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The plantaris tendon in relation to the Achilles tendon in midportion Achilles tendinopathy: studies on morphology, innervation and signalling substances
Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). (Neuropeptide Group)
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Midportion Achilles tendinopathy (tendinosis) is a troublesome painful condition, often characterised by pain, local swelling, tenderness and functional disability. Despite extensive research, the pathogenesis is poorly understood and treatment remains challenging. Features related to the peritendinous connective tissue can be of importance. Recently it has been suggested that the plantaris tendon might be involved in this condition. Furthermore, it has been hypothesised that tendon pain and the tendinosis-related tissue changes in tendinopathy might be mediated by signalling substances such as glutamate and acetylcholine. A clinical observation, not scientifically evaluated, has been that unilateral treatment for bilateral Achilles tendinosis can lead to an effect on the contralateral side.

     The aim of this work was to examine the morphology and innervation patterns in the plantaris tendon and the peritendinous connective tissue in between the Achillles and plantaris tendons in midportion Achilles tendinopathy, and to evaluate if plantaris tendon removal has an effect on Achilles tendon structure. Another aim was to determine if unilateral treatment for Achilles tendinopathy targeting the peritendinous connective tissue can result in bilateral recovery. Furthermore the presence of non-neuronal cholinergic and glutamate systems was examined.

     Sections of plantaris tendons with adjacent peritendinous connective tissue from patients with midportion Achilles tendinopathy were stained for morphology (H&E), and innervation patterns were evaluated using antibodies against general nerve marker (PGP9.5), sensory (CGRP) and sympathetic (TH) nerve fibres and Schwann cells (S-100β). Furthermore immunostainings against non-neuronal aceylcholine (ChAT) and glutamate signalling components (glutamate, VGluT2, NMDAR1) were performed. Plantaris tendon cells were cultured and also stained for glutamate signalling components, and were stimulated with glutamate and glutamate receptor agonist NMDA. Furthermore, Ultrasound Tissue Characterisation (UTC) was used to monitor the integrity of the Achilles tendon collagen structure after plantaris tendon removal.

     Plantaris tendons exhibited tendinosis-like tissue patterns such as hypercellularity, collagen disorganisation and large numbers of blood vessels. The peritendinous connective tissue between the plantaris and Achilles tendons contained large numbers of fibroblasts and blood vessels and to some extent macrophages and mast cells. A marked innervation was found in the peritendinous connective tissue and there were also nerve fibres in the loose connective tissue spaces within the tendon tissue proper. Most nerve fibres were identified as sensory fibres. Some nerve fascicles in the peritendinous connective tissue showed absence of axons but homogenous reactions for Schwann cell marker. Tenocytes and cells in the peritendinous connective tissue expressed ChAT, glutamate, VGluT2 and NMDAR1. Tendon cells in vitro expressed VGluT2, NMDAR1 and glutamate. UTC showed significant improvement of Achilles tendon integrity 6 months after surgical plantaris tendon removal and scraping procedure. Eleven out of thirteen patients reported of a bilateral recovery after unilateral surgical treatment.

     The results of this work show that plantaris tendons exhibit tendinosis-like tissue changes, internal innervation and features that suggest occurrence of glutamate and acetylcholine production and signalling. Plantaris removal improves Achilles tendon structure suggesting possible compressive/shearing interference between the Achilles and plantaris tendons in tendinopathy. The peritendinous connective tissue shows marked innervation, which thus might transmit pain when being compressed. The partial absence of axons indicates a possible nerve degeneration. On the whole, the study gives new evidence favouring that the plantaris tendon and the peritendinous connective tissue might be of importance for pain and the tendinopathy process in midportion Achilles tendinopathy.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2015. , 71 p.
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 1729
Keyword [en]
Plantaris tendon, Achilles tendon, Achilles tendinopathy, innervation, morphology
National Category
Cell and Molecular Biology Orthopedics Sport and Fitness Sciences
Identifiers
URN: urn:nbn:se:umu:diva-103292ISBN: 978-91-7601-290-1 (print)OAI: oai:DiVA.org:umu-103292DiVA: diva2:812691
Public defence
2015-06-12, BiA201, Biologihuset, Umeå University, Umeå, 09:00 (English)
Opponent
Supervisors
Available from: 2015-05-21 Created: 2015-05-19 Last updated: 2015-05-21Bibliographically approved
List of papers
1. The plantaris tendon in association with mid-portion Achilles tendinosis: tendinosis-like morphological features and presence of a non-neuronal cholinergic system
Open this publication in new window or tab >>The plantaris tendon in association with mid-portion Achilles tendinosis: tendinosis-like morphological features and presence of a non-neuronal cholinergic system
Show others...
2013 (English)In: Histology and Histopathology, ISSN 0213-3911, E-ISSN 1699-5848, Vol. 28, 623-632 p.Article in journal (Refereed) Published
Abstract [en]

