CM. Barone, D.E Jimenez, and A. Frempog-Bodeau
BLOOD-FLOW MEASUREMENTS OF INJURED PERIPHERAL NERVES BY LASER DOPPLER FLOWMETRY Downloaded by: Universite de Sherbrooke. Copyrighted material.
ABSTRACT The effects of injury on peripheral nerve blood flow were studied, using a Laserflo® blood perfusion monitor. A total of 11 nerves were studied, five normal and six injured nerves in four patients. Two of the patients had lacerating brachial plexus injuries, and two other patients had compressive neuropathies of their ulnar nerves at the elbow. All of the readings were taken intraoperatively while the patients were undergoing exploration and repair under general anesthesia. Measurements of the damaged nerves were taken serially from the site of injury proximally and distally, by approximating a flexible metric ruler to the dorsal aspect of the nerve along the same axis. In the acutely lacerated injured nerves (3 to 7 days), the measurements were taken at 1, 5,10, and 20 mm. The maximal amount of retraction in any of the nerves was 1 cm; thus, the overall architecture of the nerves was maintained. In the compressed nerves, measurements were taken at 1, 2 and 3 cm proximal and distal to the medial epicondyle. Measurement of normal undamaged nerves was performed at six different sites along the same axis of the nerve. The averaged results indicate that the normal blood flow ranged from 47 ml/100 g/min to 63 ml/100 g/min, with a mean of 56 ml/100 g/min. In the injured nerves, blood flow was most depressed at sites closest to the laceration, and increased consistently and progressively at sites distant from the injury in both directions. Proximally, blood flow was decreased between 64.2 percent and 81.9 percent at 1 mm; between 37.5 percent and 56.4 percent at 5 mm; between 27.0 percent and 50.3 percent at 10 mm; and between 6.6 percent and 43.4 percent at 20 mm. Distally, blood flow was decreased between 55.5 percent and 86.0 percent at 1 mm; between 24.4 percent and 61.9 percent at 5 mm; between 10.7 percent and 37.5 percent at 10 mm; and between 10.7 percent and 43.7 percent at 20 mm in the acutely injured nerves. In the nerves damaged by chronic compression, the blood flow decreased between 62.6 percent and 65.1 percent at 1 cm; between 58.0 percent and 59.4 percent at 2 cm; and to 43.7 percent at 3 cm proximally. In the distal areas, the decrease in blood flow was found to be between 74.2 percent and 39.8 percent at 1 cm; between 62.5 percent and 24.1 percent at 2 cm; and to 46.5 percent at 3 cm. The data were analyzed using ANOVA and post-hoc analysis. These preliminary findings indicate that, in addition to the actual penetrating injury, there are marked changes in the regional blood flow of injured nerves. There is a marked reduction in blood flow at sites near the penetrating injury. There is also a marked decrease in peripheral nerve blood flow at the site of compression in the ulnar nerves, with progressive increase in both directions. However, due to the anatomic arrangement of peripheral nerve vasculature, the changes noted in peripheral blood flow cause only regional damage and ischemia, and there is progressive normalization in both proximal and distal directions. This constitutes the first report of intraoperative measurement of peripheral nerve blood flow in humans. Laser Doppler flowmetry may become a useful adjunct in the management of peripheral nerve injuries. For a peripheral nerve to maintain normal physiologic function adequately, two essential conditions must be met. There must be 1) an intact connection with the cell body; and 2) a constant and sufficient supply of oxygen and nutrients via its intraneural vas-
cular network. An injury to the nerve may have a detrimental effect on one or both of these conditions. Following transection of a nerve, there is loss of electrical excitability distal to the injury site within 3 to 8 days. Complete ischemia causes rapid deterioration of nerve
Departments of Plastic Surgery and Neurosurgery, Temple University Health Science Center, Philadelphia, PA Materials in this paper were presented at the 60th Annual Scientific Meeting of the American Society of Plastic and Reconstructive Surgeons, Seattle, WA, September, 1991 Reprint requests-. Dr. Barone, Section of Plastic Surgery, University of Missouri, 1 Hospital Drive, Columbia, MO 65212 Accepted for publication February 25, 1992 Copyright © 1992 by Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, NY 10016. All rights reserved.
