Digital clubbing: A unique case and a new hypothesis A study of a unique case of unilateral digital clubbing secondary to a true posttmaumatic aneurysm of the ulnar artery in the palm is presented. The clubbing of the digits resolved following resection of the aneurysm. Detailed evaluation of the patient included Doppler flow studies, differential pulse pressure recordings, measurement of reactive hyperemia, angiography, and differential capillary blood gas determinations. The contralateral hand of this otherwise healthy young patient was employed as a control. Findings of increased blood flow, decreased peripheral resistance, and increased oxygenation then were evaluated in light of the findings of other investigators. This study and the information gathered from an extensive review of the literature strongly suggest that a neurocirculatory reflex is the common denominator of the various conditions associated with clubbing. The afferent and efferent limbs of this reflex are proposed.
Alan H. Gold, M.D., Bertram E. Bromberg, M.D., Joseph G. Herbstritt, M.D., and Harry Stein, M.D., Manhasset and Mineola, N. Y.
The earliest recorded description of the phenomenon
of clubbing of the digits usually is attributed to Hippocrates, who noted it in association with a case of empyema in the fifth century B.C. He wrote, "The nails of the hand are bent; the fingers are hot especially in their extremities. "1 Despite repeated observations over the centuries as a phenomenon common to many varied disease states, the significance and pathogenesis of digital clubbing has remained somewhat of an enigma. Case history A 32-year-old white policeman developed a pulsatile mass in the palm of his dominant right hand shortly after a single episode of rather minimal trauma approximately I year earlier. This was a blunt injury to his hypothenar eminence sustained as he forcefully slammed closed an open window. He had no complaints, except a vague feeling of "not enough blood" in his long finger. Examination was normal, except for the right hand. A 2 by 2 cm non tender , pulsatile mass was noted in the proximal hypothenar region, just distal to the hamate. No bruit was audible. No thrill was palpable. All of the fingers of the right hand showed marked clubbing, with the thumb being clubbed From The Department of Surgery (Plastic Surgery), North Shore University Hospital, Manhasset, N. Y., and The Long Island Plastic Surgical Group, P.C., Mineola, N. Y. Received for publication Dec. 9, 1977. Revised for publication June 22, 1978. Reprint requests: Alan H. Gold, M.D., 110 Willis Ave., Mineola, NY 11501.
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to a lesser degree (Fig. I). This contrasted sharply with normal, nonclubbed digits of the left hand and both feet (Fig. 2). An unusual opportunity to study the circulatory changes associated with clubbing in a healthy individual, using his own normal hand as a control, was recognized, and an extensive work-up followed_ Patient evaluation and treatment. Individual digital flow studies were performed using a Doppler technique. These showed an increased blood flow at rest and an increased rate of venous filling and emptying on the right (Table I). Comparison of reactive hyperemia between the right and left hands showed the right to be increased, further substantiating the finding of increased flow to the clubbed digits (Table II). Differential pulse pressure recordings were taken, comparing the clubbed to the nonclubbed side (Table III). The absolute values were not important; what was important was the comparative trend, a decrease in the digital artery pressure in the clubbed digits in relation to the nonclubbed. Comparative finger tip blood gases were studied prior to operation (Table IV). These were obtained by the microcapillary technique. Again, the general trend, not the absolute values, was important. Before operation, an increased P0 2 was noted in the blood obtained from the clubbed digits. A right brachial arteriogram was obtained (Fig. 3) and demonstrated an aneurysm of the ulnar artery just distal to its contribution to the deep palmar arch. A true aneurysm was found, and the ulnar digital artery to the little finger, which arose from the aneurysm, was ligated, the aneurysm was resected (Fig. 4), and an end-to-end anastomosis of the ulnar artery was performed. Microscopic examination of the specimen verified it as a true aneurysm
0363·5023/79/010060 028a07$00.70/0 © 1979 American Society for Surgery of the Hand
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Fig. 1. At the time the patient first presented, the fingers of the right hand showed marked clubbing, with the thumb being clubbed to a lesser degree. (Fig. 5). After operation, follow-up studies were performed on several occasions. Finger tip blood gases were reevaluated 7 months following the operation (Table V). There still was a minimal elevation of the P0 2 in the right hand as compared with the left. A brachial arteriogram at this time (Fig. 6) showed no evidence of blood flow in the ulnar artery distal to the site of resection. The Allen test was positive. At no time, however, did the patient complain of cold intolerance or claudication. At this time it also was noted that the conformation of the nails was changing. A line of demarcation was apparent across the nails, seeming to mark the juncture between the formerly clubbed nail and normal proximal nail growth (Fig. 7). At 27 months after operation, the fingers of both hands were very nearly symmetrical. Viewed from the side, the digits no longer demonstrated the' 'profile sign" of Lovibond and therefore, by definition, no longer were clubbed (Fig. 8). Fingertip blood gases again were studied, and the P0 2 of both hands was identical (Table VI). A comparison of the average finger tip gas determinations for each of the dates studied demonstrates the changes (Table VII).
