- Email: [email protected]
Martin-Gruber revisited
Vol. 17A, No. 1 January 1992
Carpal tunnel syndrome in children
5. McKusick VA. Heritable disorers of connective tissue. 4th ed. St. Louis: CV Mosby, 1972521-664. 6. Kaibara N, Katsuki I, Hotokebuchi T, Takagishi K, Kure T. Hurler-Scheie phenotype with parental consanguinity. Clin Orthop 1983;175:233-6. 7. Colavita N, Orazi C, Fileni A, Leone PC, Ricci R, Segni G. A further contribution to the knowledge of mucopolysaccharidosis I H/S compound: presentation of two cases and review of the literature. Australas Radio1 1986;30:142-9. 8. Luderschmidt CH, Schill WB, Surg D, Von Figura K, Hubner G, Pongratz D. Mucopolysaccharidose I-S (Morbus Scheie) Dtsch Med Wochenschr 1979; 104: 1482-7. 9. Pronicka E, Tylki-Szymanska A, Kwast 0, Chmielik J. Maciejko D, Cedro A. Carpal tunnel syndrome in children with mucopolysaccharidoses: needs for surgical tendons and median nerve release. J Ment Delic Res 1988;32:7982.
must be assessed preoperatively by an experienced anesthetist. Furthermore, the child’s general health and life expectancy must be appreciated before surgical carpal tunnel decompression is considered. Clinical improvement in the two children with hand pain and improvement in electrical studies of all four children reported in this study confirm the worth of surgical intervention in well-selected cases. REFERENCES Heinz C. Karpaltunnelsyndrom bei Kleinkindem. Handchirurgie 1981;13:272-4. Cuhadar M, Blaauw Cl. Carpal tunnel syndrome in childhood. Z Kinderchir 1983;38:330-2. Fisher RC, Homer RL, Wood VE. The hand in mucopolysaccharide disorders. Clin Orthop 1974;104:191-9. MacDougal B, Weeks PM, Wray RC Jr. Median nerve compression and trigger finger in mucopolysaccharidoses and related diseases. Plast Reconstr Surg 1977;59:260-3.
Martin-Gruber revisited A new classification system for Martin-Gruber connections is described. This comprises four types of connection that can theoretically exist and that differ by their source and destination. The world literature has been reexamined and the incidence of Martin-Gruber connections was found to be 17% overall. By the new classification, 60% are type I, sending motor branches from the median to the ulnar nerve to innervate “median” muscles; 35% are type II, sending motor branches from median to ulnar nerves to innervate “ulnar” muscles; 3% are type III, sending motor fibers from the ulnar to the median nerve to innervate “median” muscles; and 1% are type IV, sending motor fibers from the ulnar to the median nerve to innervate ‘blnar” muscles. (J HAND SURC 1992;17A:47-53.)
Stephen J. Leibovic, MD, and Hill Hastings II, MD, Indianapolis, Znd.
From the Indiana Center for Surgery and Rehabilitation of the Hand and Upper Extremity, Indianapolis. Ind. Received for publication Aug. 22, 1990; accepted in revised form Feb. 18, 1991. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Reprint requests: Stephen J. Leibovic, MD, 2911 Grove Ave., Richmond, VA 23221. 311129293
C
onnections between the median and nerves in the forearm were first described by Martin’ in 1763. Various forms of connection were found between the two nerves in Martin’s cadaver dissections. He described a branch between median and ulnar nerves that “sometimes runs under the pronator teres muscle.” He also described a connection between median and ulnar nerves in the palm, the “arcus volaris nervorum,” and described “an often ulnar
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48
Leibovic and Hastings
appearing anastomosing branch between median and ulnar nerves, distal to the flexor digitorum profundus branches, though it is not always present.” Martin made no comment on the content of these connecting branches, whether they were motor or sensory. He did not speculate on the final destination of their fibers. GrubeI-2 was apparently the next to mention these findings, in 1870. He dissected 212 forearms and found a connection between median and ulnar nerves in 38. The nerve branches generally coursed from the median nerve proximally to the ulnar nerve distally, although rarely there was a U-shaped connection between the two nerves. Gruber never described a branch coursing from the ulnar nerve proximally to the median nerve distally. This connection has since been called the MartinGruber anastomosis. We will refer to it as a “connection.” Despite its long history, its nature remains unclear. In 1763 anatomists had the ability only to identify and describe the crossing nerve fibers. The connection was described as going “from” the median nerve “to” the ulnar nerve. Such directionality referred to the apparent direction of the fibers; if a branch was noted to course from the median nerve proximally to the ulnar nerve distally, it was assumed to be efferent, coming from the median nerve and sending fibers to the ulnar nerve. Yet nerves such as the ansa cervicalis demonstrate that direction of the electrical signal cannot always be inferred by the local course of the nerve; signals can travel in a direction that may appear backward from strictly gross anatomic considerations. 3*4 Furthermore, nerves have efferent and afferent fibers. One cannot define the source and destination of electrical signals if one does not know whether the fibers are afferent or efferent . Curtis’ recognized in 1886, “It is of great interest to define the physiologic situation of this anastomosis, but the exact physiologic situation remains poorly defined” [author’s translation]. Are connecting motor fibers destined for muscles normally innervated by the ulnar nerve or for muscles normally innervated by the median nerve? Are they fibers that normally travel in the ulnar or median nerves? These questions bear significantly on clinical diagnosis. Martin-Gruber connections are often proposed as causes of unusual motor losses from peripheral nerve lesions, and they are invoked as explanations for missed diagnoses in such lesions. Defining the pattern of innervation of these crossing fibers is a prerequisite to understanding the anatomy of peripheral nerve lesions whenever a MartinGruber connection may play a part. We have determined the possible nature of medianulnar communications in the forearm and hand and de-
