Remarkable physicians associated with Pulsus Paradoxus, the Classic Sign-Richard Lower and Adolf Kussmaul

Woo, H & Fung, C.

(Editor's note: This paper was first published here in 2006. It was later plagiarised in 2010. The 2010 paper was subsequently retracted by the International Journal of Cardiology in 2011).

Summary:


The modern definition of pulsus paradoxus is the greater than 10 mm Hg inspiratory decline in systolic arterial pressure.  (Bickley et al, 1999; Tierney et al, 2006; Valentin et al, 2004; Warrell et al, 2003)  Kussmaul originated the term pulsus paradoxus in 1873.  (Kussmaul, 1873/2006)  Interestingly Lower also described the characteristic phenomena of pulsus paradoxus.  (Lower, 1669/1832)  However, his contributions to pulsus paradoxus are not as well recognized as that of Kussmaul’s contributions.  (Gauchat et al, 1924; Bilchick et al, 2002; Swami et al, 2003)  In this article, we examine the original descriptions of pulsus paradoxus by both Lower and Kussmaul.  We also highlight some of the major contributions of Lower to cardiovascular physiology.  We aim to help readers appreciate Lower as a noteworthy figure in the history of medicine.  We end by comparing and contrasting the historic and modern definitions of pulsus paradoxus.

Richard Lower (1631-1691):
One of the few known portraits of Richard Lower shows a young man in his 20’s, his intense eyes penetrating through dark shoulder-length hair.  (Dewhurst, 1980)  He does not look familiar to many, especially to those without a medical background.  Yet Lower undoubtedly belongs in the pantheon of the greatest physicians.  His life and work paint a portrait of a passionate and non-conforming mind.  These characteristics helped him challenge tradition and make major contributions in anatomy and physiology, bringing great acclaim in his lifetime.  These same characteristics may have also brought him misfortune and attenuated his standing in the history of pulsus paradoxus as well as the history of medicine.


Lower was born in Cornwall of a “very good family.”  (Lower, 1669/1932)  Isolated on the southwest corner of England, Cornwall seems like a perfect beginning place for Lower.  It was the last part of England to submit to Saxon rule.  (“Cornwall”, 2006)  Lower seemed to embody the Cornish legacy with a habit of not submitting to conformity.


Scientific Career
Oxford was an ideal starting place for Lower to study medicine.  He soon fell into the fold of the “Oxford Experimental Philosophical Clubbe” whose “virtuosi” included Robert Boyle (1627-1691), Thomas Willis (1621-1675), and John Locke (1631-1691).  (Dewhurst, 1980)  Lower had a gift as an anatomical dissector which caught the attention of Willis, who put him and Christopher Wren (1632-1723) to work in the anatomy lab.  Their efforts produced a masterpiece, Cerebri anatome.  (Willis, 1664/1971)  In the treatise’s introduction, Willis celebrated Lower as “a most Learned Physician and highly skilful Anatomist.”  (Willis, 1664/1971)  Lower began practicing medicine even before receiving his medical degree from Oxford.  He was abetted by Boyle, who sent shipments of laudanum (tincture of opium) to use as treatments.  (Dewhurst, 1980)  Lower stamped his name into history by performing the first known transfusion between animals in 1665.  (Gotch, 1908)  Later that year, Lower finally received his medical degree.


Lower’s pioneering research in anatomy and physiology culminated in the 1669 publication of Tractatus de Corde.  His investigations challenged much of the established medical knowledge which was mostly rooted in Galenic and humoral tradition.  He ventured to consider the treatise as an extension of the work of the great William Harvey:
“…there are points not mentioned in Harvey’s circulation which need consideration….Harvey himself, indeed, seems to promise further contributions, had age and time allowed ….I have myself tried to fulfil the promises of that excellent man, and to bring nearest to completion than they have hitherto been.”  (Lower, 1669/ 1932) 