Discussion How do our data compare with the findings of other investigators through the years? Hemodynamic changes in clubbing have included increased digital blood flow,2-8 decreased arteriovenous P0 2 differences,1-9 increased digital artery pressure,2-4, 8 and a resolution of the clubbing after correction of the instigating abnormality, that is, resection of the neoplasm, clearing of the infection, resection of the aneurysm, etc. 2, 4, 6-\1 Our findings are consistent with those in the literature, but two points require some explanation. Our finding of a decreased digital artery pressure is attributable to the alteration of local flow dynamics in
Fig. 2. The patient's clubbed digits contrasted sharply with the normal digits of his nonclubbed hand. the digital vessels by the proximity of the aneurysm. The normal situation of high pressure and low flow is changed to one of low pressure and high flow, by a combination of class III turbulence 12 and a compression
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Gold et al.
Fig. 3. A right brachial arteriogram obtained as part of the preoperative evaluation showed an aneurysm of the ulnar artery just distal to the ulnar contribution to the deep palmer arch. The ulnar digital vessel to the little finger arose from the aneurysm.
Table I. Blood flow studies (mIIlOO ml of tissue/min) Time (sec)
Digit Right long Left long
9.85 7.6
1.09 1.05
26.6 25.9
23 23
Table II. Blood flow studies (mil 100 ml of tissue/min)
Fig. 4. A section through the resected aneurysm demonstrates its proximal and distal ends. The base of the ulnar digital artery to the little finger which arose from the aneurysm is indicated by the large arrow in the upper left comer of the picture.
Digit
Reactive hyperemia
Right long Left long
28.2 23.2
Cuff tolerance
8 8
Nonnal Nonnal
laminar flow system. Because there has been no other reported study of so distal an aneurysm associated with digital clubbing, this local mechanical effect has not been described previously. The fingertip blood gas analyses also deserve comment. These studies were performed by a micro method of so-called capillary blood gas analysis. Though in normal flow circumstances, this is practically equivalent to an arterial blood sample, an alteration in the path of blood flow in the clubbed fingertip provided samples which contained proportionately little capillary blood. Many theories have been advanced to explain clubbing, some capable of explaining the production of
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Fig. 5. Microscopic examination of the specimen verified it as a true aneurysm. There is full thickness of the aneurysm wall, with fibrous thickening of the intima, and some attenuation and prominent fibrosis of the media. This probably reflects the pathogenesis of this lesion; trauma with scarring rather than initial arterosclerosis of the intima with secondary changes in the media. (Hematoxylin and eosin. Original magnification x 20.)
Table III. Pulse pressure recordings
Brachial Radial Ulnar Thumb Long finger Little finger
Right
Left
150/88 144/120/86/102/128/-
140/92 140/136/132/126/114/-
clubbing under limited circumstances, but none truly satisfactory. The most productive and satisfying studies to date have been those dealing with the dynamics of the circulatory changes in the involved digits and extremities.9. 13-16 These changes and the observed increase in local vascularity redirected attention to the local changes in the vascular anatomy. It was found that the distribution of the arteriovenous shunts, first described by Souquet in 1862 and then by Hoyer in 1877, strikingly paral-
Table IV. Fingertip blood gases before operation (June 7, 1974)
I
pH
HeOi
Po 2 *
Peo 2
Right thumb Right long Right little
7.48 7.48 7.48
26 25 24
76 76 87
36 35 34
Left thumb Left long Left little
7.48 7.48 7.48
23 23 27
62 61 66
32 34 37
Digit
'Po, valves of the right and left hands for each of the studied dates may show the change more clearly.
leled the localization of the pathological changes in clubbing.18. 19 These arteriovenous anastomoses are highly specialized vessels which permit blood to pass directly from small arterioles into the venous channels of the intermediate plexus, thus bypassing the normal capillary
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Fig. 6. An arteriogram performed after operation showed no evidence of blood flow in the ulnar artery distal to the site of resection. This patient ' s operation was performed before the use of vein grafts to provide tension-free anastamoses. It was tension that caused the obliteration at this point. In spite of this. the patient had no cold intolerance or claudication.
Fig. 7. Seven months after operation a line of demarcation (arrows) could be seen which seemed to mark the junction between the formerly clubbed nail and normal proximal nail growth.
bed and precluding any opportunity for exchange with the extravascular fluids . These shunts vary in structure, from very simple to quite complex. In 1924, Masson 20 termed them "glomeruli," in order to underscore their complexity and function as neurohumoral end organs. The digital glomus organs of more advanced structure are confined to the nail bed and pulp areas and lie adjacent to the periosteal arteries. 18 These glomeruli are richly innervated by nonmedul-
lated sympathetic vasomotor fibers which terminate in the adventitia. This extensive innervation has been shown to be under the control of the autonomic sympathetic nervous system, with the main action of the plexus being adrenergic (or vasoconstrictive), but with a significant cholinergic (or vasodilatory) action as well . 19 These shunts appear to be the end regulatory organs of the digital microcirculation. It has been shown also that the development of, or
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Table V. Fingertip blood gases after operation (January 14, 1975)
I
pH
HCO l
P0 2
Peo 2
Right thumb Right long Right Little
7.43 7.42 7.46
22 22 25
71 76 75
33 33 37
Left thumb Left long Left little
7.42 7.48 7.46
22 26 25
69 68
36 36 36
Digit
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Fig. 8. At 27 months following operation, the fingers of both hands were very nearly symmetrical, with the signs of clubbing no longer apparent.