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function within 30 to 90 min.1'2 The effects of different types of trauma on peripheral nerve blood flow are of great interest to surgeons who deal with this kind of injury. A relatively small number of experimental studies have been performed which examine this subject, and most of these have been done on animals.3-8 Until the development of Doppler flowmetry,9 methods for determining the regional blood flow of peripheral nerves have been cumbersome, complex, invasive, and damaging to the nerve. 3410 This study utilizes the new technology to study, intraoperatively, the acute and late effects of penetrating trauma and compressive effects on peripheral nerve blood flow.
JULY 1992
The patient population consisted of two patients who had suffered sharp lacerating injuries (one male and one female) and two patients (one male and one female) who had ulnar nerve compression at the elbow. The analyzed damaged nerves were the following: posterior cord, suprascapular nerve, Tl, axillary nerve, and ulnar nerves. The normal nerves included C5, C7, C8, medial cord, and median nerve. The Tl and suprascapular nerves were studied 3 days post-injury; the posterior cord and axillary nerve 7 days post-injury. Patients with ulnar nerve compression were symptomatic between 8 and 14 months. The results of the blood flow measurements are given in units of ml/100 g of tissue/min.
MATERIALS AND METHODS
320
Serial blood-flow measurement at six different sites of normal nerves during exploration revealed that blood flow in these nerves ranged from 47 to 63 ml/100 g/min. Averaging all of these readings, a normal mean blood flow was 56 ml/100 g/min. This is the value that was used to compare all of the other abnormal values. Flow in the injured nerves was measured at selected intervals, and the results of the averaged values are depicted in Figures 2 to 7. These graphs show mean blood flow for each nerve, as well as the range of all ten readings. The maximal amount of blood-flow decrease was noted at sites closest to the level of injury. Table 1 presents the average amount of percent change in blood flow from a normal mean of 56 ml/100 g/min. Some areas of hyperemia were found at 5 mm and 10 mm, but these were not consistent in all nerves. The changes in blood flow were found to be statistically significant (p = 0.01), using ANOVA and post-hoc anal-
Figure 1. Intraoperative set-up showing the laser Doppler probe held in place over a peripheral nerve by a Greenberg self-retaining retractor.
Downloaded by: Universite de Sherbrooke. Copyrighted material.
RESULTS A TSI laser blood flow perfusion monitor (Model BPM 403ATSI, St. Paul, MN) was used for this study. A description of the theory, physics, and practical aspects of this technology has been eloquently provided by various authors.11-13 All the patients were induced under general anesthesia, using a combination of Forane, nitrous oxide, and narcotics. Muscle relaxants were reversed prior to nerve stimulation and flow measurements. In order to minimize result variability secondary to probe motion, the sensor was placed in a Greenberg self-retaining retractor system (Fig. 1). The tip of the probe [Needle probe #p433 (1.4 x 180 mm)) was placed 1 to 2 mm above a "macroscopic" avascular area, i.e., away from large prominent vessels. Ten readings were taken from each sample area. Sampling time averaged 30 sec after the readings were stabilized. All readings were recorded on thermographic paper for subsequent analysis.
BLOOD-FLOW MEASUREMENTS/BARONE, JIMENEZ, FREMPOG-BODEAU
60 50
nl/IOOg.-mln
20
injury site
10
20
20 10
distal
proximal
10
proximal
50
10
1
20 distal
distance in millimeters
distance in millimeters
Figure 2. Range of measurements in a lacerated posterior cord (n = 10) and mean values.
BLOOD FLOW ml/iOOg/mln
injury site
Figure 5. Range of measurements in a lacerated suprascapular nerve (n = 10) and mean values.
BLOOO FLOW 50
ml/100g/mln
40
60 50 40
injury site
20 10
10
proximal
20
Injury site proximal
distal
Figure 6. Range of measurements in compressed ulnar nerve I (n = 10) and mean values.