The Journal of HAND SURGERY
scribe them by a new classification system. Theoretically, five possibilities exist for median-ulnar communications in the forearm. First, there is the usual situation: the median nerve innervates the abductor pollicis brevis (APB), the opponens pollicis (OP), the superficial head of the flexor pollicis brevis (FPB), and the radial two lumbricals, while the ulnar nerve innervates the hypothenar muscles, the adductor pollicis (AdP), the deep head of the flexor pollicis brevis, the interossei, and the remaining lumbricals. We have labeled the remaining possibilities Martin-Gruber types I to IV Evidence to date has indicated that MartinGruber connections carry only motor fibers.“-*’ We will therefore use “to” and “from” to refer to the source and destination of motor fibers or electrical signals in these nerves (Fig. 1). Type I is a branch coursing from the median nerve to the ulnar nerve in the forearm and continuing into the hand to innervate the thenar muscles (i.e., those normally innervated by the median nerve). These are median nerve fibers, just traveling on the ulnar nerve to the hand. In type Ia, these fibers innervate thenar muscles only, and in type Ib they innervate ulnar intrinsic as well as thenar muscles. Type II is a branch coursing from the median to the ulnar nerve in the forearm and continuing into the hand to innervate ulnar intrinsic muscles (i.e., interossei, adductor pollicis, deep head of the flexor pollicis brevis, ulnar two lumbricals, and the hypothenar muscles). These are ulnar nerve fibers traveling on the median nerve down to the forearm, where they return to the ulnar nerve. Type III is a branch coursing from the ulnar nerve to the median nerve in the forearm and continuing into the hand to innervate thenar muscles. These are median nerve fibers traveling on the ulnar nerve down to the forearm, where they return to the median nerve. Finally, type IV is a branch coursing from the ulnar nerve to the median nerve in the forearm and continuing into the hand to innervate ulnar intrinsic muscles. In type IVa, these fibers innervate ulnar intrinsic muscles only, while in type IVb they innervate ulnar intrinsic and thenar muscles. We must distinguish between median-to-ulnar nerve connections and anomalous muscle innervation. In median-to-ulnar connections, identifiable branches exist between the median and ulnar nerve trunks. With anomalous innervation, a muscle “normally” innervated by nerve A has instead motor fibers from nerve B coursing directly to its motor end plates without first joining the nerve A. For some time we have had the ability to identify the origin and destination of nerve fibers by techniques of
Vol. 17A, No. January 1992
Martin-Gruher
ULNAR
“MEDIAN
\
%SCLES” PE Lumbricals 1.2 FPB (superllclali
Abu
M
M
“ULNAR MUSCLES lnterossei AdP FPB (deep) Lumbricals 3.4 Hypothenar M
U
, “ULNAR MUSCLES”
“MEDIAN MUSCLES”
“ULNAR MUSCLES-
u
“ULNAR MUSCLES’
1 lb
M
U
U
\
I “MEDIAN MUSCLES
“ULNAR MUSCLES’
“ULNAR MUSCLES”
IVa
II
49
U
“MEDIAN MUSCI~ES”
‘la
I
“MEDIAN MUSCI.E.5”
M
U
“MEDIAN MUSCLES’
revisired
“MEDIAN MUSCLES
“ULNAR MUSC! ES”
IVb’
Fig. 1. The normal pattern of median and ulnar nerve innervation is shown above. Theoretically possible connections between the median and ulnar nerves in the forearm and hand are shown as types I to IV. In type Ia, a branch coursing from the median nerve to the ulnar nerve in the forearm travels with the ulnar nerve before returning to the thenar muscles in the hand. In type Ib the same branch sends innervation to both thenar (normally innervated by the median nerve) and intrinsic (normally innervated by the ulnar nerve) muscles. In type II a branch from the median to the ulnar nerve in the forearm terminates in the intrinsic muscles. In type III a branch from the ulnar to the
median nerve terminates in the thenar muscles. In type IVa, a branch from the ulnar to the median nerve terminates in the intrinsic muscles, and in type IVb the same branch terminates in the thenar and intrinsic muscles.
(See text for full explanation.)
electrophysiology and pharmaceutical nerve blockade that were not available to the anatomists of the nineteenth and eighteenth centuries. It is appropriate to reexamine the existing literature in light of these capabilities. Early writings on anatomy In early works on anatomy, connections were described from cadaver dissections, but physiology could not be investigated.
In the nineteenth and early twentieth centuries anatomists continued to follow the example of Martin and Gruber and described incidences of various forms of connection between the two nerves. Curtis,5 Thomsoq6 Thane,’ and Hirasawa* each described results of dissections, which were essentially in agreement (Fig. 2). They saw fibers coursing from the median nerve at the elbow or proximal forearm distally down the forearm to join the ulnar nerve. They sometimes saw a loop of fibers on the flexor digitorum profundus between the
The Journal 50
Leibovic
and Hastings
MEDJAN
ULNAR
of
HAND SURG”RY
ULNAR
MEDIAN
i\
ULNAR
MEDIAN
MEDIAN
ULNAR
q
A
C
B
Fig. 2. Anatomic arrangement of connections between median and ulnar nerves found by dissection by anatomists of the eighteenth to the early nineteenth centuries. It was not known at this time whether the fibers contained in these branches were motor or sensory. (After Hirasawa K. Arh Anat Inst Kaiserlichen Univ Kyoto A 1931;2: 135-40.)
Table I. Data from literature descriptions Reference 11 12 13 14 16 17 18 19 20 21 22 23 24 25
TOTALS
of Martin-Gruber
where incidence
is available
# Tvpe I
# T.vpe II
# Type Ill
f%J
f%j
f%bl
2 616 (100%) 13177 (17%) 33151 (65%) 7
?
Overall incidence Case report 6/41 (15%) 961656 (15%) 511150 (34%) 221108 (21%) Case report 15% 5165 (8%) Case report 16/63 (25%) Case report 5196 (5%) Case report Case report S-34% (average 17%)
connection
64/77t 18/51
(83%) (35%) ?