The plantaris tendon is often neglected in morphological/clinical studies on the lower extremity. There is, however, clinical evidence that the plantaris tendon is involved in cases with Achilles midportion tendinopathy/tendinosis. It is nevertheless unclear if the plantaris tendon exhibits tendinosis-like features in this situation. We therefore investigated the plantaris tendon of patients with midportion Achilles tendinosis when the plantaris tendon was found to be located very close to or invaginated into the Achilles tendon, a situation which very often has been found to be the case. There was a very large number of tenocytes in the tendon tissue and the tenocytes showed abnormal and irregular appearances, exhibiting widened/rounded and wavy appearances, and were frequently lined up in rows. These features are characteristic features in Achilles tendinosis tendons. The tendon cells showed a distinct immunoreaction for the acetylcholine (ACh) -producing enzyme choline acetyltransferase (ChAT). Frequent fibroblasts were found in the loose connective tissue and these cells also showed a marked ChAT immunoreaction. The study shows that the plantaris tendon is morphologically affected in a similar way to the Achilles tendon in cases with midportion Achilles tendinosis and medial pain. The plantaris tendon may accordingly be a co-factor in these cases. The results also favour that there is a local ACh production both within the tendon tissue of the plantaris tendon and in the loose connective tissue. In conclusion, it is evident that plantaris tendons lying invaginated into or very close to the Achilles tendon in cases with midportion Achilles tendinosis show similar tendinosis features, as previously shown for the Achilles tendon itself in these cases.

Keyword
Plantaris tendon, Achilles tendon, Tendinopathy, Tenocyte morphology, Cholinergic, Choline acetyltransferase
National Category
Physiology
Identifiers
urn:nbn:se:umu:diva-66856 (URN)10.14670/HH-28.623 (DOI)000317749100008 ()23378267 (PubMedID)
Available from: 2013-03-06 Created: 2013-03-06 Last updated: 2017-12-06Bibliographically approved
2. Achilles tendinopathy - do plantaris tendon removal and Achilles tendon scraping improve tendon structure?: A prospective study using ultrasound tissue characterisation
Open this publication in new window or tab >>Achilles tendinopathy - do plantaris tendon removal and Achilles tendon scraping improve tendon structure?: A prospective study using ultrasound tissue characterisation
2015 (English)In: BMJ Open Sport & Exercise Medicine, ISSN 2055-7647, Vol. 1, no 1, e000005Article in journal (Refereed) Published
Abstract [en]

Objectives The plantaris tendon has recently been described as a possible important factor in midportion Achilles tendinopathy. Ultrasound tissue characterisation (UTC) is a method to study tendon structure (matrix integrity). The effect of plantaris tendon removal on Achilles tendon structure was studied using UTC.

Design and setting Prospective case series study at one centre.

Participants Nine tendons in eight physically active and healthy patients (mean age 39 years) with chronic painful midportion Achilles tendinopathy were included. Preoperative two-dimensional ultrasound and UTC showed midportion Achilles tendinopathy (tendinosis) with medial tendon changes and suspected plantaris tendon involvement. Patients with previous operations to the Achilles tendon were excluded.

Interventions Operative treatment consisted of excision of the plantaris tendon and scraping of the ventromedial surface of the Achilles tendon under a local anaesthetic.

Primary and secondary outcome measures UTC examination and clinical scoring with the VISA-A questionnaire were performed preoperatively and 6 months postoperatively.

Results At 6 months follow-up, UTC demonstrated a statistically significant (t=5.40, p<0.001) increase in the mean organised matrix (echo-type I+II) and a decrease in the mean disorganised matrix (echo-type III+IV). Seven out of eight patients were satisfied, and the VISA-A score had increased significantly (p<0.001) from 56.8 (range 34–73) preoperatively to 93.3 (range 87–100) postoperatively.

Conclusions Excision of the plantaris tendon and scraping of the ventromedial Achilles tendon in chronic midportion tendinopathy seem to have the potential to improve tendon structure and reduce tendon pain. Studies on a larger group of patients and with a longer follow-up period are needed.