BLOOD FLOW
60
BLOOD FLOW
nl/100g/mln
50
ml/1 OO9'ml n
20 10
1
injury site
proximal
10
50
20 distal
distance in millimeters
Figure 4. Range of measurements in a lacerated Tl nerve (n = 10) and mean values.
ysis Fisher's protected LSD. All ten readings per sample area per patient were used for the ANOVA analysis. Although the differences in blood flow were not statistically significant between the injury site and the adjacent points, the differences were significant when compared to normal values and to those from the most distant sites.
distal
distance in centimeters
distance in millimeters
Figure 3. Range of measurements in a lacerated axillary nerve (n = 10) and mean values.
1
3
2
1
injury site
1
proximal
2 distal
distance in centimeters
Figure 7. Range of measurements in compressed ulnar nerve 2 (n = 10) and mean values.
DISCUSSION The first study dealing exclusively with the blood supply to peripheral nerves was published in 1768 by Isenflamm and Doerffler.14 Their method of study was the injection and perfusion of the vessels with colored 321
Downloaded by: Universite de Sherbrooke. Copyrighted material.
ml/1009/mln
Table I.
Change in Blood Flow (%) Tl
Suprascapular N.
-68.0%
-43.3% -37.5% -37.5% -64.2%
-6.6% -27.0% -50.0% -68.7%
-50.3% -56.4% -81.9%
-55.5% -37.5% -10.7% -10.7%
-64.0% -55.0% -37.5% -43.7%
-86.0% -24.4% + 2.6% + 7.4%
-60.7% -61.9% -33.9% +9.4%
Posterior Cord Proximal 20 mm 10 mm 5 mm 1 mm Injury site 1 mm 5 mm 10 mm 20 mm Distal
Proximal 3 cm 2 cm 1 cm Injury site 1 cm 2 cm 3 cm Distal
322
+ 7.1% + 1.2% -50.8%
Axillary N.
Xilnar Nerve 1
Dinar Nerve 2
-43.7% -58.0% -62.6% -67.8% -74.2% -63.5% -46.5%
-20.0% -59.4% -65.1% -66.9% -39.8% -24.1% -8.9%
wax. They were successful in identifying a network of vessels surrounding the nerves. A century later, Ranvier in 1878, and Quenu and Lejars15 in the late 1800's, gave a greater and more detailed description of these vessels. A comprehensive and thorough characterization of the human nervous vasculature has been defined by Sunderland,16 Smith,17 Lundborg,18 and others in recent years. All these studies have demonstrated that peripheral nerves are very well-vascularized structures. Their blood supply is by means of two independent, but integrated, microcirculatory systems. The extrinsic system is composed of segmentally-arranged vessels of various numbers and sizes. The origin of these vessels is from nearby arteries and periosteal vessels. Particular to this system are vessels that exhibit tortuosity and convolution on the nerve's surface, giving the nerves marked flexibility and stretching capabilities {e.g., around joints). The intrinsic system is comprised of epineural, perineurial, and endoneurial plexi, along with their anastomosing vessels with the extrinsic system. There are many arterioles and venules that extend mostly longitudinally along the nerve. These vessels anastomose richly with the endo- and perineurial systems. The overall arrangement of the vasculature is fundamentally segmental. The effects of trauma on peripheral nerves have been studied extensively by various authors.19-21 The results and consequences of dissection, stretching, compression, laceration, radiation, and other trauma have been described in some detail. 2223 It is clear that ischemia and blood-supply compromise play an important role in the final outcome of an injury to the nerve. Experimental evidence shows that nerves are
JULY 1992
well-vascularized structures, with considerable reserve capacity secondary to the segmental nature of their microcirculatory milieu. This reserve is diminished when the nerve is traumatized. Ogata4 looked at the effects of compression of the sciatic nerves in rabbits. He found that intraneural blood flow was completely stopped in all animals at compressions of 70 mmHg; 50 percent of the nerves had blood-flow restoration with compressions of 50 mmHg. With 30 mmHg compression, the blood flow was decreased by 73 percent, but all the nerves had full restoration of flow upon decompression.4 Lundborg reported that a 15 percent stretch of the rabbit tibial nerve produced complete ischemia of the nerve, with subsequent electrical shut down.3 It has been clearly demonstrated that ischemia of a nerve leads to perineurial scar formation, which produces obstruction of axonal sprouts and subsequent disturbances in nerve function.24 The studies of nerve compression and blood flow have all been done in animals, and no study has so far been done in humans to corroborate these findings. Although only two patients were studied with compression neuropathy, the affected nerves showed marked and significant decreases in blood flow at the sites of compression (-67.8 percent and —66.9 percent). This provides the first evidence that compression of a human peripheral nerve causes depression in its blood flow at the affected site. The amount of pressure could not be quantitatively ascertained and is unknown, but resolution of symptoms after release indicates that this decrease was not irreversible. In the case of the lacerated nerves, it was also found that there were marked changes in the blood flow of those nerves. The decrease in flow was found not only at the site of injury, but also at some distance from it. The flow reached near normal levels at 15 to 20 mm from the laceration point. This seems to indicate that the injury extends beyond the laceration, and may have a significant effect in cases in which primary anastomosis or cable grafting are being considered.
