Time to abandon the “tendinitis” myth

Congratulations to Khan et al on the article. I agree it is high time
those of us involved in musculoskeletal healthcare recognise the wealth of
evidence that tendon overuse injuries do not exhibit significant
inflammatory pathology. Tendinopathy would indeed seem to be a more
appropriate term for these conditions.

I wonder if the following ideas are of interest:

In addition to their usual connective tissue components, tendons are
surrounded by loose areolar connective tissue that forms a complete or
partial sheath around them (Norkin and Levangie, 1992). The sheath formed
around certain tendons is called the paratenon (Norkin and Levangie,
1992). The paratenon consists essentially of type I and type III collagen
fibrils, some elastin fibrils and an inner lining of synovial cells
(Williams, 1986). The space beneath the paratenon is rich in
mucopolysccharides which allows the paratenon to act as an elastic sleeve
that allows freedom of movement of the tendon (Kvist, 1994). The paratenon
may become a synovial fluid filled sheath, the teno-synovium, in tendons
that are subjected to friction (Curwin, 1996). The paratenon has a good
blood supply.
Khan et al (1999) note that paratenonitis (inflammation of the paratenon)
occurs when a tendon rubs excessively over a bony protuberance, the
increased friction resulting in inflammation.
With acute Achilles paratenonitis, an inflammatory cell reaction, oedema,
extravasation of plasma proteins, accumalation of fibrin and sparse
fibroblastic proliferation are seen in the paratenon (Rais, 1961). After a
few hours to a few days, fibrinous exudate fills the tendon sheath causing
crepitus that can be felt on clinical examination (Khan et al, 1999).
Mononuclear cells are seen to sparsely infiltrate the paratenon (Khan et
al, 1999).

When paratenonitis becomes chronic, the typical features include
oedema, fibrinoid exudations, proliferation of blood vessels and
thickening of the paratenon (Kvist, 1994). Fibroblasts and a perivascular
lymphocytic infiltrate appear on histological examination (Khan et al,
1999). In additon to the paratenon thickening, new connective tissue
adhesions occur (Jarvinen et al, 1997). Microscopically, cells known as
myofibroblasts are seen to appear (fibroblastic cells with cytoplasmic
myofilaments) (Jarvinen et al, 1997). Myofibroblasts are capable of active
contraction, and Jarvinen and colleagues (1997) hypothesise that they may
be responsible for the scarring and shrinkage associated with
paratenonitis. Blood vessels proliferate around the injured area of the
paratenon and inflammatory changes are visible in some of the arteries
(Khan et al, 1999). However, Kvist (1994) notes that only a slight
inflammatory cell reaction is present in the paratenon itself. Khan et al
(1999) support this observation, and note that experienced pathologists
agree that inflammation of the paratenon is a rare occurrence.
Evidence to support the concept that paratenonitis is a common feature of
chronic Achilles tendinosis is sparse. That which does exist is
conflicting.
Astrom and Rausing (1995) reported histopathological findings for 163
patients with chronic Achilles tendinopathy. They found degenerative
changes (tendinosis) in 90% of biopsy specimens (Astrom and Rausing,
1995). However, the paratenon was mostly normal, or revealed only slight
inflammatory changes (Astrom and Rausing, 1995). This would suggest that
paratenonitis is not a common feature of chronic Achilles tendinosis.
However, Kvist et al (1992) found a strong association between chronic
degenerative Achilles tendinosis and inflammation of the paratenon.
Further support for this association comes from the results of animal
experiments by Backman and colleagues (1990). Backman et al (1990) induced
Achilles tendinosis in a rabbit population by stimulating the the rabbits
using a kicking machine for 6 weeks. They found that the rabiit Achilles
tendon showed signs of degeneration (tendinosis) and the paratenon to be
inflamed (Backman et al, 1990). The results of Backman et al (1990) and
Kvist et al (1992) would suggest that paratenonitis is a common feature of
chronic Achilles tendinosis. However, Astrom and Rausing (1995) criticised
the Kvist et al (1992) experiment for poor analytical technique when
examining the involved tendons.

