A Peculiar Type of Dyspnea: Kussmaul, Cheyne-Stokes, and Biot Respirations Volume 3, Issue 1, E22 John W Stanifer, MD, MSc ISSN:1946-3316 Fellow, Duke University Hospital

Abstract:

Observations concerning respiratory rates and patterns date back to the time of Hippocrates and Galen, and there are many descriptive terms such as ataxic, agonal, and clustered. Among these terms are three well-known but often misunderstood and misused eponymous respiratory signs: Kussmaul , Cheyne-Stokes respiration, and Biot respiration. In the 21st Century, in which roentgenograms and laboratory tests often serve as surrogates for physical examination, respiratory patterns – though frequently present – are often overlooked. Herein, to rejuvenate clinical interest and clarify misconceptions concerning their application and utility, we present clear descriptions of three useful clinical signs: Kussmaul respiration, Cheyne-Stokes respiration, and Biot respiration.

Keywords: Kussmaul, Cheyne-Stokes, Biot, dyspnea

Introduction misunderstood, eponymous respiratory patterns: Kussmaul respiration, Cheyne- The most regularly overlooked and ignored Stokes respiration, and Biot respiration. vital sign in the clinic and wards today is the , and it has nearly become the Kussmaul Respiration standard to simply document twenty breaths per minute as the rate when we think of the A Peculiar Type of Dyspnea: In this patient as normally (Figure 1). In type of dyspnea there is not the least the 21st century, when physicians frequently suggestion as is so common in all spend more time in front of a computer than other types that the passage of air to at the bedside, it would be uncommon to or from the lung has to combat merely observe a patient’s respiratory obstruction in its path; to the pattern for many minutes; however, contrary it passes in and out with the important clinical information can be missed greatest of ease. The thorax expands by our lack of observation. In an effort to noticeably in all directions without a revive clinical interest, increase awareness pulling-in of the lower end of the of these signs, and clarify historical dispute, sternum or intercostals spaces… and we present the index cases1 and descriptions this complete inspiration is followed of three well-known, but often missed and by a likewise complete expiration… Yet everything is indicative of 1 Index case refers to the clinical case in which a extreme air hunger, such as the condition or sign was first described. discomfort of angusty of which the Epistola Stanifer

patient complains, the extreme The present day clinical significance is that activity of the respiratory muscles, the air-hunger described by Kussmaul is and the loud noise that the powerful secondary to extreme metabolic acidemia. inspirations and more so the Patients with this type of acidemia exhibit expirations make… A true , markedly low partial pressure of arterial however, never exists… To the carbon dioxide (pCO2) as compensation for contrary the noise of expiration often low bicarbonate. Figure 2 shows the becomes a groan even when the respiratory tracing representative of a patient patient lies unconscious in deep with Kussmaul respiration; as demonstrated coma… The marked contrast in the figure, the respiratory rate is normal between the extreme general or slightly reduced. Although the rapid, weakness of the patient and the shallow respirations that accompany less powerful respiratory movements is a severe acidemia will often be described as striking peculiarity of this picture. Kussmaul respirations, the pattern Kussmaul (1) described is more accurately a sign of severe acidemia when the rate of respiration has This clinical scenario which depicts a decreased dramatically. diabetic patient was written by Adolf Kussmaul (1822-1902) in 1874. A year after Although the index case describes a diabetic his ground-breaking accounts of Kussmaul coma, patients with advanced renal failure, Sign and Pulsus Paradoxus, he published , or intoxications such as ethylene “A Peculiar Type of Dyspnea” wherein he glycol may present in a similar manner. first documents this respiratory pattern now Physicians should be alert to such known as Kussmaul Respirations. He had possibilities, especially if they observe trained under the famous physicians Rudolf dyspnea distinguished by large tidal Virchow, Franz Näegele, Josef Skoda, Carl volumes without adventitial breath sounds von Rokitansky, and Ferdinand von Hebra or increased work of breathing. and was well-equipped by 1874 with the clinical acumen and pathologic skills to Cheyne-Stokes Respiration make such an observation. The only peculiarity in the last In describing these respirations, his name period of his illness… was in the has become synonymous with the term state of the respiration: For several diabetic coma which was formerly referred days his breathing was irregular; it to as “Kussmaul Coma”. Without would entirely cease for a quarter of understanding the acid-base physiology a minute, then it would become responsible for the “peculiar type of perceptible, though very low, then by dyspnea”, he nonetheless suspected that a degrees it became heaving and chemical imbalance due to the patient’s quick, and then it would gradually was responsible. He went on to cease again: this revolution in the study the effects of acetone, chloroform, state of his breathing occupied about ether, and alcohol on rabbits and humans a minute, during which there were which, when viewed with knowledge of the about thirty acts of respiration. (3) physiologic disturbances these substances causetoday, suggest that he was on the right Dr. John Cheyne (1777-1836) first noted track. (2) this “peculiar” breathing pattern in 1818. In that year, he published a paper entitled “A