CONCLUSIONS To study a nerve's blood flow prior to the introduction of laser Doppler flowmetry, previously required invasive and damaging procedures. This newer method has proven safe, noninvasive, and reliable. When measured against the (14C)Iodoantipyrine technique, 25 Xe washout,25 H2 clearance, and labelled microspheres,26 laser flowmetry has been found to give accurate readings and to have a high level of correlation with these time-proven techniques. Our preliminary results seem to corroborate physiologically the segmental pattern of blood distribution in human peripheral nerves. This new, "non-invasive," user-friendly, and relatively simple technology may have a place in the treat-
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JOURNAL OF RECONSTRUCTIVE MICROSURGERY/VOLUME 8, NUMBER 4
BLOOD-FLOW MEASUREMENTS/BARONE, JIMENEZ, FREMPOG-BODEAU
REFERENCES
13.
14. 15. 16. 17.
1. Eiken O, Nabseth DC, Mayer RF: Limb replantation. I. The technique and immediate results. Arch Surg 88:48, 1964 2. Eiken O, Nabseth DC, Mayer RF: Limb replantation. II. The pathological effects. Arch Surg 88:54, 1964 3. Lundborg G, Rydevyk B: Effects of stretching the tibial nerve of the rabbit. I Bone Joint Surg 55B:390, 1973 4. Ogata K, Naito M: Blood flow of peripheral nerves: Effects of dissection, stretching and compression. I Hand Surg 2B:10, 1985 5. Leffert RD, Seddon H: Infraclavicular plexus injuries. I Bone Joint Surg 47B:9, 1985 6. Liu CT, Benda CE, Lewey FH: Microvascular structure and function of the peripheral nerves. Arch Neurol Psych 59: 322, 1948 7. Lundborg G: Ischemic nerve injury. Scand J Plast Reconstr Surg Supp:16, 1970 8. Richard RL: Ischemic lesions of peripheral nerves. J Neurol Neurosurg Psych 14:76, 1951 9. Nilsson GE, Tenland T, Oberg PA: A new instrument for continuous measurements of tissue blood flow by light beating spectroscopy. Trans Biomed Eng 27:12, 1980 10. Smith OR, Kobrine AI, Rizzoli HU: Blood flow in peripheral nerves, normal and post severance flow rates. J Neurol Sci 33:341, 1977 11. Haumschild DS: Microvascular blood flow measurement by laser Doppler flowmetry. TSI Application Note, TSI Inc, 1986 12. Haberl RL, Heizer ML, Ellis EF: Laser Doppler assessment of
18. 19. 20.
