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Repair of divided peripheral nerves: experimental studies in rabbit and rat
Linköping University, Department of Biomedicine and Surgery, Plastic Surgery, Hand Surgery and Burns. Linköping University, Faculty of Health Sciences.
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The general aim of this thesis was to provide new knowledge, through experimental studies, that may contribute to an improvement of the results after microsurgical peripheral nerve repair in patients.

An adequate function of the human body depends, among other things, on a correctly functioning peripheral nervous system. Peripheral nerve injuries may impair the motor and sensory function of muscles, the proprioceptive joint control, the cutaneous sensibility, and the autonomic control of the skin, which can result in severe dysfunction of e.g. an extremity. The worst grade- of nerve injury is the division of an entire nerve. In the ideal case, the divided nerve can be sutured so that the distal and proximal nerve stumps are brought together. When peripheral nerve tissue has been lost at the site of injury, a direct repair is not possible. In such cases, the use of nerve grafts to bridge the defect, and/or suture of the distal nerve stump to an entirely different donor nerve is necessary to restore some function. Both types of such nerve repair, however, produce new sequelae due to loss of function of the nerves used for repair. To avoid such donor nerve morbidity, two different types of repair, end-to-end coaptation to part of a healthy donor nerve and end-to- side neurorrhaphy were investigated experimentally.

Neurotomy studies in the rabbit showed that use of 1/3 of a donor nerve (ulnar nerve) for reinnervation of an agonistic recipient nerve (median nerve) results in a useful muscle function with negligible donor nerve morbidity.

In the rat, end-to-side neurorrhaphy of a recipient nerve (median nerve) to an agonistic donor nerve (ulnar nerve) turned out to give a useful muscle function without causing donor nerve morbidity. After end-to-side neurorrhaphy, reinnervation of the recipient nerve stump was executed by collateral sprouting from intact donor nerve axons. The regeneration of sensory axons was numerically superior to the regeneration of motor axons. Altogether, however, good results after end-to-side neurorrhaphy are not predictable.

Both types of nerve repair (end-to-side neurorrhaphy and partial end-to-end neurorrhaphy) give better results with respect to reinnervation of a nerve to a simple muscle target than with respect to reinnervation of a nerve to a complex muscle target.

In the ideal situation, after conventional end-to-end nerve suture, nerve repair results in an axonal regeneration that restores muscle function as well as cutaneous sensibility and autonomous function. However, a completely normal function is usually not achieved due to e.g. aberrant axonal regeneration that results in a nerve-target mismatch. One of the causes for aberrant regeneration is axonal criss-crossing between fascicles in adjacency. Hence, barriers of different materials were tested in the rat to see if interfascicular axonal criss-crossing can be counteracted.

Three materials - a pedicle fat flap, Integra®, and non-vascularized autologous fasciawere used as barriers between the peroneal and the tibial fascicles in rats. The results showed that all three barriers improved axonal alignment after sciatic nerve transection and fascicular end-to-end repair. The pedicle fat flap was the most valuable barrier.

Finally, coaptation of the divided rat sciatic nerve with the aid of couplers, normally used for microvascular anastomoses, was evaluated as a method to hinder erratic centrifugal axon growth. The results showed that couplers provided a secluded coaptation site avoiding aberrant axonal sprouting to the surroundings. However, a minor nerve compression was evident.

Altogether, these results show that the microsurgical repair of nerve transections can be improved a bit further. However, the future developments in this area are likely to occur at the molecular level.

Place, publisher, year, edition, pages
Örebro: Prinfo Welins Tryckeri , 2004. , 57 p.
Series
Linköping University Medical Dissertations, ISSN 0345-0082 ; 841
National Category
Medical and Health Sciences
Identifiers
URN: urn:nbn:se:liu:diva-24389Local ID: 6482ISBN: 91-7373-813-1 (print)OAI: oai:DiVA.org:liu-24389DiVA: diva2:244707
Public defence
2004-03-19, Elsa Brändströmsalen, Hälsouniversitetet, Linköping, 13:00 (English)
Opponent
Available from: 2009-10-07 Created: 2009-10-07 Last updated: 2012-10-22Bibliographically approved
List of papers
1. Nerve transfer to the median nerve using parts of the ulnar and radial nerves in the rabbit: effects on motor recovery of the median nerve and donor nerve morbidity
Open this publication in new window or tab >>Nerve transfer to the median nerve using parts of the ulnar and radial nerves in the rabbit: effects on motor recovery of the median nerve and donor nerve morbidity
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2000 (English)In: Journal of Hand Surgery - British and European Volume, ISSN 0266-7681, E-ISSN 1532-2211, Vol. 25, no 4, 329-335 p.Article in journal (Refereed) Published
Abstract [en]

In this study, motor re-innervation of the median nerve by transfer of one-third, one-half, and two-thirds of either the agonistic ulnar nerve or the antagonistic radial nerve was investigated in both extremities of 20 rabbits.