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Case of Apoplexy, in which the Fleshy Part curiously, it was Camille Biot, known for of the Heart was converted into Fat” in the eponymous Biot Respiration, who which he described the index case of a 60- conducted much of the research. year-old man who eventually died from congestive and apoplexy We now know that Dr. Stokes was at least (stroke). Figure 3 demonstrates the partially right in his assumption of this respiratory tracing for this breathing pattern; breathing pattern’s etiology; however, it is characterized by gradual increasing and because Cheyne-Stokes respiration occurs as decreasing tidal volumes followed by short a result of damage to the respiratory control periods of .2 centers whereby the normal feedback for increasing or decreasing pCO2 levels is The breathing pattern was again diminished, it is not entirely specific for independently described by William Stokes congestive heart failure as he suggested. (1804-1878) in 1854. Propitiously, William Less commonly, it can be a sign of stroke Stokes had trained at the Meath Hospital in (apoplexy), toxic encephalopathies, Dublin where Cheyne had been an attending traumatic encephalopathies, high-altitude physician; this placed him in a unique , and sleep apnea. situation to further study the peculiar dyspnea described by Cheyne in 1818. Dr. Today, during emergency situations, its Stokes again recognized this sort of presence can be a valuable clue for the breathing pattern from a mere observation bedside physician; its prompt recognition and tried to connect it, physiologically, to during the physical assessment can lead to “degeneration of the heart” which he earlier initiation of therapy while waiting on thought was quite specific to the disease more advanced diagnostics such as state resulting in the dyspneic symptoms. In radiographs. 1854, he wrote: Biot Respiration It consists in the occurrence of a series of inspirations, increasing to a As an intern in Lyon, France, in 1876, maximum, and then declining in Camille Biot (1850-1918) wrote of a 16- force and length, until a state of year–old-patient with tuberculous apparent apnea is established. In this : condition the patient may remain for such a length of time as to [appear] Peculiarly, this breathing pattern dead, when a low inspiration…marks lacks the crescendo-decrescendo the commencement of a new cycles attributed to Cheyne-Stokes ascending and then descending breathing and is completely series of inspirations…The decline in irregular with varying periods of the length and force of respirations apnea. The breathing pattern is is as regular and remarkable as their irregular and rapid, with rhythmical progressive increase. (4) pauses lasting 10-30 seconds, but sometimes with alternating periods Cheyne-Stokes respiration was well-known of apnea and .3 (5, 6) th by the later part of the 19 century, and 3 Tachypnea is defined as a respiratory rate greater 2 Apnea refers to the absence of respiration than twenty-two times per minute