In Chapter Two of De Corde, Lower confronted the widely held belief of ebullition.  Briefly, ebullition was based on the work of Paracelsus whereby a chemical reaction was believed to occur in the blood.  (Hoff, 1936)  The reaction created among other things a turbulence that caused the circulatory movement of blood and the contractions of the heart.  (Hoff, 1936)  Rene Descartes was one of the many adherents of ebullition, but Lower had no reservations declaring that they were all wrong.  (Lower, 1669/1932)  Through a number of observations and experiments, including one where he replaced the circulating volume of a dog with beer, he disproved ebullition as the source of motion for the heart and blood.  (Lower, 1669/1932)
In Chapter Three of De Corde, Lower challenged prevailing theories regarding the change in the color of blood from dark and venous to bright and arterial.  Again by observation and experiment he ascertained that the lung was the critical organ for the blood’s color change:
“I have shown that the bright colour of arterial blood is not acquired through any heating in the heart or anywhere else at any time.  In like manner also the dark colour of venous blood is independent of any extinction of its heat within the veins….This must attributed entirely to the lungs, as I have found that the blood, which enters the lungs completely venous and dark in colour returns from them quite arterial and bright”  (Lower, 1669/1932)
In De Corde Lower also demonstrated a keen understanding of the pericardium.  He recognized the consequences of excessive fluid accumulation in the pericardial space, i.e. pericardial effusion:  “The fluid enclosed in the pericardium renders great service in lubricating the surface of the heart and in facilitating its movement; it likewise occasionally oppresses and floods the heart when it is in excess.”  (Lower, 1669/1932).


            Lower astutely recognized the converse, i.e. the consequences of pericardial fluid absence.  He hypothesized a constrictive situation for the heart:
“For, just as it [pericardium] injures the heart by accumulation of fluid within in, so, when this is completely absent, it approaches so close to the heart, that at length it adheres everywhere to this organ….How great a hindrance and disadvantage this must be for both organs….”  (Lower, 1669/1932).


Lower went on to illustrate a case of constrictive pericarditis.  In describing the case, he makes a discerning observation on the pulse that would foreshadow Kussmaul, i.e., the paradoxical pulse:


“The wife of a certain citizen of London, aged 30, healthy and active enough previously, became very dejected and melancholy during the last three years of her life, suffered from breathlessness on the least exertion, had a small and often an intermittent pulse.” (Lower, 1669/1932)


Lower hypothesized in great detail how the intermittent pulse may have occurred.  He suggested that because of an adherence between the pericardium and diaphragm, the subsequent motion of the “the diaphragm must of necessity have carried the heart down with it at every inspiration, and during that time must have held up and suppressed its movement.  So the observed intermission of the pulse succeeded regularly at every inspiration.” (Lower, 1669/1932).


Lower’s last major publication was De Catarrhis in 1672.  Again he would go on to challenge a widely held belief regarding catarrh.  Based on the humoral theory, many thought that catarrh was a vital fluid draining from the brain.  (Lower, 1672/1963)  Lower proved with his usual method of observation and experiment that catarrh was not cerebral fluid, but instead a secretion from the nasal passages.  (Lower, 1672/1963)  Possibly more significant but added only as an appendix to the treatise, Lower had “a few words” about venesection.  (Lower, 1672/1963)  He carefully described his technique of phlebotomy as well as the instruments he used which would become the prototypes of the modern syringe and needle.  (Lower, 1672/1963) 


            Lower rose to be one of the most eminent physicians of London.  (Gotch, 1908)  He was elected to the Royal College of Physicians, and enjoyed a period of great acclaim.  (Felts, 2000)  Fame may have diverted his attention from further research and scientific inquiry as he did not publish any major works after De Catarrhis.  However, De Corde did go through seven editions with significant changes, suggesting that Lower continued to perform some research. (Lower, Lower 1672/1963)


A Legacy without an Eponym


Lower had a strong sense of loyalty to his teacher Willis.  When the Irish doctor Edmund O’Meara disparaged Willis, Lower quickly came to his teacher’s defense.  He published Vindicatio, vindicating Willis and striking at O’Meara’s humoral traditions. (Felts, 2000)  Lower did not use soft tones in his dispute with O’Meara, calling him “a little frog from the swamps of Ireland.”  (Hughes, 1991)  In addition, Lower proved that he was a formidable adversary who had a long memory of past slights.  When De Corde was published years later, Lower condemned O’Meara again, referring to him as someone who “takes first prize for sheer perversity and stupidity. (Lower, 1669/1932)


Not surprisingly, Lower’s strong medical opinions were coupled with strong political convictions.  His Whig and anti-catholic positions cost him his repute when James the Second ascended to the English throne in 1685.  (Gotch, 1908)  Lower fell into dishonor and died at his London home in Covent Garden from a febrile illness.  (Lower, 1669/1932)  That Lower was not recognized as a greater figure in medicine may be partially due to the disrepute at the twilight of his career.  (Felts, 2000)  Additionally, his masterpiece De Corde was not translated to English from Latin until 1932.  (Lower, 1669/1932)  His political disgrace did not mean he was destitute.  His will revealed a significant estate.  Even with his final words, Lower asserted his opinion, willing part of his estate to the poor, but nothing to the then financially-strapped Royal College of Physicians.  (Lower, 1672/1963)