Recipient median nerve: Muscle contraction force of the flexor digitorum sublimus muscle after a one-third and a one-half of the ulnar nerve transfer achieved an average of 75 and 97% muscle power respectively as compared to conventional end-to-end neurorrhaphy. Muscle contraction force after one-third or one-half of the radial nerve transfer was significantly lower (36%).

Donor nerves: Extensor carpi radialis muscle or flexor carpi ulnaris muscle contraction force 6 months postoperatively demonstrated a significant decrease after a one-half ulnar nerve and a two-thirds ulnar or radial nerve transfer, but not after a one-third transfer of either radial or ulnar nerves.

Histologically, the number of axons in the re-innervated median nerve and both donor nerves distal to the coaptation site seemed to follow variable patterns.

It was concluded that in the rabbit use of one-third of the agonistic ulnar nerve for re-innervation of the median nerve results in useful motor recovery with negligible donor site morbidity. Clinically, this technique may offer an alternative option for proximal nerve injuries or for free functioning muscle transplantations.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-84781 (URN)10.1054/jhsb.2000.0389 (DOI)
Available from: 2012-10-22 Created: 2012-10-22 Last updated: 2017-12-07Bibliographically approved
2. Selection of donor nerves: an important factor in end-to-side neurorrhaphy
Open this publication in new window or tab >>Selection of donor nerves: an important factor in end-to-side neurorrhaphy
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2000 (English)In: British Journal of Plastic Surgery, ISSN 0007-1226, E-ISSN 1465-3087, Vol. 53, no 2, 149-154 p.Article in journal (Refereed) Published
Abstract [en]

We have examined the effects of end-to-side neurorrhaphy on peripheral nerve regeneration usingthe median nerve as recipient nerve and either the antagonistic radial nerve or the agonistic ulnar nerve as donor nerves in rat upper limbs. A perineural window was created in all cases. Motor recovery up to 16 weeks postoperation was tested with the grasping test. No recovery of motor function was evident after end-to-side neurorrhaphy of the median nerve to the antagonistic radial nerve, whereas six of eight rats with end-to-side neurorrhaphy to the agonistic ulnar nerve achieved 367 g±47 g grasping power as compared to 526 g±6 g in end-to-end coapted control animals. No significant difference in flexor digitorum sublimus-motor nerve conduction velocity was found among all three groups. Radial nerve stimulation produced simultaneous contraction of both extensor and flexor muscles of the lower arm that disabled any coordinated movement of the paw. Histology (toluidine blue, acetylcholinesterase-stain) showed multiple regenerated (motor)-axons distal to the coaptation site in the median nerve. Reinnervation of the median nerve solely by the respective donor nerve was demonstrated by a retrograde double labelling technique. These results show that averaged 70% muscle power as compared to end-to-end neurorrhaphy with well coordinated muscle function can be achieved by axonal sprouting through end-to-side neurorrhaphy if an agonistic nerve is used as donor nerve. However, satisfying results are unpredictable. Antagonistic nerves show the ability to induce axonal regeneration, but no useful function can be expected.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-84782 (URN)10.1054/bjps.1999.3252 (DOI)
Available from: 2012-10-22 Created: 2012-10-22 Last updated: 2017-12-07Bibliographically approved
3. Role of the target in end-to-side neurorrhaphy: reinnervation of a single muscle vs. multiple muscles
Open this publication in new window or tab >>Role of the target in end-to-side neurorrhaphy: reinnervation of a single muscle vs. multiple muscles
2000 (English)In: Journal of reconstructive microsurgery, ISSN 0743-684X, E-ISSN 1098-8947, Vol. 16, no 6, 443-448 p.Article in journal (Refereed) Published
Abstract [en]