21. 22
23 24. 25. 26.
brain microcirculation: Effect of local alterations. Heart Circ Physiol 25H1255, 1989 WinsorT, Haumschild DJ, Winsor DW, etai: Clinical application of laser Doppler flowmetry of measurement of cutaneous circulation in health and disease. Angio J Vase Dis 38:727, 1987 Isenflamm JF, Doerffler JF: Devasis Nervorum Enlangen, 1768 Quenu J, Lejars F: The arteries and veins of the nerves (Fr). Compt Rend Acad Sci 111:508, 1890 Sunderland S: Blood supply of the nerves of the upper limb in man. Arch Neurol Psych 53:91, 1945 Smith JW: Factors influencing nerve repair I. Blood supply of peripheral nerves. Arch Surg 93:335, 1966 Lundorg G: Structure and function of the intraneural microvessels as related to trauma, edema formation and nerve function. J Bone Joint Surg 57A:938, 1975 Bacsich P, Wyburn GM: The effects of interference with the blood supply on regeneration of peripheral nerves. J Anat 79:74, 1945 Kline DG, Hackett ER, Davis GD, Myers MB: Effects of mobilization on the blood supply and regeneration of injured nerves. J Surg Res 12:254, 1972 Haftek J: Stretch injury of peripheral nerves: Acute effects of stretching on rabbit nerve. I Bone Joint Surg 52B:354, 1970 Starkweather RJ, Neviaser RJ, Adams JP, Parsons DB: The effect of devascularization on the regeneration of lacerated peripheral nerves: An experimental study. I Hand Surg 3:163, 1978 RydevikB, Lundborg G, BaggeU: Effects of graded compression on intraneural blood flow, an in vivo study on rabbit tibial nerve. J Hand Surg 6:3, 1981 Millesi H, Meissl G, Berger A: The intrafascicular nerve grafting of the median nerve and ulnar nerve. J Bone Joint Surg 54A: 727, 1972 Engelheart M, Kristensen JK: Evaluation of cutaneous blood flow responses by l33xenon washout and laser Doppler flowmetry. I Invest Dermatol 80:12, 1983 Kvietys PR, Shepperd AP, Granger CD: H2 clearance and microsphere estimates of mucosal blood flow. Gl Liver Physiol 12:G221, 1985
Downloaded by: Universite de Sherbrooke. Copyrighted material.
ment of peripheral nerve injuries. Other possible areas of study include diseases affecting peripheral nerves, such as diabetic, neoplastic, and drug-induced neuropathies and traumatic nerve injuries sustained from crush and gun-shot wounds.
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BLOOD-FLOW MEASUREMENTS OF INJURED PERIPHERAL NERVES BY LASER DOPPLER FLOWMETRY Downloaded by: Universite de Sherbrooke. Copyrighted material.
ABSTRACT The effects of injury on peripheral nerve blood flow were studied, using a Laserflo® blood perfusion monitor. A total of 11 nerves were studied, five normal and six injured nerves in four patients. Two of the patients had lacerating brachial plexus injuries, and two other patients had compressive neuropathies of their ulnar nerves at the elbow. All of the readings were taken intraoperatively while the patients were undergoing exploration and repair under general anesthesia. Measurements of the damaged nerves were taken serially from the site of injury proximally and distally, by approximating a flexible metric ruler to the dorsal aspect of the nerve along the same axis. In the acutely lacerated injured nerves (3 to 7 days), the measurements were taken at 1, 5,10, and 20 mm. The maximal amount of retraction in any of the nerves was 1 cm; thus, the overall architecture of the nerves was maintained. In the compressed nerves, measurements were taken at 1, 2 and 3 cm proximal and distal to the medial epicondyle. Measurement of normal undamaged nerves was performed at six different sites along the same axis of the nerve. The averaged results indicate that the normal blood flow ranged from 47 ml/100 g/min to 63 ml/100 g/min, with a mean of 56 ml/100 g/min. In the injured nerves, blood flow was most depressed at sites closest to the laceration, and increased consistently and progressively at sites distant from the injury in both directions. Proximally, blood flow was decreased between 64.2 percent and 81.9 percent at 1 mm; between 37.5 percent and 56.4 percent at 5 mm; between 27.0 percent and 50.3 percent at 10 mm; and between 6.6 percent and 43.4 percent at 20 mm. Distally, blood flow was decreased between 55.5 percent and 86.0 percent at 1 mm; between 24.4 percent and 61.9 percent at 5 mm; between 10.7 percent and 37.5 percent at 10 mm; and between 10.7 percent and 43.7 percent at 20 mm in the acutely injured nerves. In the nerves damaged by chronic compression, the blood flow decreased between 62.6 percent and 65.1 percent at 1 cm; between 58.0 percent and 59.4 percent at 2 cm; and to 43.7 percent at 3 cm proximally. In the distal areas, the decrease in blood flow was found