Adolf Kussmaul and his description of Pulsus Paradoxus:
Unlike his predecessor Lower, Adolf Kussmaul (1822-1902) is a well recognized figure in the history of medicine.  Eponyms like Kussmaul’s sign and Kussmaul breathing give him instant recognition to clinicians.  Like Lower, he studied medicine at university with a strong foundation in the scientific method.  Kussmaul considered his alma mater, Heidelberg, as a university built on “the secure ground of natural sciences” (Kussmaul, 1899/1981) at time when the Germany university was the “undisputed center of scientific medicine.” (Walker et al, 1990)


Kussmaul started his medical career as a country doctor.  However, his career was cut short due to a severe illness, self-diagnosed as “meningitis”.  (Kussmaul, 1899/1981)   Upon recovery, he “renounced the country practice” feeling he “was no longer equal to it” and turned to a career in academic medicine in 1853.  (Kussmaul, 1899/1981)  He meticulously prepared for an academic career with coursework at Wurzburg (Kussmaul, 1899/1981).  He spent about a year building up his credentials learning from the likes of Rudolph Virchow.  (Kussmaul, 1899/1981) 
Kussmaul originated the term pulsus paradoxus in 1873 with the publication of Ueber schwielge mediastinopericarditis und den paradoxen puls (On adhesive mediastino-pericarditis and the paradoxical pulse).  (Kussmaul, 1873/2006)  In the document Kussmaul carefully described three cases of constrictive pericarditis and pulsus paradoxus with meticulous clinical observation.  In each case, he draws attention to “an interesting phenomenon” of the pulse, exemplified in the excerpt:
“A 34 year old unemployed servant girl, whose mother had died of pulmonary disease, had suffered for many years each winter from a dry cough and for three years a constricting feeling which at times became dyspnea….On admission, she appeared cachectic, with edema of the legs and ascites.  The phenomenon of the arterial pulse with regular and constant action of the heart was observed at the initial examination.  The pulse would become smaller with inspiration or would become totally impalpable on deep inspiration.  On expiration it returned to its former amplitude….  The disappearance or diminution of the pulse during inspiration was manifest in all palpable arteries.”  (Kussmaul, 1873/2006)


Kussmaul proposed the intriguing term paradoxical pulse (pulsus paradoxus in Latin) to describe his findings: 
“I suggest naming this pulse paradoxical, partly because of the conspicuous discrepancy between the cardiac action and the arterial pulse, partly because of the pulse, despite its irregularity, actually waxes and wanes in a regular fashion….The interesting phenomenon which these three cases of mediastinopericarditis present is the pulse.  In all three, it was rapid, almost always more than 100, the impulse of low amplitude, the tension soft, and the rhythm paradoxical in two ways:  (1) despite continuing action of the heart, the pulse disappeared for short intervals at the palpating finger, one or two beats completely or almost completely and then returned immediately for two or more beats; (2) the apparent irregularity was in actuality only the difference associated with he phases of respiration…This unique phenomenon was manifest in all palpable arteries.”  (Kussmaul, 1873/2006)
Kussmaul acknowledged that he was not the first to describe pulsus paradoxus:  “According to my knowledge, up to now only one case of this interesting disorder has been published, namely, Griesinger in 1854…”  (Kussmaul, 1873/2006)  While Kussmaul was not aware of Lower’s description of pulsus paradoxus, probably because De Corde was only available in Latin or an even rarer French translation, their astute minds were connected across the centuries by their writings.  (Lower, 1669/1932)


Kussmaul hypothesized about the pathophysiology of pulsus paradoxus in constrictive pericarditis.  He came to a similar conclusion as Lower that somehow the physical adherence of the pericardium to a nearby structure was critical:  “The essential anatomic condition for the development of the paradoxical pulse appears to be the adherence between the pericardium and the sternum…”  (Kussmaul, 1873/2006)
Kussmaul noted that pulsus paradoxus was not unique to constrictive pericarditis, describing the phenomenon in a patient with a massively dilated right main bronchus from tuberculosis.  He concluded that
“...the paradoxical pulse may also occur without pericarditis.  This sign is consistently a result of mediastinal disease, and we may only assume that it is mediastino-pericarditis when the history, onset, and course of the disease present as additional criteria for the diagnosis of pericarditis.”  (Kussmaul, 1873/2006)