The authors examined the effects of end-to-side neurorrhaphy for reinnervation of the musculocutaneous nerve (Group A) which innervates the biceps muscle, compared to reinnervation of the median nerve which innervates multiple muscles in a rat model. Additionally, end-to-end neurorrhaphy to the musculocutaneous nerve using one-third of the median nerve (Group B) was investigated. End-to-end coaptation of the musculocutaneous nerve served as a control (Group C). In a grooming test, the biceps muscle function in Group A animals demonstrated a slower but nearly similar good recovery to Groups B and C. Biceps muscle contraction force investigated after 24 weeks demonstrated no statistically significant differences among all groups. In Groups A and B, no significant impairment of the donor median nerve function was found in a grasping test and the muscle contraction force of the flexor carpi radialis muscle, and histologic evaluation of the musculocutaneous nerve showed multiple regenerated axons distal to the coaptation site. Retrograde double-labeling in Group A animals showed reinnervation of the musculocutaneous nerve by median nerve axons located at the coaptation site. These results validate that end-to-side neurorrhaphy to a nerve innervating a single muscle is more efficient than to a nerve innervating multiple muscles, as demonstrated in an earlier study. The reason for this phenomenon is most likely that all sprouting axons are directed toward one target rather than toward multiple targets, with the latter situation resulting in a smaller number of axons and a variable distribution of axons per target. Since donor nerve sprouting axons were observed at the coaptation site, a relevance of the selected site for end-to-side neurorrhaphy is suggested. Both end-to-side neurorrhaphy and end-to-end neurorrhaphy, using one-third of the median nerve, led to useful functional recovery in this rat model, if an agonistic donor nerve is employed.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-84783 (URN)10.1055/s-2006-947151 (DOI)10993090 (PubMedID)
Available from: 2012-10-22 Created: 2012-10-22 Last updated: 2017-12-07Bibliographically approved
4. Interposition of a pedicle fat flap significantly improves specificity of reinnervation and motor recovery after repair of transected nerves in adjacency in rats
Open this publication in new window or tab >>Interposition of a pedicle fat flap significantly improves specificity of reinnervation and motor recovery after repair of transected nerves in adjacency in rats
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2001 (English)In: Plastic and reconstructive surgery (1963), ISSN 0032-1052, E-ISSN 1529-4242, Vol. 107, no 1, 116-123 p.Article in journal (Refereed) Published
Abstract [en]

Despite highest standards in nerve repair, functional recovery following nerve transection still remains unsatisfactory. Nonspecific reinnervation of target organs caused by misdirected axonal growth at the repair site is regarded as one reason for a poor functional outcome. This study was conducted to establish a method for preventing aberrant reinnervation between transected and repaired nerves in adjacency.

Rat sciatic nerve was transected and repaired as follows: epineural sutures of the sciatic nerve (group A, n = 6), fascicular repair of tibial and peroneal nerves respectively (group B, n = 8), and, as in group B, separating both nerves using a pedicle fat flap as barrier (group C, n = 8). As control only, the tibial nerve was transected and repaired (group D, n = 5).

Muscle contraction force of the gastrocnemius muscle was significantly higher in group C as compared with groups A and B after 4 months. Muscle weight showed significantly lower values in group A as compared with groups B, C, and D. Histologic examination in group C revealed little growth of axons from the tibial to the peroneal nerve and vice versa. This axon crossing was observed only when gaps between the fat cells were available. These findings were confirmed by a significantly lower rate of misdirected axonal growth as compared with groups A and B using sequential retrograde double labeling technique of the soleus motoneuron pool.

We conclude that a pedicle fat flap significantly prevents aberrant reinnervation between repaired adjacent nerves resulting in significantly improved motor recovery in rats. Clinically, this is of importance for brachial plexus, sciatic nerve, and facial nerve repair.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-84788 (URN)11176609 (PubMedID)
Available from: 2012-10-22 Created: 2012-10-22 Last updated: 2017-12-07Bibliographically approved
5. Specificity of reinnervation and motor recovery after interposition of an artificial barrier between transected and repaired nerves in adjacency: an experimental study in the rat
Open this publication in new window or tab >>Specificity of reinnervation and motor recovery after interposition of an artificial barrier between transected and repaired nerves in adjacency: an experimental study in the rat
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2001 (English)In: Acta Neurochirurgica, ISSN 0001-6268, E-ISSN 0942-0940, Vol. 143, no 4, 393-399 p.Article in journal (Refereed) Published
Abstract [en]

Non-specific re-innervation of target organs caused by misdirected axonal growth at the repair site is regarded as one reason for a poor functional outcome after peripheral nerve transsection and repair. This study investigates the rate of aberrant re-innervation and its influence on motor recovery in the rat sciatic nerve using artificial sheets as barrier between tibial and peroneal nerves.