Table VI. Fingertip blood gases after operation September 9, 1976 Digit
I
pH
HCO:';
Pat
Peat
Right thumb Right long Right little
7.45 7.47 7.45
24 25 24
66 72
74
35 36 35
Left thumb Left long Left little
7.49 7.48 7.49
27 25 27
74 75 71
37 35 36
Table VII. Comparative average P02 values
IRight ILeft I Difference
Before operation (June 7, 1974) After operation (January 14 , 1975) After operation (September 9 , 1976)
80 74 71
63 67 73
17 7 2
opening up of, new arteriovenous anastomoses can be provoked by certain alterations in vascular dynamics. This response appears to depend upon an intact nervous mechanism. 19 The available evidence strongly suggests that a neurocirculatory reflex is the common denominator of the various conditions associated with clubbing. The efferent limb of this reflex appears to be the cholinergic fibers of the autonomic sympathetic innervation of the digital arteriovenous shunts. The afferent limb of this reflex is somewhat more difficult to delineate. A number of authors have implicated the vagus nerve, and it does seem to provide a common pathway for stimuli from many of the intrathoracic and intraabdominal conditions associated with clubbing. In cases of unilateral clubbing, perhaps it is a change in blood flow dynamics which stimulates a baroreceptor or flow-receptor type of mechanism , which may comprise the afferent arc . Finally, it is the study of these shunts and their response to various neurological , chemical, and hemody-
namic stimuli which may provide the answer to the puzzle of digital clubbing. It is in this direction that we may look for fruitful investigations in the future . REFERENCES I. Hippocrates: Prognostic No . 17 , Vol 2, 1923, Loeb
Classical Library, p 25 2. Mendelowitz M: Clubbing and hypertrophic osteoarthropathy. Medicine 21 :269-306, 1942 3. Mendelowitz M: Some observations on clubbed finger. Clin Sci 3:387-400, 1938 4. Mendelowitz M: Measurement of blood flow and blood pressure in clubbed fingers . JClin Invest 20: 113-7, 1941 5. Racoceanu S, Mendelowitz M , Suck A , et al : Digital capillary blood flow in clubbing. Ann Intern Med 75:933-5 , 1971 6. Wilson GM: Local circulatory changes associated with clubbing of the fingers and toes. Q JMed 21:201-4,1952 7 . Mendelowitz M, Leslie A: Experimental simulation in dogs of cyanosis and hypertrophic osteoarthropathy which are associated with congenital heart disease. Am Heart J 24:141-52, 1942 8. Bigler FC: The morphology of clubbing . Am J Pat hoi 34:237, 1958 9 . Cross KW , Wilson GM: Circulatory changes associated with an aneurysm of the axillary artery and clubbing of the fingers. Clin Sci 9:59-69, 1950 10. Branwood W: Clubbing of the fingers, Edinb Med J 56: 105-20, 1949 II . Brooks B: Aneurysm of the axillary artery. S Clin North Am 10:741-55, 1930 12. Weslowski SA, Fries CC , Sawyer PN: The production and significance of turbulence in hemic systems. Trans Am Soc Artif Intern Organs 8: I 1-18, 1962 13 . Mauer EF: On the etiology of clubbing of the fingers . Am Heart J 34:852-9, 1947 14. Lovibond JL: Diagnosis of clubbed fingers. Lancet 1:363, 1938 15 . Just-Viera 10: Clubbed digits: An enigma. Arch Int Med 113: 122-8,1964
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Gold et al.
16. ChaIT R, Swenson PC: Clubbed fingers . Am J Roentgenol Radium Ther Nucl Med 55:325-30, 1946 17. Ponchon Y, Chelloul N, Roujeau 1: Contribution a l'etude anatomo-pathologique de I'Hippocratisme digital. Sem Hop Paris 45 :20, 1969 18. Hale RR , Burch GE: The arteriovenous anastomoses and blood vessels of the human finger: Morphological and functional aspects. Medicine 39:191-240, 1960
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19 . Abramson DI: Pathophysiology of the arteriovenous shunts in the extremeties. J Cardiovasc Surg Suppl: Congress of the International Cardiovascular Society, 1965 20 . Masson P: Le glomus neuromyo-arterial des regions taclilies el ses tumeurs. Lyon CI IR 21 :257, 1924
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