Pulsus Paradoxus:  Modern Definition:
The modern definition of pulsus paradoxus is the greater than 10 mm Hg inspiratory decline in systolic arterial pressure.  (Bickley, 1999; Tierney, 2006; Valentin, 2004; Warrell, 2003) This more precise modern and quantitative definition of pulsus paradoxus differs from the original in a number of important ways. 
First, the clinical method of determining pulsus paradoxus has gone through a number of transitions.  When first described by Lower and Kussmaul, pulsus paradoxus was determined simply by palpating the patient’s pulse and ascertaining for the characteristic pattern.  In 1924, Gauchat and Katz proposed a systematic codification of pulsus paradoxus that built on Kussmaul’s observations, and included criteria on the respirations and blood pressure:


“By a pulsus paradoxus, pulsus respiratio, or Kussmaul’s pulse, we mean a rhythmical pulse which diminishes perceptibly in amplitude or is totally obliterated during inspiration in all palpable arteries.  It is a periodic waxing and waning of pulse amplitude, which from the standpoint of clinical interest must occur without conscious effort on the part of the patient to modify his breathing.  This diminuation in pulse amplitude is always accompanied by a fall in systolic blood pressure….we exclude all pulse phenomena which cannot be detected by the palpating finger and likewise any instances in which the subject intentionally influences the character of his respirations”  (Gauchat & Katz, 1924)
In 1952, Dornhorst et al. performed experiments to quantify the change in the pulse pressure in pulsus paradoxus.  They proposed that a drop of 10-15 mm Hg in pressure was essential to create pulsus paradoxus, setting the stage for the current modern definition.


            Second, the clinical significance of pulsus paradoxus has also changed over time.  In their original descriptions, Lower and Kussmaul both wrote about pulsus paradoxus in the clinical context of constrictive pericarditis, a chronic condition.  In the modern setting, pulsus paradoxus is usually seen as a warning sign of an acute medical emergency such as cardiac tamponade.  (Tierney, 2006)  Pulsus paradoxus is also observed in a number of other clinical situations, including obstructive pulmonary disease, pulmonary embolism, circulatory shock, tension pneumothorax, right ventricular infarct, bilateral pleural effusion, restrictive cardiomyopathy and tracheal compression.  (Swami et al, 2003).

 
            Third, the physiology of pulsus paradoxus is now much better understood.  Lower and Kussmaul both hypothesized that somehow the physical adherence of the pericardium to nearby anatomic structures caused pulsus paradoxus.  The exact mechanism is still debated by modern physiologists.  (Bilchik, 2002)  The most common theory relates to more blood filling the right ventricle during inspiration due to increased venous return.  The increased volume in the right ventricle causes the interventricular septum to shift from right to left, consequently decreasing the left ventricle stroke volume and systolic pressure.  (Valentin, 2003) .


            Fourth, we now know that the pulsus paradoxus phenomenon is a continuum.  For Lower and Kussmaul, the intriguing behavior of the pulse was either present or not present on examination of the patient.  With the advent of direct arterial catheters, the normal rhythmic fluctuations in the blood pressure with normal inspiration are readily observed. (Swami, 2003)  In effect, the finding of pulsus paradoxus is actually an exaggeration of a normal phenomenon produced by extreme circumstances.


            Lastly, the term pulsus paradoxus seems like a misnomer to many modern clinicians.  Pulsus paradoxus was an elegant term that aptly described the seeming paradoxus of a beating central pulse (heart) but absent peripheral pulse.  In the modern setting, a patient may or may not have an intermittently absent pulse, yet still have pulsus paradoxus as defined by the requisite drop in blood pressure.


Submission date:  August 27, 2006

Publication Date: September 2006

 

 

References:

 

Bickley, L.S., Hoekelman, R.A.  (1999). Bates’ Guide to Physical Examination and History Taking (7th ed.), Philadelphia: Lippincott. p. 317.

Bilchick, K.C., Wise, R.A.  (2002)  Paradoxical physical findings described by Kussmaul: pulsus paradoxus and Kussmaul’s sign. Lancet; 359, 1940-42.