to be between 74.2 percent and 39.8 percent at 1 cm; between 62.5 percent and 24.1 percent at 2 cm; and to 46.5 percent at 3 cm. The data were analyzed using ANOVA and post-hoc analysis. These preliminary findings indicate that, in addition to the actual penetrating injury, there are marked changes in the regional blood flow of injured nerves. There is a marked reduction in blood flow at sites near the penetrating injury. There is also a marked decrease in peripheral nerve blood flow at the site of compression in the ulnar nerves, with progressive increase in both directions. However, due to the anatomic arrangement of peripheral nerve vasculature, the changes noted in peripheral blood flow cause only regional damage and ischemia, and there is progressive normalization in both proximal and distal directions. This constitutes the first report of intraoperative measurement of peripheral nerve blood flow in humans. Laser Doppler flowmetry may become a useful adjunct in the management of peripheral nerve injuries. For a peripheral nerve to maintain normal physiologic function adequately, two essential conditions must be met. There must be 1) an intact connection with the cell body; and 2) a constant and sufficient supply of oxygen and nutrients via its intraneural vas-
cular network. An injury to the nerve may have a detrimental effect on one or both of these conditions. Following transection of a nerve, there is loss of electrical excitability distal to the injury site within 3 to 8 days. Complete ischemia causes rapid deterioration of nerve
Departments of Plastic Surgery and Neurosurgery, Temple University Health Science Center, Philadelphia, PA Materials in this paper were presented at the 60th Annual Scientific Meeting of the American Society of Plastic and Reconstructive Surgeons, Seattle, WA, September, 1991 Reprint requests-. Dr. Barone, Section of Plastic Surgery, University of Missouri, 1 Hospital Drive, Columbia, MO 65212 Accepted for publication February 25, 1992 Copyright © 1992 by Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, NY 10016. All rights reserved.
319
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function within 30 to 90 min.1'2 The effects of different types of trauma on peripheral nerve blood flow are of great interest to surgeons who deal with this kind of injury. A relatively small number of experimental studies have been performed which examine this subject, and most of these have been done on animals.3-8 Until the development of Doppler flowmetry,9 methods for determining the regional blood flow of peripheral nerves have been cumbersome, complex, invasive, and damaging to the nerve. 3410 This study utilizes the new technology to study, intraoperatively, the acute and late effects of penetrating trauma and compressive effects on peripheral nerve blood flow.
JULY 1992
The patient population consisted of two patients who had suffered sharp lacerating injuries (one male and one female) and two patients (one male and one female) who had ulnar nerve compression at the elbow. The analyzed damaged nerves were the following: posterior cord, suprascapular nerve, Tl, axillary nerve, and ulnar nerves. The normal nerves included C5, C7, C8, medial cord, and median nerve. The Tl and suprascapular nerves were studied 3 days post-injury; the posterior cord and axillary nerve 7 days post-injury. Patients with ulnar nerve compression were symptomatic between 8 and 14 months. The results of the blood flow measurements are given in units of ml/100 g of tissue/min.
MATERIALS AND METHODS
320
Serial blood-flow measurement at six different sites of normal nerves during exploration revealed that blood flow in these nerves ranged from 47 to 63 ml/100 g/min. Averaging all of these readings, a normal mean blood flow was 56 ml/100 g/min. This is the value that was used to compare all of the other abnormal values. Flow in the injured nerves was measured at selected intervals, and the results of the averaged values are depicted in Figures 2 to 7. These graphs show mean blood flow for each nerve, as well as the range of all ten readings. The maximal amount of blood-flow decrease was noted at sites closest to the level of injury. Table 1 presents the average amount of percent change in blood flow from a normal mean of 56 ml/100 g/min. Some areas of hyperemia were found at 5 mm and 10 mm, but these were not consistent in all nerves. The changes in blood flow were found to be statistically significant (p = 0.01), using ANOVA and post-hoc anal-
Figure 1. Intraoperative set-up showing the laser Doppler probe held in place over a peripheral nerve by a Greenberg self-retaining retractor.