# Type IV 6)
7
1 I 515 (100%) 8113 (61%)
“all” (lOO%)*
113
1
(39%) 1 case Type III or IV 515 (lW%)$ 2 2
113 (60%)
66 (35%)
6 (7) (3%)
2 (I) (1%)
*Text states 100% Type II, but 1 case Type I, 1case Type IV described in text. tNinety-six cases of Martin-Gruber connection identified. Only 77 of these were investigated in sufficient detail to assign type. SOther cases cited: Anomalous distribution.
median and ulnar nerves. They saw branches from the anterior interosseous nerve coursing distally to the ulnar nerve, and on occasion a branch coursing from the ulnar nerve proximally to the median nerve distally in the forearm. None of these descriptions could be classified into the present system, however, since function could not be determined. Recent reports: Re-evaluation and classification We have reviewed recent literature concerning Martin-Gruber connections and have classified reported
findings according to our four-type classification systern. This allows comparisons to be made between studies, and the overall reported incidence of each type of connection can be found. In these reported cases, any connection from the median nerve to the ulnar nerve has been called a Martin-Gruber connection. Often it has been possible, by careful review of reported data, to infer the origin and destination of motor fibers and therefore assign findings to one of our four types (Table I). Cliffton’ described cases of “all median hand,” in
Vol. 17A, No. 1 January 1992
Martin-Gruber
MEDIAN
M
ULNAR
revisited
51
U
NORMAL 1 [ PATTERN /
r
I- 1 “MEDIAN MUSCLES” OP Abd PB Lumbrlcals 1,2 FPB (superfclal)
“ULNAR MUSCLES” lnterossei AdP FPB (deep) Lumbticals 3.4 Hypothenar
“ULNAR MUSCLES”
“MEDIAN MUSCLES”
“MEDIAN MUSCLEV
,_. _.
“ULNAR MUSCLES-
lb ~
u
M
L
./
i
“MEDIAN MUSCLES”
“ULNAR MUSCLES”
. “MEDIAN MUSCLES”
“ULNAR MUSCLES”
.+ “MEDIAN MUSCLES”
i “ULNAR MUSCLES”
i II
“MEDIAN MUSCLES”
‘ULNAR MUSCLES”
IVb
El
Indicates site where nerve interruption would be masked by noted Martin-Gruber type connections
Fig. 3. Clear boxes indicate sites where nerve interruption could be partly or completely masked by noted types of Martin-Gruber connections. The types are the same as shown in Fig. 1. In each
case, a lesion in the site shown would be undetectable by routine clinical tests if the Martin-Gruber innervation of the muscles indicated was complete.
which the ulnar nerve was transected but “ulnar intrinsits” remained functional in spite of anesthesia in the ulnar distribution, and cases of “all ulnar hand,” with continued function of the “median-innervated” muscles in spite of sectioning of the median nerve and anesthesia in the median distribution. Data in Cliffton’s article are insufficient to determine which type of connections existed in his sample. Marinacci”. ” described two cases of ulnar nerve lacerations with good residual interosseous function. He stimulated nerves intraoperatively and found what we interpret as type II connections. This was the first example of intraoperative stimulation to determine the destination of crossing fibers in the forearm. His findings were essentially in agreement with those of Man-
nerfelt,” who investigated Martin-Gruber connections with nerve blocks and found the overall incidence to be 15% (6/41 patients tested). All connections were what we classify as type II; in two patients branches went to the first dorsal interosseous (FDI) and AdP muscles only, in one to the FDI, in one to the AdP, in one to the FDI and abductor digiti quinti (AbDQ), and in one probably to the AbDQ, FDI, and AdP. Kimura et a1.,13 in a careful study using a collision technique and eiectromyograms, found evidence of Martin-Gruber connections in 96 of 656 arms tested (15%). This technique entails a somewhat more sophisticated measurement than simple electromyography (EMG), but it is quite specific in determining the destination of efferent motor fibers. Extrapolating from
52
The Journal of HAND SURGERY
Leibovic and Hastings
their data, one can estimate the incidence of each type by our classification system: 78 of 656 (12%) would be type Ib, 1.25 of 656 (0.2%) type Ia, and 16 of 656 (2.5%) type II, with no type III and no type IVb. (Noninteger incidence is due to extrapolation from smaller sample size. Only 77 of 96 hands with a Martin-Gruber connection were investigated in sufficient detail for us to assign type. Of these l/77 was type Ia.) Testing would not have shown the separate existence of type IVa. Streib and Sun’4s l5 investigated 150 patients with EMGs and found evidence of a connection in 5 1 (34%) arms. The connections were type Ib in 18 (12%) and type II in 33 (22%) by our classification. Streib and Sun cite the data of Wilbourn and Lambe@ as being in agreement with theirs. In fact, however, Wilbourn and Lambert16 found an incidence of Martin-Gruber connections in 21 of 108 limbs (20%), but there were insufficient data in their abstract for us to assign a type. In 1979 Streib” described a case of a patient studied by EMG who had what we consider a type III connection. He contrasted this with the “usual median to ulnar Martin-Gruber anastomosis.” From the data in his article, however, it is conceivable that the patient described actually had a type Ib connection; again, insufficient data are presented to rule this out. In his textbook Spinner’* states that the overall incidence of Martin-Gruber connection is 15% and that these are all what we consider type II, sending fibers to some or all of the FDI, AdP, AbDQ, and second and third DI muscles. He implies that the usual situation in the Martin-Gruber-innervated hand is that all muscles so supplied also (usually) receive innervation from another “normal” source, although on occasion the Martin-Gruber connection may be their sole source of innervation. Spinner states that “for the most part” Martin-Gruber connections carry motor fibers from the median nerve or its branches to the ulnar nerve. He then proceeds, however, to describe a cadaver dissection in which both a forearm median-to-ulnar communication and a communication from the ulnar to the median nerve in the hand existed (i.e., type Ia or Ib). He continues to describe, still in the section on MartinGruber connections, an “extremely rare” example of what we would classify as a type IV, ulnar-to-median connection. Iyer and Fenichel” found connections coursing from the median nerve to the ulnar nerve (type I) in 5 of 65 (8%) patients. Bergman et al.” described one case of nerve trauma investigated by EMG, which we interpret as a type I connection. Careful reading of the latter case reveals that the findings could also be explained by anomalous ulnar innervation of thenar muscles. Initial positive potentials in EMG tracings shown suggest that