The sciatic nerve was transsected and repaired as follows: epineural sutures (A × 6), fascicular repair of tibial and peroneal nerves respectively (B × 8), and the same as in group B, but separating both nerves using an Integra®-sheet with silicone (C × 8), or Integra® without silicone (D × 8). As control, solely the tibial nerve was transsected and repaired (E × 5).

Final investigations after 4 months revealed that in group C, 50% of the Integra®-silicone sheets were dislocated. No dislocation was found in group D. Muscle contraction force of the gastrocnemius muscle was significantly higher in group E as compared to all other groups. However although not significant, group D showed a consistently higher muscle contraction force than groups A, B, and C. Histology in groups A, B, and C with dislocated sheets demonstrated multiple axons growing from the tibial to the peroneal nerve and vice versa. In groups D and E, no such axonal growth was visible. These findings were confirmed by a significantly higher rate of specific re-innervation of the soleus muscle using sequential retrograde double labelling technique.

Results of this study suggest that an artificial sheet such as Integra® bears the potential of preventing aberrant re-innervation between repaired adjacent nerves resulting in improved motor recovery. Clinically, this technique may be of importance for brachial plexus, sciatic nerve, and facial nerve repair.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-25220 (URN)10.1007/s007010170095 (DOI)9659 (Local ID)9659 (Archive number)9659 (OAI)
Available from: 2009-10-07 Created: 2009-10-07 Last updated: 2017-12-13Bibliographically approved
6. Structural and functional regeneration of muscle-related axons after transection and repair of the rat sciatic nerve using nonvascularized autologous fascia as a barrier between tibial and peroneal nerve fascicles
Open this publication in new window or tab >>Structural and functional regeneration of muscle-related axons after transection and repair of the rat sciatic nerve using nonvascularized autologous fascia as a barrier between tibial and peroneal nerve fascicles
2004 (English)In: Journal of reconstructive microsurgery, ISSN 0743-684X, E-ISSN 1098-8947, Vol. 20, no 8, 637-644 p.Article in journal (Refereed) Published
Abstract [en]

Aberrant reinnervation of target organs caused by misdirected axonal growth at the repair site is a major reason for the poor functional outcome usually seen after peripheral nerve transection and repair. This study investigates whether the criss-crossing of regenerating rat sciatic nerve axons between tibial and peroneal nerve fascicles can be reduced by using non-vascularized autologous fascia as a barrier.

The left sciatic nerve was transected and repaired at midthigh as follows: epineurialy sutures (Group A); fascicular repair of tibial and peroneal nerve fascicles (Group B); fascicular repair of tibial and peroneal nerve fascicles separating the two fascicles by non-vascularized autologous fascia (Group C). In the control Group D, only the left tibial fascicle was transected and repaired. Five months postoperatively, the outcome of regeneration was evaluated by histology, by retrograde tracing, and by assessment of the contraction force of the gastrocnemius and tibial anterior muscles. The tracing experiments showed that muscle reinnervation was less abnormal in Group C than in Groups A and B. However, muscle contraction force was not better in Group C than in Groups A and B. With respect to the peroneal nerve innervated muscle, the contraction force in Group C was significantly lower than in Group B. The histologic picture indicated that this inferior result in Group C was due to nerve compression caused by fibrotic scar tissue at the site of the fascia graft.

Results of this study show that a non-vascularized autologous fascial graft used as a barrier between two sutured nerve fascicles in adjacency reduces criss-crossing of regenerating axons between the fascicles, but causes significant nerve compression.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-24436 (URN)10.1055/s-2004-861524 (DOI)6543 (Local ID)6543 (Archive number)6543 (OAI)
Available from: 2009-10-07 Created: 2009-10-07 Last updated: 2017-12-13Bibliographically approved

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