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DEVELOPMENT OF COLLATERAL CIRCULATION IN PARTIALLY EEVASCULARIZED FELINE SCIATIC NERVE 31 JOHN FRANCIS O'KALLEY A THESIS Submitted to the Faculty of the Graduate School of the Creighton University in Partial Fulfillment of the Requirements for the Degree of Master of Science in the Department of Anatomy Omaha, 1 969 V ACKNOWLEDGMENTS I am deeply indebted ana grateful to my advisor, Doctor Julian J. Baumel, for his patience, unselfish assistance, and constructive criticism throughout this investigation. I also wish to express my appreciation to Dr. R. Dale Smith for his valuaole assistance, to Dr. John 3arton for his help with the photogranhie representations, to Mrs. Edith Witt for the expert typing of the final manuscript, and to all the members of the faculty of the Anatomy Department for the excellent graduate training I have received. I especially wish to acknowledge my wife, Helen, for her understanding and perseverance through out my graduate studies, and it is to her that I dedicate this t h e s i s . vi TABLE OF CONTENTS A C KN OWLE DG ï T E N T S .......... LIST OF ILLUSTRATIONS Chapter I. INTRODUCTION ....................................... 1 II. HISTORY ............................................ 1+ Vasa Nervorum Collateral Circulation III. MATERIALS AND METHODS ............................ 10 Surgical Exposure Devascularization Vascular Injection Clearing IV. O B S E R V A T I O N S ....................................... l£ Sciatic Nerve - Anatomy Vascular Supply of Sciatic Nerve Art e r i e s Veins Development of Collateral Circulation Three-Day ‘/ascular Pattern Six-Seven Day Vascular Patterns Fourteen-Seventeen Day Vascular Patterns V. D I S C U S S I O N ....................................... 23 Role of Vasa Nervorum Collateral Circulation LITERATURE C I T E D .............................................. vii LIST OF ILLUSTRATIONS Figure 1. Sciatic Nerve Bed Showing Relationships to S u r r o u n d i n g M u s c u l a t u r e .......................... 33 2. Segment of Normal Sciatic Nerve Showing Linear Pattern of Blood Vessels ....................... 36 3. Bifurcation of Sciatic Nerve Into Tibial and Common Peroneal Divisions ....................... 37 h. Transitional Zone Between Intermediate and Lower Segments Showing Characteristic Features of Three Day Operated Nerve .... 38 5» Intermediate Segment of Three Day Operated Nerve Demonstrating Incipient Enlargement of Longitudinal Epineurial Vein and Smaller U n f i l l e d Tortuous Veins .......................... 38 6. Three Day Operated Nerves Viewed Macro- s c o p i c a l l y .....................................................................39 7. Segment of Three Day Nerve Demonstrating Poor Filling at Higher Magnification .... 39 8. Comparison Between Six-Seven Day Operated Nerve and N o r m a l N e r v e .............................[¿0 9. Six-Seven Day Nerve in situ With Portion of Enveloping Sheaths Displayed .................. ]RL 10. Plexiform Vascular Pattern in Tibial Division of Fourteen Day Operated N e r v e ............... ¡+2 11. Segment of Six-Seven Day Operated Nerve Demonstrating Comparative Response of Smaller Epineurial Arteries end Veins .... 1+3 12. Segment of Six-Seven Day Operated Nerve Characterized by Very Prominent Longitudinal Epineurial V e i n .................. '\1+l 1. INTRODUCTION A survey of the existing literature in the field of peripheral nerve vascularity has established that nerve function is influenced by vascular supply; however, opinion varies considerably concerning the extent of such dependence• Apparently, influence of vascular supply is unquestioned; its importance is suspected, whereas its necessity is highly polemical. Just how important is vascular supply to a nerve? Its neces sity in other body organs is unquestioned; yet its value for normal nerve function is still controversial. Since the discovery of axioplasmic flow (Weiss, 'k3; Weiss and Davis, *U3) two schools of thought have arisen; one holding that the only essential require ment for normal peripheral nerve function is the anatomical and physiological continuity of the axon with its cell body and that the primary source of neuronal nutrition is the pulsating flow of axoplasm proceeding distally along the fiber, blood supply being only incidental. The other school claims that vascular supply is essential if normal neuronal structure and function are to be maintained. In all probability both contribute to normal nerve function. Reports in the literature have shown that ischemia of peripher al nerves causes decreased nerve fmiction and have indicated a definite correlation between the vascular state of the nerve and its performance. In an endeavor to verify this, preliminary 2 experiments were conducted