volume-conducted potentials may have led to erroneous interpretation of data in this case. Iyer and Fenichel pointed out that connections from the median to the ulnar nerve in the forearm, which terminate in the thenar muscles (type Ia), may produce normal distal motor latencies measured from the proximal forearm to the thenar muscles in a patient with carpal tunnel syndrome; the motor signal may course down the ulnar nerve to the thenar muscles, avoiding a compressive lesion in the carpal canal. Gutmann” also called attention to the possiblity of normal median nerve motor conduction velocities in patients with carpal tunnel syndrome and MartinGruber connections. Using EMG criteria, he found evidence of connections in 16 of 63 (25%) patients. His text describes the destinations of the fibers as the muscles of the hand that are normally innervated by the ulnar nerve (i.e., type II), but his diagram shows a type I connection. The text goes on to suggest that in 61% of patients there is evidence of a connection that we interpret as type Ib. The evidence presented is more convincing for type II than for type I, as the compound motor action potential recorded from them-u muscles by stimulation of the ulnar nerve at the wrist is rather small in Gutmann’s cases. Convincing evidence of type III or type IV connections is found in two additional articles. Komar et a1.22 describe a case of traumatic laceration of the median nerve with retained motor strength in the opponens pollicis. Using EMG, they determined that fibers bound for the opponens pollicis originated in the ulnar nerve and crossed to the median nerve in the forearm (i.e., type III or IV Martin-Gtuber connections). Rosen23 examined 96 arms with EMG and found evidence of abnormal connections to opponens pollicis and abductor digiti quinti muscles, although there may have been anomalous innervation. However, in 5 arms (5%) he found evidence of a true ulnar-to-median (type III) connection. Brandsma et a1.24 described two cases of Hansen’s disease investigated by EMG, in which connections between median and ulnar nerves that terminated in the intrinsic muscles (type II) occurred in at least one of them. Van Tieghem et a1.25described two cases of ulnar nerve lesions at the elbow with retained function of the intrinsic muscles innervated by the ulnar nerve. While their data suggest a type II connection, there is insufficient evidence to substantiate this in one of their cases. Discussion There is no consensus in the literature on which type of communication constitutes a Martin-Gruber connection. In all documented occurrences of such connections
Vol. l7A, No. 1 January 1992
from the literature surveyed (Table I), the incidence of Martin-Gruber connections ranges from 5% to 34%. The average incidence is 17%. One hundred eightyseven cases of Martin-Gruber connections are described in sufficient detail to determine type and, of these, 113 (60%) are type I, 66 (35%) are type II, 6 (3%) are type III, and 2 ( 1%) are type IV. Clinical implications of the various types are different (Fig. 3). In a type Ia connection, a low median nerve lesion could be completely masked; a low median or high ulnar lesion would be masked in a type Ib connection. In type II a high ulnar lesion could be completely masked. In the rare type III a high median lesion may be missed, and in the even rarer type IV a low ulnar lesion (type IVa) or a low ulnar and high median (type IVb) lesion may be missed. All of these possibilities can be equally referred to as Martin-Gruber connections; these are simply any connections between the median and ulnar nerves in the forearm. By recognizing the existence of different types of connection, mistakes in diagnosis of peripheral nerve lesions in the forearm can be avoided. Special thanks are due K. Nicholas and Marianne Leibovic for their help with the translation of the works of Gruber, Hirasawa, and Komar et al. and Dr. Bert Vinnars for the translation of Martin’s tome.
REFERENCES 1. Martin R. Tal om Nervus allmanna Egenskaper i Manniskans Kropp. Stockholm: Lars Salvius, 1763. 2. Gruber W. Uber die Verbindung des Nervus medianus mit dem Nervus ulnaris am Unterarme des Menschen und der Saugethiere. Arch Anat Physiol 1870;37:50122. 3. Netter FH. CIBA collection of medical illustrations. Vol. I. Part 1. Nervous system. West Caldwell, N.J.: CIBA, 1983. 4. Crafts RC. Anatomy. 2nd ed. New York: John Wiley, 1979. 5. Curtis F. Recherches anatomiques sur l’anastomose du median et du cubital a l’avantbras. lnt Monatssctu Anat Physiol 1886;3:309-24. 6. Thomson A. Third annual report of the committee of collective investigation of the Anatomical Society of Great Britain and Ireland for the year 189 l- 1892. J Anat 1893;27:183-94. 7. Thane GD. The nerves. In: Schafer EA. Thane GD, eds. Quain’s anatomy. 10th ed. Vo13, Part II. London: Longmans, Green, 1895. 8. Hirasawa K. Untersuchungen tiber das periphere Nervensystem Plexus brachialis und die Nerven der oberen
Martin-Gruber revisited
9.
10. 11. 12.
13.
14.
15.
16.
17.
18. 19.
20.
21.
22.
23.
24. 25.
53
Extremitat. Arb Anat Inst Kaiserlichen Univ Kyoto A 1931;2:135-40. Cliffton EE. Unusual innervation of the intrinsic muscles of the hand by median and ulnar nerve. Surgery 1948;23:12-31. Marinacci AA. Diagnosis of all median hand. Bull Los Angeles Neurol Sot 1964;29:191-7. Marinacci AA. Diagnosis of all median hand. Electromyography 1964;4:85-91. Mannerfelt L. Studies on the hand in ulnar nerve paralysis: a clinical experimental investigation in normal and anomalous innervation. Acta Orthop Stand 1966;Suppl 87. Kimura J, Murphy MJ, Varda DJ. Electrophysiological study of anomalous innervation of intrinsic hand muscles. Arch Neurol 1976;33:842-4. Streib EW, Sun SF. Martin Gruber anastomosis: electromyographic studies. Part 1. Electromyogr Clin Neurophysiol 1983;23:261-70. Streib EW, Sun SF. Martin Gruber anastomosis: electromyographic studies. Part 2. Electromyogr Clin Neurophysiol 1983;23:271-85. Wilboum AJ, Lambert EH. The forearm median to ulnar nerve communication: electrodiagnostic aspects. Neurology 1976;26:368. Streib EW. Ulnar to median nerve anastomosis in the forearm: electromyographic studies. Neurology 1979; 29: 1533-7. Spinner M. Injuries to the major branches of peripheral nerves of the forearm. Philadelphia: WB Saunders, 1972. Iyer V, Fenichel GM. Normal median nerve proximal latency in carpal tunnel syndrome: a clue to coexisting Martin Gruber anastomosis. J Neurol Neurosurg Psychiatry 1976;39:449-52. Bergman FO, Blom SE, Stenstrom SJ. Radical excision of a fibrofatty proliferation of the median nerve. with no neurological loss symptoms. Plast Reconstr Surg 1970;46:375-80. Gutmann L. Median-ulnar nerve communications and carpal tunnel syndrome. J Neurol Neurosurg Psychiatry 1977;40:982-6. Komar J, Szegvari M, Gloviczky Z. Szanto A. Traumatischer Durchschnitt des N. medianus ohne komplette motorische parese: Martin-Grubersche Anastomose. Nervenarzt 1978;49:697-9. Rosen AD. Innervation of the hand: an electromyographic study. Electromyogr Clin Neurophysiol 1973;134:175-8. Brandsma JW, Birke JA, Sims DS. The Martin-Gruber innervated hand. J HAND SURG 1986;l lA:536-9. Van Tieghem J, Vandendriessche G, Vanhecke J. MartinGruber anastomosis: the explanation for late diagnosis of severe ulnar nerve lesions at the elbow. Electromyogr Clin Neurophysiol 1987;27: 13-8.