Downloaded by: Universite de Sherbrooke. Copyrighted material.
RESULTS A TSI laser blood flow perfusion monitor (Model BPM 403ATSI, St. Paul, MN) was used for this study. A description of the theory, physics, and practical aspects of this technology has been eloquently provided by various authors.11-13 All the patients were induced under general anesthesia, using a combination of Forane, nitrous oxide, and narcotics. Muscle relaxants were reversed prior to nerve stimulation and flow measurements. In order to minimize result variability secondary to probe motion, the sensor was placed in a Greenberg self-retaining retractor system (Fig. 1). The tip of the probe [Needle probe #p433 (1.4 x 180 mm)) was placed 1 to 2 mm above a "macroscopic" avascular area, i.e., away from large prominent vessels. Ten readings were taken from each sample area. Sampling time averaged 30 sec after the readings were stabilized. All readings were recorded on thermographic paper for subsequent analysis.
BLOOD-FLOW MEASUREMENTS/BARONE, JIMENEZ, FREMPOG-BODEAU
60 50
nl/IOOg.-mln
20
injury site
10
20
20 10
distal
proximal
10
proximal
50
10
1
20 distal
distance in millimeters
distance in millimeters
Figure 2. Range of measurements in a lacerated posterior cord (n = 10) and mean values.
BLOOD FLOW ml/iOOg/mln
injury site
Figure 5. Range of measurements in a lacerated suprascapular nerve (n = 10) and mean values.
BLOOO FLOW 50
ml/100g/mln
40
60 50 40
injury site
20 10
10
proximal
20
Injury site proximal
distal
Figure 6. Range of measurements in compressed ulnar nerve I (n = 10) and mean values.
BLOOD FLOW
60
BLOOD FLOW
nl/100g/mln
50
ml/1 OO9'ml n
20 10
1
injury site
proximal
10
50
20 distal
distance in millimeters
Figure 4. Range of measurements in a lacerated Tl nerve (n = 10) and mean values.
ysis Fisher's protected LSD. All ten readings per sample area per patient were used for the ANOVA analysis. Although the differences in blood flow were not statistically significant between the injury site and the adjacent points, the differences were significant when compared to normal values and to those from the most distant sites.
distal
distance in centimeters
distance in millimeters
Figure 3. Range of measurements in a lacerated axillary nerve (n = 10) and mean values.
1
3
2
1
injury site
1
proximal
2 distal
distance in centimeters
Figure 7. Range of measurements in compressed ulnar nerve 2 (n = 10) and mean values.
DISCUSSION The first study dealing exclusively with the blood supply to peripheral nerves was published in 1768 by Isenflamm and Doerffler.14 Their method of study was the injection and perfusion of the vessels with colored 321
Downloaded by: Universite de Sherbrooke. Copyrighted material.
ml/1009/mln
Table I.
Change in Blood Flow (%) Tl
Suprascapular N.
-68.0%
-43.3% -37.5% -37.5% -64.2%
-6.6% -27.0% -50.0% -68.7%
-50.3% -56.4% -81.9%
-55.5% -37.5% -10.7% -10.7%
-64.0% -55.0% -37.5% -43.7%
-86.0% -24.4% + 2.6% + 7.4%
-60.7% -61.9% -33.9% +9.4%
Posterior Cord Proximal 20 mm 10 mm 5 mm 1 mm Injury site 1 mm 5 mm 10 mm 20 mm Distal
Proximal 3 cm 2 cm 1 cm Injury site 1 cm 2 cm 3 cm Distal
322
+ 7.1% + 1.2% -50.8%
Axillary N.