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cluster breathing implies a regular pattern Originally, this breathing pattern was called with variable tidal volumes and periods of “rhythme meningitique” as it was routinely apnea (Figure 5). used by physicians as a diagnostic tool for meningitis; however, today we know it as The clinical significance of Biot respiration Biot respiration. (5) Although others before today can be appreciated by again him, such as Armand Trousseau, had examining the setting in which he initially remarked on this “peculiar” breathing described it. The index case was a sixteen pattern, Biot was the first to categorically set year old man with severe central nervous it as a distinct entity. system pathology, i.e. tuberculous meningitis; thus, it is not unexpected that it It is characterized by a highly irregular or is still considered a sign of brainstem ataxic breathing pattern with variable tidal infarction or uncal herniation. (7) volumes and random periods of apnea Additionally, some have suggested that Biot (Figure 4). Unfortunately, there is much respiration can also occur in prolonged, historical confusion regarding the definition chronic opiate use (8) as well as being of Biot respiration. Biot, who was an expert erroneously attributed to high-altitude in the study of Cheyne-Stokes respiration, pulmonary edema, where it was confused first described his eponymous respiratory with the correctly associated Cheyne-Stokes pattern in a paper examining Cheyne-Stokes respirations. (9) respiration, and this may have initially led to the confusion. However, most conspicuous As with any type of agonal breathing, is the misunderstanding between Biot recognition of Biot respiration should respiration and cluster breathing, both of prompt urgent action by the physician which are types of agonal breathing patterns. especially if it occurs in conjunction with Definitions of Biot respiration vary from altered mental status, decreased level of “rapid, shallow breaths” to “clustered, consciousness, or other neurologic deficits. periodic breathing” but Biot respiration In these settings, where seconds and minutes should properly refer only to breathing are critical to patient outcomes, the alert patterns with markedly variable tidal physician who observes Biot respiration will volume, random , and no regularity: be able to act immediately rather than waiting for additional diagnostics. This irregularity of the respiratory movements is not periodic, Conclusion sometimes slow, sometimes rapid, Respiratory patterns can provide valuable sometimes superficial, sometimes and rapid insight into the clinical scenario of deep, but without any constant patients, and vigilance in observation should relation of succession between the be encouraged. By presenting and clarifying two types, with pauses following these eponymous respiratory patterns, it is irregular intervals, preceded and hoped that a rejuvenation of interest will be often followed by a sigh more or less sparked and lead to enhanced patient care. prolonged. (5)

This description lucidly illustrates that Biot References. respiration or is easily 1. Kussmaul, A. Zur Lehre vom distinguished from cluster breathing by its Diabetes mellitus. Deutsches Arch. irregularity. As suggested by the name, F. klin. Med. 1874; Leipz. Vol 14.

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2. Bast, Theodore. The Life and Times Adaptive Servoventilation (ASV) in of Adolf Kussmaul. Paul B Hoeffner, Patients with Sleep Disordered Inc. New York; 1926. Breathing Associated with Chronic 3. Cheyne, John. Case of Apoplexy, in Opioid Medications for Non- which the Fleshy part of the Heart Malignant Pain. J Clin Sleep Med. was converted into Fat. In The 2008 August 15; 4(4): 311–319. Dublin Hospital Reports and 9. Fujimoto K, Matsuzawa Y, Hirai K, Communications in Medicine and Yagi H, Fukushima M, Shibamoto T, Surgery. Dublin Press. Dublin; 1818: Koyama S, Levine BD, Kobayashi T. Vol II, pp 216-223. Irregulat nocturnal breathing patterns 4. Stokes, William. The Diseases of the high altitude in subjects susceptible Heart and the Aorta. Lindsay and to high-altitude pulmonary edema Blakiston. Philadelphia; 1854: 324- (HAPE): a preliminary study. 326. Aviation, Space, and Environmental 5. Biot MC. Contribution a l’etude du Medicine. 1989; 60(8): 786-91. phenomene respiratoire de Cheyne- Stokes. Lyon Med. 1876; 23:517- 528, 561-567. 6. Powell, R Douglas. Biot on Cheyne- About the Author: John W Stanifer, MD, Stokes Repiration. The London MSc is a Clinical Fellow at Duke University Medical Record. 1877 Feb 15; 4: 65- Hospital in Durham, NC who is currently practicing internal medicine and global 66. health medicine. In addition to his plans to 7. Wijdicks, EFM. Biot’s Breathing. J pursue a career in academic Nephrology, Neurol Neurosurg Psychiatry. 2007; Global Health, and Internal Medicine, he has 78:512-513. a strong interest in the history of medicine 8. Farney, Robert J; James M. Walker, especially as it pertains to disease Kathleen M. Boyle, Tom V. recognition and physical diagnosis. Cloward, and Kevin C. Shilling. (Email: [email protected])

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