Carpal tunnel syndrome in children
5. McKusick VA. Heritable disorers of connective tissue. 4th ed. St. Louis: CV Mosby, 1972521-664. 6. Kaibara N, Katsuki I, Hotokebuchi T, Takagishi K, Kure T. Hurler-Scheie phenotype with parental consanguinity. Clin Orthop 1983;175:233-6. 7. Colavita N, Orazi C, Fileni A, Leone PC, Ricci R, Segni G. A further contribution to the knowledge of mucopolysaccharidosis I H/S compound: presentation of two cases and review of the literature. Australas Radio1 1986;30:142-9. 8. Luderschmidt CH, Schill WB, Surg D, Von Figura K, Hubner G, Pongratz D. Mucopolysaccharidose I-S (Morbus Scheie) Dtsch Med Wochenschr 1979; 104: 1482-7. 9. Pronicka E, Tylki-Szymanska A, Kwast 0, Chmielik J. Maciejko D, Cedro A. Carpal tunnel syndrome in children with mucopolysaccharidoses: needs for surgical tendons and median nerve release. J Ment Delic Res 1988;32:7982.
must be assessed preoperatively by an experienced anesthetist. Furthermore, the child’s general health and life expectancy must be appreciated before surgical carpal tunnel decompression is considered. Clinical improvement in the two children with hand pain and improvement in electrical studies of all four children reported in this study confirm the worth of surgical intervention in well-selected cases. REFERENCES Heinz C. Karpaltunnelsyndrom bei Kleinkindem. Handchirurgie 1981;13:272-4. Cuhadar M, Blaauw Cl. Carpal tunnel syndrome in childhood. Z Kinderchir 1983;38:330-2. Fisher RC, Homer RL, Wood VE. The hand in mucopolysaccharide disorders. Clin Orthop 1974;104:191-9. MacDougal B, Weeks PM, Wray RC Jr. Median nerve compression and trigger finger in mucopolysaccharidoses and related diseases. Plast Reconstr Surg 1977;59:260-3.
Martin-Gruber revisited A new classification system for Martin-Gruber connections is described. This comprises four types of connection that can theoretically exist and that differ by their source and destination. The world literature has been reexamined and the incidence of Martin-Gruber connections was found to be 17% overall. By the new classification, 60% are type I, sending motor branches from the median to the ulnar nerve to innervate “median” muscles; 35% are type II, sending motor branches from median to ulnar nerves to innervate “ulnar” muscles; 3% are type III, sending motor fibers from the ulnar to the median nerve to innervate “median” muscles; and 1% are type IV, sending motor fibers from the ulnar to the median nerve to innervate ‘blnar” muscles. (J HAND SURC 1992;17A:47-53.)
Stephen J. Leibovic, MD, and Hill Hastings II, MD, Indianapolis, Znd.
From the Indiana Center for Surgery and Rehabilitation of the Hand and Upper Extremity, Indianapolis. Ind. Received for publication Aug. 22, 1990; accepted in revised form Feb. 18, 1991. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Reprint requests: Stephen J. Leibovic, MD, 2911 Grove Ave., Richmond, VA 23221. 311129293
C
onnections between the median and nerves in the forearm were first described by Martin’ in 1763. Various forms of connection were found between the two nerves in Martin’s cadaver dissections. He described a branch between median and ulnar nerves that “sometimes runs under the pronator teres muscle.” He also described a connection between median and ulnar nerves in the palm, the “arcus volaris nervorum,” and described “an often ulnar
THE JOURNAL OF HAND SURGERY
47
48
Leibovic and Hastings
appearing anastomosing branch between median and ulnar nerves, distal to the flexor digitorum profundus branches, though it is not always present.” Martin made no comment on the content of these connecting branches, whether they were motor or sensory. He did not speculate on the final destination of their fibers. GrubeI-2 was apparently the next to mention these findings, in 1870. He dissected 212 forearms and found a connection between median and ulnar nerves in 38. The nerve branches generally coursed from the median nerve proximally to the ulnar nerve distally, although rarely there was a U-shaped connection between the two nerves. Gruber never described a branch coursing from the ulnar nerve proximally to the median nerve distally. This connection has since been called the MartinGruber anastomosis. We will refer to it as a “connection.” Despite its long history, its nature remains unclear. In 1763 anatomists had the ability only to identify and describe the crossing nerve fibers. The connection was described as going “from” the median nerve “to” the ulnar nerve. Such directionality referred to the apparent direction of the fibers; if a branch was noted to course from the median nerve proximally to the ulnar nerve distally, it was assumed to be efferent, coming from the median nerve and sending fibers to the ulnar nerve. Yet nerves such as the ansa cervicalis demonstrate that direction of the electrical signal cannot always be inferred by the local course of the nerve; signals can travel in a direction that may appear backward from strictly gross anatomic considerations. 3*4 Furthermore, nerves have efferent and afferent fibers. One cannot define the source and destination of electrical signals if one does not know whether the fibers are afferent or efferent . Curtis’ recognized in 1886, “It is of great interest to define the physiologic situation of this anastomosis, but the exact physiologic situation remains poorly defined” [author’s translation]. Are connecting motor fibers destined for muscles normally innervated by the ulnar nerve or for muscles normally innervated by the median nerve? Are they fibers that normally travel in the ulnar or median nerves? These questions bear significantly on clinical diagnosis. Martin-Gruber connections are often proposed as causes of unusual motor losses from peripheral nerve lesions, and they are invoked as explanations for missed diagnoses in such lesions. Defining the pattern of innervation of these crossing fibers is a prerequisite to understanding the anatomy of peripheral nerve lesions whenever a MartinGruber connection may play a part. We have determined the possible nature of medianulnar communications in the forearm and hand and de-