Cornwall. (2006). In Encyclopædia Britannica. Retrieved August 27,  2006, from Encyclopædia Britannica Online: http://search.eb.com/eb/article-9026362

Dewhurst, K. (1980) Thomas Willis’s Oxford Lectures. Oxford: Sandford Publications.  p. 7-9, 22, 42-45.

Dornhorst, A.C., Howard, P., Leathart, G.L.  (1952).  Pulsus Paradoxus.  Lancet, 1(15). 746-748.

Felts, J.H. (2000).  Richard Lower: Anatomist and Physiologist.  Ann. Intern. Med.  132. p. 420-423.

Gauchat, H.W., Katz, L.N.  (1924).  Observations on Pulsus Paradoxus.  Arch. Intern. Med., 33. 350-370.

Gotch, F. (1908).  Two Oxford Physiologists.  Oxford: Clarendon Press.  p. 6-7.

Hoff, P.M., Hoff, E.C. (1936).  The Life and Times of Richard Lower, Physiologist and Physician.  Bulletin of the Institute of the History of Medicine.  4:7.  p. 521.

Hughes, J.T., (1991).  Thomas Willis 1621-1675: his life and work.  New York: Royal Society of Medicine Services. p. 35.

Kussmaul, A. (1981). Memoirs of an Old Physician. (2nd ed.) (WR Stewart, Ed. Trans).  New Delhi: Amerind (Original work published 1899). p. 132, 340, 344-345.

Kussmaul, A. (2006).  On Adhesive Mediastino-Pericarditis and the paradoxical pulse.  (Translated excerpts) Berliner Klinische Wochenschrift, (Original work published 1873). Retrieved August 27, 2006 from http://www2.umdnj.edu/~shindler/pulsuspdx.html.

Lower, R. (1932).  A Treatise on the Heart (K.J. Franklin, Trans.).  In R.T.Gunther (Series Ed.), Early Science in Oxford: Vol. 9. De Corde by Richard Lower (pp. xi-xiv, [1-120]). Oxford: Printed for the Subscribers. (Original published 1669).

Lower, R. (1963).  De Catarrhis (R. Hunter & I. Macalpine, Trans.).  London: Dawsons of Pall Mall (Original work published 1672).  p. xiii-xiv, 4-14, 17.

Swami, A., Spodick, D.H.  (2003)  Pulsus Paradoxus in Cardiac Tamponade: A Pathophysiologic Continuum.  Clin. Cardiol., 26, 215-217.

Tierney, L.M., McPhee, S.J., Papadakis, M.A.  (2006).   Current Medical Diagnosis and Treatment (45th ed.), San Francisco, Lange Medical Books/McGraw-Hill, p. 409.

Trevor, J.T. (1991) Thomas Willis 1621-1675: his life and work, New York, Royal Society of Medicine Services, 35.

Valentin, F., Alexander, R.W., O’Rourke, R.A. (2004).  Hurst’s The Heart (11thed.), Retrieved August 27, 2006 from McGraw-Hill’s Access Medicine Online subscription service http://www.accessmedicine.com/home.aspx.

Walker, H.K. (1990).  Origins of the History and Physical Examination. In Clinical Methods: The History, Physical and Laboratory Examinations (3rd Ed.).  Retrieved August 27, 2006 from
http://www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=cm

Warrell, D.A., Cox, T.M., Firth, J.D., Benz, E.J.  (2003) Oxford Textbook of Medicine 4th Edition, New York: Oxford University Press, 1045.

Willis, T.  (1971). The Anatomy of the Brain. (S. Pordage, Trans.).  Tuckahoe, New York: USV Pharmaceutical Corp. (Original work published 1664).  pp. 3-4.

 

Authors and affiliations:
Hawkin E. Woo, M.D.
University of California, Los Angeles
Los Angeles, California  90095
United States
hewoo@mednet.ucla.edu

Constance H. Fung, M.D., M.S.H.S.
Veteran Administration Greater Los Angeles Healthcare System
Los Angeles, California  90073
United States

 

 

Submission date: August 27, 2006

Publication Date: September 2006

 

Substnatial portions of this paper were later plagiarised and published: Abu-Hilal MA. Mookadam F. Pulsus paradoxus; historical and clinical perspectives. International Journal of Cardiology. 138(3):229-32, 2010 Feb 4. This latter plagiarised paper has subsequently been retracted by the International Journal of Cardiology.

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