Xilnar Nerve 1
Dinar Nerve 2
-43.7% -58.0% -62.6% -67.8% -74.2% -63.5% -46.5%
-20.0% -59.4% -65.1% -66.9% -39.8% -24.1% -8.9%
wax. They were successful in identifying a network of vessels surrounding the nerves. A century later, Ranvier in 1878, and Quenu and Lejars15 in the late 1800's, gave a greater and more detailed description of these vessels. A comprehensive and thorough characterization of the human nervous vasculature has been defined by Sunderland,16 Smith,17 Lundborg,18 and others in recent years. All these studies have demonstrated that peripheral nerves are very well-vascularized structures. Their blood supply is by means of two independent, but integrated, microcirculatory systems. The extrinsic system is composed of segmentally-arranged vessels of various numbers and sizes. The origin of these vessels is from nearby arteries and periosteal vessels. Particular to this system are vessels that exhibit tortuosity and convolution on the nerve's surface, giving the nerves marked flexibility and stretching capabilities {e.g., around joints). The intrinsic system is comprised of epineural, perineurial, and endoneurial plexi, along with their anastomosing vessels with the extrinsic system. There are many arterioles and venules that extend mostly longitudinally along the nerve. These vessels anastomose richly with the endo- and perineurial systems. The overall arrangement of the vasculature is fundamentally segmental. The effects of trauma on peripheral nerves have been studied extensively by various authors.19-21 The results and consequences of dissection, stretching, compression, laceration, radiation, and other trauma have been described in some detail. 2223 It is clear that ischemia and blood-supply compromise play an important role in the final outcome of an injury to the nerve. Experimental evidence shows that nerves are
JULY 1992
well-vascularized structures, with considerable reserve capacity secondary to the segmental nature of their microcirculatory milieu. This reserve is diminished when the nerve is traumatized. Ogata4 looked at the effects of compression of the sciatic nerves in rabbits. He found that intraneural blood flow was completely stopped in all animals at compressions of 70 mmHg; 50 percent of the nerves had blood-flow restoration with compressions of 50 mmHg. With 30 mmHg compression, the blood flow was decreased by 73 percent, but all the nerves had full restoration of flow upon decompression.4 Lundborg reported that a 15 percent stretch of the rabbit tibial nerve produced complete ischemia of the nerve, with subsequent electrical shut down.3 It has been clearly demonstrated that ischemia of a nerve leads to perineurial scar formation, which produces obstruction of axonal sprouts and subsequent disturbances in nerve function.24 The studies of nerve compression and blood flow have all been done in animals, and no study has so far been done in humans to corroborate these findings. Although only two patients were studied with compression neuropathy, the affected nerves showed marked and significant decreases in blood flow at the sites of compression (-67.8 percent and —66.9 percent). This provides the first evidence that compression of a human peripheral nerve causes depression in its blood flow at the affected site. The amount of pressure could not be quantitatively ascertained and is unknown, but resolution of symptoms after release indicates that this decrease was not irreversible. In the case of the lacerated nerves, it was also found that there were marked changes in the blood flow of those nerves. The decrease in flow was found not only at the site of injury, but also at some distance from it. The flow reached near normal levels at 15 to 20 mm from the laceration point. This seems to indicate that the injury extends beyond the laceration, and may have a significant effect in cases in which primary anastomosis or cable grafting are being considered.
CONCLUSIONS To study a nerve's blood flow prior to the introduction of laser Doppler flowmetry, previously required invasive and damaging procedures. This newer method has proven safe, noninvasive, and reliable. When measured against the (14C)Iodoantipyrine technique, 25 Xe washout,25 H2 clearance, and labelled microspheres,26 laser flowmetry has been found to give accurate readings and to have a high level of correlation with these time-proven techniques. Our preliminary results seem to corroborate physiologically the segmental pattern of blood distribution in human peripheral nerves. This new, "non-invasive," user-friendly, and relatively simple technology may have a place in the treat-
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JOURNAL OF RECONSTRUCTIVE MICROSURGERY/VOLUME 8, NUMBER 4
BLOOD-FLOW MEASUREMENTS/BARONE, JIMENEZ, FREMPOG-BODEAU
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ment of peripheral nerve injuries. Other possible areas of study include diseases affecting peripheral nerves, such as diabetic, neoplastic, and drug-induced neuropathies and traumatic nerve injuries sustained from crush and gun-shot wounds.
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