The Journal of HAND SURGERY
scribe them by a new classification system. Theoretically, five possibilities exist for median-ulnar communications in the forearm. First, there is the usual situation: the median nerve innervates the abductor pollicis brevis (APB), the opponens pollicis (OP), the superficial head of the flexor pollicis brevis (FPB), and the radial two lumbricals, while the ulnar nerve innervates the hypothenar muscles, the adductor pollicis (AdP), the deep head of the flexor pollicis brevis, the interossei, and the remaining lumbricals. We have labeled the remaining possibilities Martin-Gruber types I to IV Evidence to date has indicated that MartinGruber connections carry only motor fibers.“-*’ We will therefore use “to” and “from” to refer to the source and destination of motor fibers or electrical signals in these nerves (Fig. 1). Type I is a branch coursing from the median nerve to the ulnar nerve in the forearm and continuing into the hand to innervate the thenar muscles (i.e., those normally innervated by the median nerve). These are median nerve fibers, just traveling on the ulnar nerve to the hand. In type Ia, these fibers innervate thenar muscles only, and in type Ib they innervate ulnar intrinsic as well as thenar muscles. Type II is a branch coursing from the median to the ulnar nerve in the forearm and continuing into the hand to innervate ulnar intrinsic muscles (i.e., interossei, adductor pollicis, deep head of the flexor pollicis brevis, ulnar two lumbricals, and the hypothenar muscles). These are ulnar nerve fibers traveling on the median nerve down to the forearm, where they return to the ulnar nerve. Type III is a branch coursing from the ulnar nerve to the median nerve in the forearm and continuing into the hand to innervate thenar muscles. These are median nerve fibers traveling on the ulnar nerve down to the forearm, where they return to the median nerve. Finally, type IV is a branch coursing from the ulnar nerve to the median nerve in the forearm and continuing into the hand to innervate ulnar intrinsic muscles. In type IVa, these fibers innervate ulnar intrinsic muscles only, while in type IVb they innervate ulnar intrinsic and thenar muscles. We must distinguish between median-to-ulnar nerve connections and anomalous muscle innervation. In median-to-ulnar connections, identifiable branches exist between the median and ulnar nerve trunks. With anomalous innervation, a muscle “normally” innervated by nerve A has instead motor fibers from nerve B coursing directly to its motor end plates without first joining the nerve A. For some time we have had the ability to identify the origin and destination of nerve fibers by techniques of
Vol. 17A, No. January 1992
Martin-Gruher
ULNAR
“MEDIAN
\
%SCLES” PE Lumbricals 1.2 FPB (superllclali
Abu
M
M
“ULNAR MUSCLES lnterossei AdP FPB (deep) Lumbricals 3.4 Hypothenar M
U
, “ULNAR MUSCLES”
“MEDIAN MUSCLES”
“ULNAR MUSCLES-
u
“ULNAR MUSCLES’
1 lb
M
U
U
\
I “MEDIAN MUSCLES
“ULNAR MUSCLES’
“ULNAR MUSCLES”
IVa
II
49
U
“MEDIAN MUSCI~ES”
‘la
I
“MEDIAN MUSCI.E.5”
M
U
“MEDIAN MUSCLES’
revisired
“MEDIAN MUSCLES
“ULNAR MUSC! ES”
IVb’
Fig. 1. The normal pattern of median and ulnar nerve innervation is shown above. Theoretically possible connections between the median and ulnar nerves in the forearm and hand are shown as types I to IV. In type Ia, a branch coursing from the median nerve to the ulnar nerve in the forearm travels with the ulnar nerve before returning to the thenar muscles in the hand. In type Ib the same branch sends innervation to both thenar (normally innervated by the median nerve) and intrinsic (normally innervated by the ulnar nerve) muscles. In type II a branch from the median to the ulnar nerve in the forearm terminates in the intrinsic muscles. In type III a branch from the ulnar to the
median nerve terminates in the thenar muscles. In type IVa, a branch from the ulnar to the median nerve terminates in the intrinsic muscles, and in type IVb the same branch terminates in the thenar and intrinsic muscles.
(See text for full explanation.)
electrophysiology and pharmaceutical nerve blockade that were not available to the anatomists of the nineteenth and eighteenth centuries. It is appropriate to reexamine the existing literature in light of these capabilities. Early writings on anatomy In early works on anatomy, connections were described from cadaver dissections, but physiology could not be investigated.
In the nineteenth and early twentieth centuries anatomists continued to follow the example of Martin and Gruber and described incidences of various forms of connection between the two nerves. Curtis,5 Thomsoq6 Thane,’ and Hirasawa* each described results of dissections, which were essentially in agreement (Fig. 2). They saw fibers coursing from the median nerve at the elbow or proximal forearm distally down the forearm to join the ulnar nerve. They sometimes saw a loop of fibers on the flexor digitorum profundus between the
The Journal 50
Leibovic
and Hastings
MEDJAN
ULNAR
of
HAND SURG”RY
ULNAR
MEDIAN
i\
ULNAR
MEDIAN
MEDIAN
ULNAR
q
A
C
B
Fig. 2. Anatomic arrangement of connections between median and ulnar nerves found by dissection by anatomists of the eighteenth to the early nineteenth centuries. It was not known at this time whether the fibers contained in these branches were motor or sensory. (After Hirasawa K. Arh Anat Inst Kaiserlichen Univ Kyoto A 1931;2: 135-40.)
Table I. Data from literature descriptions Reference 11 12 13 14 16 17 18 19 20 21 22 23 24 25
TOTALS
of Martin-Gruber
where incidence
is available
# Tvpe I
# T.vpe II
# Type Ill
f%J
f%j
f%bl
2 616 (100%) 13177 (17%) 33151 (65%) 7
?
Overall incidence Case report 6/41 (15%) 961656 (15%) 511150 (34%) 221108 (21%) Case report 15% 5165 (8%) Case report 16/63 (25%) Case report 5196 (5%) Case report Case report S-34% (average 17%)
connection
64/77t 18/51
(83%) (35%) ?
