4 This observation was the basic building block in our understanding of the TCR.

In the early twentieth century (1908), Austrian gynecologist Bernhard Aschner (1883–1960) and Italian physician Giuseppe Dagnini (1886–1928) independently described yet another theretofore unknown phenomenon. They both observed that the application of pressure to the eyeball resulted in slowing of the heart rate.6,7 Aschner also described the oculorespiratory reflex and, by dividing the branches of cerebral nerves, demonstrated that a stimulation of all branches of the trigeminal nerve elicited a positive reflex. He was the first to describe the reflex pathway.8 The afferent limb of this reflex is the ophthalmic branch of the trigeminal nerve (CN V), from which fibers pass to the gasserian ganglion and thereafter to the main sensory nucleus of the trigeminal nerve; the efferent pathway is the vagus nerve (CN X).8 Since the Aschner and Dagnini descriptions, the oculocardiac reflex (OCR) and oculorespiratory reflex have been studied extensively in early and mid twentieth century publications in the specialties of ophthalmology and anesthesiology.9–31

The OCR remained under close attention by anesthesiologists and ophthalmologists; however, there were reports of a similar reflex in areas that were not innervated by the ophthalmic branch of the trigeminal nerve, and authors interpreted that reflex as a variation of the OCR.32–35 Referring to these reports, and on the basis of their own observations, M. P. Shelly and J. J. Church, two English anesthesiologists, mentioned in a letter to the editor that they had observed bradycardia associated with ventricular ectopic beats during cosmetic maxillary ostotomy when the maxilla is manipulated. They concluded, “Since the parasympathetic supply of the face is carried in the trigeminal nerve, traction on areas within its distribution will result in parasympathetic stimulation and bradycardia in a manner analogous to traction on viscera. Perhaps it is … time we discarded the term oculocardiac reflex in favor of trigeminocardiac reflex. It would then be clearer that the oculocardiac reflex, although most commonly elicited, is just one manifestation of a more general reflex phenomenon. In addition, it would no longer be a surprise when traction on areas within the trigeminal distribution produced bradycardia.”36

Coining the term “trigeminocardiac reflex” was the most important milestone in the history of the TCR. Not only did the phenomenon get an appropriate name, but it also got a broader definition, from which so many questions seemed to be answered.

There were several facial plastic and maxillofacial surgical procedures during which surgeons had observed occurrences of bradycardia. In agreement with previous observations, these findings led to the conclusion that, regardless of which branch of the trigeminal nerve transmits the afferent impulses, an efferent arc always involves the vagus.37–42 The same findings suggested that, no matter which branch of CN V and what part of the branch in question is manipulated, the result is the same and the reflex may occur. Together with an earlier finding from Kumada et al. (1977) that described similar autonomic “trigeminal depressor” responses after low-frequency electrical stimulation within portions of the trigeminal complex in anaesthetized or decerebrated rabbits, the surgeons’ findings indicated that not only peripheral, but also central, stimulation of parts of the trigeminal pathway results in autonomic reflex responses.43

On the basis of these different observations, in 1999 Bernhard Schaller, a young Swiss neurosurgeon, and his team defined the phenomenon of the TCR as currently known and initially described the occurrence of the central TCR in humans after stimulation of central parts of the trigeminal nerve during cerebellopontine angle and brain stem surgery.44 Because his team synthesized previous knowledge and incorporated it into their own observations, Schaller is considered the discoverer of the TCR. Besides defining the phenomenon, Schaller employed a causal approach that emphasized the nature of the TCR and led to its acceptance all over the globe. Subsequently, the scientific and medical world’s understanding of the underlying mechanism and clinical relevance of this reflex response and its implications for postoperative outcomes increased nearly year by year.45–47 It was in this context that Schaller then merged the two phenomena of the peripheral TCR and the central TCR to a common concept, which is now generally accepted.48

Although clinical case reports are usually underestimated by mainstream scientific journals, they represent an important, and sometimes even exclusive, way of communicating new and unusual clinical findings. Moreover, they may represent the main source of new knowledge about rare clinical features in medicine, especially surgery. Generalizing and hypothesizing from a few case reports always presents a substantial problem. However, in the development of our current understanding of the TCR, initial single-case reports led to multiple cases, systematic reviews, and experimental cases in craniomaxillofacial surgery, facial plastic surgery ophthalmology, and neurosurgery.43–78 The findings obtained from these different sources, irrespective of both their small sample size and the particular surgical subdisciplines they represented, shed light on new investigations. As a result, researchers all over the world began to be interested in the TCR and, indeed, the topic became popular among medical scientists. But it was Schaller again who alone understood, as he did in the early years of his TCR research, that the phenomenon could be further explicated only by case reports or small series of cases.

Despite the...