on cats, devascularizing the femoral extent of their sciatic nerves. These experiments have demonstrated that ischemia produces alterations in the rate of alpha fiber con ductivity. It was consistently observed that during the first three days following controlled devascularization slower conduction velocities were obtained from the devascularized nerve than from the control side. On the other hand, conduction velocities of the ischemic nerves of 5-7 day animals approximated those obtained from the contralateral control side. The pilot studies were consistent with the findings of Gillilan (’66), relating conduction velocity to ischemia. Inspection of the partially devascularized nerve in injected specimens led to the belief that the return of "normal” conductivity occurred synchronously with the restoration of vascular supply via collateral pathways, evidenced by the enlargement, proliferation, and tortuosity of the epineurial vessels. In other words, it appeared that vascular embarrassment of the sciatic nerve caused decreased conduction velocity initially, whereas collateral circu lation, when functionally established, restored, perhaps even enhanced, blood supply, increasing the velocity. This apparent correlation between the vascular competency of the nerve and its functional state required that the details of the development of a collateral circulation be investigated prior to continuation of conduction velocity studies. The research endeavor was now focused on producing "standard" ischemia of the sciatic nerve and studying 3. the reestablishment of circulation on a temporal basis — its mode, extent, pattern, and salient features as contrasted with the vascular pattern of the normal feline sciatic nerve♦ b- HISTORY The brief historical review which follows is necessarily two fold. It is concerned with the normal vascular supply to peripheral nerves (vasa nervorum), and with the development of collateral circulation evidenced by the changing angioarchitectural pattern that emerges in response to ischemia. A survey of the literature dis closes that both topics, the blood supply of nerves, and the development of collateral circulation, have been repeatedly examined and periodically reviewed. However, re-examinâtions must continue as new observations are made and more recent findings become avail able. Vasa Nervorum It is generally agreed that Albrecht von Haller (1?5>6), be credited the first to consider the vascular supply of nerves in detail. In 1627, Van der Spiegel opined that vasa nervorum might be important in the nutrition of peripheral nerves. Ruysch (1701) was also apparently aware of the potential significance of the vasa nervorum. The first publication devoted exclusively to the subject of peripheral nerve vascularity entitled "De Vasis Nervorum" was co-authored by Isenflamm and Doerffler (1768). Using colored wax they successfully displayed the networks of vessels surrounding nerves. Still another century passed before Ranvier (1878)" delin eated these extrinsic vessels in greater detail, in addition demonstrating that nerves housed internal as well as external 5 vascular plexuses which were in communication with one another, anastomoses occurring at both the intrafascicular and interfascic ular levels. Hyrtl, between 1859 and 186U, published a series of papers which marked the initial attempt to formulate general principles regarding the angio-architecture of peripheral nerves. He established certain principles concerning peripheral nerve vascu larity, proposing in essence that: 1) every nerve, regardless of size, receives nutrient arteries which run to the nerve without branching and after passing along its surface, enter it to form internal capillary plexuses ; 2) these arteries supply only the nerve and do not provide any branches to adjacent muscles; and 3) each vessel, although concerned primarily with the supply of a definite segment of the nerve, bifurcates into ascending and descending branches, each of which, in turn, anastomoses with the corresponding branches of adjacent nutrient arteries. In this way, a continuous longitudinal anastomosis is formed within the nerve ; it was to this anastomosis that Hyrtl attached great o. significance. The monographs of Quenu and Lejars near the termination of the 19th century (1890, 1892, 189U;, deserve special note. Their descriptions are classical in detail and presentation, and their appreciation of functional significance profound. They paid particular attention to the numerous anastomoses between adjacent vasa nervorum both on the surfaces and within the trunks, contend ing that such an arrangement would indeed render a total interruption of blood supply to the nerve highly improbable. They demonstrated insight as to the importance of these vessels beyond representing