# Type IV 6)
7
1 I 515 (100%) 8113 (61%)
“all” (lOO%)*
113
1
(39%) 1 case Type III or IV 515 (lW%)$ 2 2
113 (60%)
66 (35%)
6 (7) (3%)
2 (I) (1%)
*Text states 100% Type II, but 1 case Type I, 1case Type IV described in text. tNinety-six cases of Martin-Gruber connection identified. Only 77 of these were investigated in sufficient detail to assign type. SOther cases cited: Anomalous distribution.
median and ulnar nerves. They saw branches from the anterior interosseous nerve coursing distally to the ulnar nerve, and on occasion a branch coursing from the ulnar nerve proximally to the median nerve distally in the forearm. None of these descriptions could be classified into the present system, however, since function could not be determined. Recent reports: Re-evaluation and classification We have reviewed recent literature concerning Martin-Gruber connections and have classified reported
findings according to our four-type classification systern. This allows comparisons to be made between studies, and the overall reported incidence of each type of connection can be found. In these reported cases, any connection from the median nerve to the ulnar nerve has been called a Martin-Gruber connection. Often it has been possible, by careful review of reported data, to infer the origin and destination of motor fibers and therefore assign findings to one of our four types (Table I). Cliffton’ described cases of “all median hand,” in
Vol. 17A, No. 1 January 1992
Martin-Gruber
MEDIAN
M
ULNAR
revisited
51
U
NORMAL 1 [ PATTERN /
r
I- 1 “MEDIAN MUSCLES” OP Abd PB Lumbrlcals 1,2 FPB (superfclal)
“ULNAR MUSCLES” lnterossei AdP FPB (deep) Lumbticals 3.4 Hypothenar
“ULNAR MUSCLES”
“MEDIAN MUSCLES”
“MEDIAN MUSCLEV
,_. _.
“ULNAR MUSCLES-
lb ~
u
M
L
./
i
“MEDIAN MUSCLES”
“ULNAR MUSCLES”
. “MEDIAN MUSCLES”
“ULNAR MUSCLES”
.+ “MEDIAN MUSCLES”
i “ULNAR MUSCLES”
i II
“MEDIAN MUSCLES”
‘ULNAR MUSCLES”
IVb
El
Indicates site where nerve interruption would be masked by noted Martin-Gruber type connections
Fig. 3. Clear boxes indicate sites where nerve interruption could be partly or completely masked by noted types of Martin-Gruber connections. The types are the same as shown in Fig. 1. In each
case, a lesion in the site shown would be undetectable by routine clinical tests if the Martin-Gruber innervation of the muscles indicated was complete.
which the ulnar nerve was transected but “ulnar intrinsits” remained functional in spite of anesthesia in the ulnar distribution, and cases of “all ulnar hand,” with continued function of the “median-innervated” muscles in spite of sectioning of the median nerve and anesthesia in the median distribution. Data in Cliffton’s article are insufficient to determine which type of connections existed in his sample. Marinacci”. ” described two cases of ulnar nerve lacerations with good residual interosseous function. He stimulated nerves intraoperatively and found what we interpret as type II connections. This was the first example of intraoperative stimulation to determine the destination of crossing fibers in the forearm. His findings were essentially in agreement with those of Man-
nerfelt,” who investigated Martin-Gruber connections with nerve blocks and found the overall incidence to be 15% (6/41 patients tested). All connections were what we classify as type II; in two patients branches went to the first dorsal interosseous (FDI) and AdP muscles only, in one to the FDI, in one to the AdP, in one to the FDI and abductor digiti quinti (AbDQ), and in one probably to the AbDQ, FDI, and AdP. Kimura et a1.,13 in a careful study using a collision technique and eiectromyograms, found evidence of Martin-Gruber connections in 96 of 656 arms tested (15%). This technique entails a somewhat more sophisticated measurement than simple electromyography (EMG), but it is quite specific in determining the destination of efferent motor fibers. Extrapolating from
52
The Journal of HAND SURGERY
Leibovic and Hastings
their data, one can estimate the incidence of each type by our classification system: 78 of 656 (12%) would be type Ib, 1.25 of 656 (0.2%) type Ia, and 16 of 656 (2.5%) type II, with no type III and no type IVb. (Noninteger incidence is due to extrapolation from smaller sample size. Only 77 of 96 hands with a Martin-Gruber connection were investigated in sufficient detail for us to assign type. Of these l/77 was type Ia.) Testing would not have shown the separate existence of type IVa. Streib and Sun’4s l5 investigated 150 patients with EMGs and found evidence of a connection in 5 1 (34%) arms. The connections were type Ib in 18 (12%) and type II in 33 (22%) by our classification. Streib and Sun cite the data of Wilbourn and Lambe@ as being in agreement with theirs. In fact, however, Wilbourn and Lambert16 found an incidence of Martin-Gruber connections in 21 of 108 limbs (20%), but there were insufficient data in their abstract for us to assign a type. In 1979 Streib” described a case of a patient studied by EMG who had what we consider a type III connection. He contrasted this with the “usual median to ulnar Martin-Gruber anastomosis.” From the data in his article, however, it is conceivable that the patient described actually had a type Ib connection; again, insufficient data are presented to rule this out. In his textbook Spinner’* states that the overall incidence of Martin-Gruber connection is 15% and that these are all what we consider type II, sending fibers to some or all of the FDI, AdP, AbDQ, and second and third DI muscles. He implies that the usual situation in the Martin-Gruber-innervated hand is that all muscles so supplied also (usually) receive innervation from another “normal” source, although on occasion the Martin-Gruber connection may be their sole source of innervation. Spinner states that “for the most part” Martin-Gruber connections carry motor fibers from the median nerve or its branches to the ulnar nerve. He then proceeds, however, to describe a cadaver dissection in which both a forearm median-to-ulnar communication and a communication from the ulnar to the median nerve in the hand existed (i.e., type Ia or Ib). He continues to describe, still in the section on MartinGruber connections, an “extremely rare” example of what we would classify as a type IV, ulnar-to-median connection. Iyer and Fenichel” found connections coursing from the median nerve to the ulnar nerve (type I) in 5 of 65 (8%) patients. Bergman et al.” described one case of nerve trauma investigated by EMG, which we interpret as a type I connection. Careful reading of the latter case reveals that the findings could also be explained by anomalous ulnar innervation of thenar muscles. Initial positive potentials in EMG tracings shown suggest that