National Category
Physiology Sport and Fitness Sciences
Identifiers
urn:nbn:se:umu:diva-103307 (URN)10.1136/bmjsem-2015-000005 (DOI)
Available from: 2015-05-20 Created: 2015-05-20 Last updated: 2015-05-20Bibliographically approved
3. Marked innervation but also signs of nerve degeneration in between the Achilles and plantaris tendons and presence of innervation within the plantaris tendon in midportion Achilles tendinopathy
Open this publication in new window or tab >>Marked innervation but also signs of nerve degeneration in between the Achilles and plantaris tendons and presence of innervation within the plantaris tendon in midportion Achilles tendinopathy
2015 (English)In: Journal of Musculoskeletal and Neuronal Interactions - JMNI, ISSN 1108-7161, Vol. 15, no 2, 197-206 p.Article in journal (Refereed) Published
Abstract [en]

Objectives: The plantaris tendon is increasingly recognised as an important factor in midportion Achilles tendinopathy. Its innervation pattern is completely unknown. Methods: Plantaris tendons (n=56) and associated peritendinous tissue from 46 patients with midportion Achilles tendinopathy and where the plantaris tendon was closely related to the Achilles tendon were evaluated. Morphological evaluations and stainings for nerve markers [general (PGP9.5), sensory (CGRP), sympathetic (TH)], glutamate NMDA receptor and Schwann cells (S-100β) were made. Results: A marked innervation, as evidenced by evaluation for PGP9.5 reactions, occurred in the peritendinous tissue located between the plantaris and Achilles tendons. It contained sensory and to some extent sympathetic and NMDAR1-positive axons. There was also an innervation in the zones of connective tissue within the plantaris tendons. Interestingly, some of the nerve fascicles showed a partial lack of axonal reactions. Conclusion: New information on the innervation patterns for the plantaris tendon in situations with midportion Achilles tendinopathy has here been obtained. The peritendinous tissue was found to be markedly innervated and there was also innervation within the plantaris tendon. Furthermore, axonal degeneration is likely to occur. Both features should be further taken into account when considering the relationship between the nervous system and tendinopathy

Keyword
Plantaris Tendon, Achilles Tendinopathy, Pain, Innervation, Peritendinous Connective Tissue
National Category
Physiology
Identifiers
urn:nbn:se:umu:diva-103312 (URN)000356001800011 ()
Available from: 2015-05-20 Created: 2015-05-20 Last updated: 2017-12-04Bibliographically approved
4. Unilateral surgical treatment for patients with midportion Achilles tendinopathy may result in bilateral recovery
Open this publication in new window or tab >>Unilateral surgical treatment for patients with midportion Achilles tendinopathy may result in bilateral recovery
2014 (English)In: British Journal of Sports Medicine, ISSN 0306-3674, E-ISSN 1473-0480, Vol. 48, no 19, 1421-1424 p.Article in journal (Refereed) Published
Abstract [en]

BACKGROUND: Bilateral midportion Achilles tendinopathy/tendinosis is not unusual, and treatment of both sides is often carried out. Experiments in animals suggest of the potential involvement of central neuronal mechanisms in Achilles tendinosis. OBJECTIVES: To evaluate the outcome of surgery for Achilles tendinopathy. METHODS: This observational study included 13 patients (7 men and 6 women, mean age 53 years) with a long duration (6-120 months) of chronic painful bilateral midportion Achilles tendinopathy. The most painful side at the time for investigation was selected to be operated on first. Treatment was ultrasound-guided and Doppler-guided scraping procedure outside the ventral part of the tendon under local anaesthetic. The patients started walking on the first day after surgery. Follow-ups were conducted and the primary outcome was pain by visual analogue scale. In an additional part of the study, specimens from Achilles and plantaris tendons in three patients with bilateral Achilles tendinosis were examined. RESULTS: Short-term follow-ups showed postoperative improvement on the non-operated side as well as the operated side in 11 of 13 patients. Final follow-up after 37 (mean) months showed significant pain relief and patient satisfaction on both sides for these 11 patients. In 2 of 13 patients operation on the other, initially non-operated side, was instituted due to persisting pain. Morphologically, it was found that there were similar morphological effects, and immunohistochemical patterns of enzyme involved in signal substance production, bilaterally. CONCLUSION: Unilateral treatment with a scraping operation can have benefits contralaterally; the clinical implication is that unilateral surgery may be a logical first treatment in cases of bilateral Achilles tendinopathy.

Place, publisher, year, edition, pages
BMJ Publishing Group, 2014
National Category
Basic Medicine Sport and Fitness Sciences
Identifiers
urn:nbn:se:umu:diva-66859 (URN)10.1136/bjsports-2012-091399 (DOI)000341947200007 ()23193327 (PubMedID)
Available from: 2013-03-06 Created: 2013-03-06 Last updated: 2017-12-06Bibliographically approved
5. Plantaris tendon tissue of tendinosis patients displays a glutamate signallingmachinery that may influence tenocyte phenotype
Open this publication in new window or tab >>Plantaris tendon tissue of tendinosis patients displays a glutamate signallingmachinery that may influence tenocyte phenotype
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Physiology
Identifiers
urn:nbn:se:umu:diva-103313 (URN)
Available from: 2015-05-20 Created: 2015-05-20 Last updated: 2015-05-20Bibliographically approved

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