volume-conducted potentials may have led to erroneous interpretation of data in this case. Iyer and Fenichel pointed out that connections from the median to the ulnar nerve in the forearm, which terminate in the thenar muscles (type Ia), may produce normal distal motor latencies measured from the proximal forearm to the thenar muscles in a patient with carpal tunnel syndrome; the motor signal may course down the ulnar nerve to the thenar muscles, avoiding a compressive lesion in the carpal canal. Gutmann” also called attention to the possiblity of normal median nerve motor conduction velocities in patients with carpal tunnel syndrome and MartinGruber connections. Using EMG criteria, he found evidence of connections in 16 of 63 (25%) patients. His text describes the destinations of the fibers as the muscles of the hand that are normally innervated by the ulnar nerve (i.e., type II), but his diagram shows a type I connection. The text goes on to suggest that in 61% of patients there is evidence of a connection that we interpret as type Ib. The evidence presented is more convincing for type II than for type I, as the compound motor action potential recorded from them-u muscles by stimulation of the ulnar nerve at the wrist is rather small in Gutmann’s cases. Convincing evidence of type III or type IV connections is found in two additional articles. Komar et a1.22 describe a case of traumatic laceration of the median nerve with retained motor strength in the opponens pollicis. Using EMG, they determined that fibers bound for the opponens pollicis originated in the ulnar nerve and crossed to the median nerve in the forearm (i.e., type III or IV Martin-Gtuber connections). Rosen23 examined 96 arms with EMG and found evidence of abnormal connections to opponens pollicis and abductor digiti quinti muscles, although there may have been anomalous innervation. However, in 5 arms (5%) he found evidence of a true ulnar-to-median (type III) connection. Brandsma et a1.24 described two cases of Hansen’s disease investigated by EMG, in which connections between median and ulnar nerves that terminated in the intrinsic muscles (type II) occurred in at least one of them. Van Tieghem et a1.25described two cases of ulnar nerve lesions at the elbow with retained function of the intrinsic muscles innervated by the ulnar nerve. While their data suggest a type II connection, there is insufficient evidence to substantiate this in one of their cases. Discussion There is no consensus in the literature on which type of communication constitutes a Martin-Gruber connection. In all documented occurrences of such connections
Vol. l7A, No. 1 January 1992
from the literature surveyed (Table I), the incidence of Martin-Gruber connections ranges from 5% to 34%. The average incidence is 17%. One hundred eightyseven cases of Martin-Gruber connections are described in sufficient detail to determine type and, of these, 113 (60%) are type I, 66 (35%) are type II, 6 (3%) are type III, and 2 ( 1%) are type IV. Clinical implications of the various types are different (Fig. 3). In a type Ia connection, a low median nerve lesion could be completely masked; a low median or high ulnar lesion would be masked in a type Ib connection. In type II a high ulnar lesion could be completely masked. In the rare type III a high median lesion may be missed, and in the even rarer type IV a low ulnar lesion (type IVa) or a low ulnar and high median (type IVb) lesion may be missed. All of these possibilities can be equally referred to as Martin-Gruber connections; these are simply any connections between the median and ulnar nerves in the forearm. By recognizing the existence of different types of connection, mistakes in diagnosis of peripheral nerve lesions in the forearm can be avoided. Special thanks are due K. Nicholas and Marianne Leibovic for their help with the translation of the works of Gruber, Hirasawa, and Komar et al. and Dr. Bert Vinnars for the translation of Martin’s tome.
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Extremitat. Arb Anat Inst Kaiserlichen Univ Kyoto A 1931;2:135-40. Cliffton EE. Unusual innervation of the intrinsic muscles of the hand by median and ulnar nerve. Surgery 1948;23:12-31. Marinacci AA. Diagnosis of all median hand. Bull Los Angeles Neurol Sot 1964;29:191-7. Marinacci AA. Diagnosis of all median hand. Electromyography 1964;4:85-91. Mannerfelt L. Studies on the hand in ulnar nerve paralysis: a clinical experimental investigation in normal and anomalous innervation. Acta Orthop Stand 1966;Suppl 87. Kimura J, Murphy MJ, Varda DJ. Electrophysiological study of anomalous innervation of intrinsic hand muscles. Arch Neurol 1976;33:842-4. Streib EW, Sun SF. Martin Gruber anastomosis: electromyographic studies. Part 1. Electromyogr Clin Neurophysiol 1983;23:261-70. Streib EW, Sun SF. Martin Gruber anastomosis: electromyographic studies. Part 2. Electromyogr Clin Neurophysiol 1983;23:271-85. Wilboum AJ, Lambert EH. The forearm median to ulnar nerve communication: electrodiagnostic aspects. Neurology 1976;26:368. Streib EW. Ulnar to median nerve anastomosis in the forearm: electromyographic studies. Neurology 1979; 29: 1533-7. Spinner M. Injuries to the major branches of peripheral nerves of the forearm. Philadelphia: WB Saunders, 1972. Iyer V, Fenichel GM. Normal median nerve proximal latency in carpal tunnel syndrome: a clue to coexisting Martin Gruber anastomosis. J Neurol Neurosurg Psychiatry 1976;39:449-52. Bergman FO, Blom SE, Stenstrom SJ. Radical excision of a fibrofatty proliferation of the median nerve. with no neurological loss symptoms. Plast Reconstr Surg 1970;46:375-80. Gutmann L. Median-ulnar nerve communications and carpal tunnel syndrome. J Neurol Neurosurg Psychiatry 1977;40:982-6. Komar J, Szegvari M, Gloviczky Z. Szanto A. Traumatischer Durchschnitt des N. medianus ohne komplette motorische parese: Martin-Grubersche Anastomose. Nervenarzt 1978;49:697-9. Rosen AD. Innervation of the hand: an electromyographic study. Electromyogr Clin Neurophysiol 1973;134:175-8. Brandsma JW, Birke JA, Sims DS. The Martin-Gruber innervated hand. J HAND SURG 1986;l lA:536-9. Van Tieghem J, Vandendriessche G, Vanhecke J. MartinGruber anastomosis: the explanation for late diagnosis of severe ulnar nerve lesions at the elbow. Electromyogr Clin Neurophysiol 1987;27: 13-8.