In light of this, does one need to clinically differentiate between a
paratenonitis and tendinopathy, and if so, how is this done? Additionally,
is there any evidence on the effects of NSAIDS when used to treat acute
paratenonitis as a distinct clinical entity?

With regard to treatment techniques for tendinopathy I would agree
with Khan and Colleagues that biomechanical factors are of paramount
importance. As a physiotherapist with an interest in Achilles tendinopathy
I have found the following factors to be of particular interest.

· Poor flexibility / Muscle imbalance
Shortened muscles and tight muscles often occur after exercise and
endurance sports and weakening and imbalance of muscles often results
(Kvist, 1994). Poor flexibility of the gastrocnemius-soleus complex has
been implicated in a Achilles tedinopathy (Kvist, 1994; Clement et al,
1984). Malone et al (1996) note that strong, flexible muscles have a
greater capacity to absorb energy. Stiff, less flexible, weak muscles
absorb less energy during activity, resulting in greater energy transfer
to other structures, including tendon. One can hypothesise that poor
muscle strength and flexibility of the gastrocnemius-soleus complex
results in greater energy transfer to the Achilles tendon, and hence an
increased risk of pathology during activity.

· Anatomical / Biomechanical abnormalities
Anatomical and functional asymmetry of the locomotor apparatus is common
(Kvist, 1994). Well controlled studies of the affects of biomechanical
abnormalities on Achilles tendon pathology are scarce. However, Clement et
al (1984) suggest that over-pronation combined with external rotation
during running produces a whipping action of the Achilles tendon. Clement
et al (1984) suggest that this whipping action results in an area of
vascular blanching 2-6cm above the Achilles tendon insertion. The reduced
blood supply is thought to result in a succession of local ischaemia and
degeneration (Kvist, 1994). Additionally, increased pronation has been
linked to an increase in stress on the Achilles during the mid-stance
phase of running (Leach et al, 1983). This increased stress may result in
a predisposition to microtrauma and tendon pathology.

The cavus foot is thought to absorb shock poorly and tends to place
more stress on the lateral side of the Achilles tendon (Subotnick, 1989)
and is associated with Achilles tendon pathology.

Numerous studies have associated biomechanical abnormalities
including forefoot varus, tibia vara, talipes equines, and tight
hamstrings and calf muscles, with Achilles tendon pathology (Kvist, 1994;
Subotnick, 1989; Curwin, 1996).

· Abnormal loading for other reasons
Excess loading of the Achilles due to any other factors presumably
increases the risk of tendon pathology due to an increased likelihood of
microtrauma. In a series of over 1000 runners, heavier runners sustained
injuries more frequently than their lightweight companions (Pagliano and
Jackson, 1980).

· Improper footwear
Shoes that are not sufficiently firm along the medial border result in
increased pronation. Increased pronation has been implicated in Achilles
tendon pathology via the mechanism outlined above. A sole that is too
rigid is thought to increase the stress on the Achilles tendon and lead to
an increased risk of microtrauma and subsequent pathology (Subotnick,
1989). Additionally, insertional disorders of the Achilles tendon can be
caused by the shoe rubbing on the back of the heel, and paratenonitis may
also be secondary to irritation from a shoe counter (Subotnick, 1989;
Kvist, 1994).

Hopefully, if those involved in management of tendon overuse injuries
adopt the ‘tendinopathy’ paradigm, not only will physical treatment become
more effective but research into pharmacological management can look away
from the simple inflammatory model. I would be interested in peoples ideas
on the role of non-inflammatory substances such as glutamate and
substance P in pain production in tendinopathy.

Regards

Dan

Astrom M, Rausing A (1995) Chronic Achilles tendinopathy. A survey of
surgical and histopathologic findings. Clin Orthop 316: 151-164

Clement DB, Taunton JE, Smart GW (1984) Achilles tendinitis and
peritendinitis: etiology and treatment. Am J Sports Med 12: 179-184

Curwin S (1996) Tendon injuries: Pathophysiology and treatment. In:
Zachasewski JE, Magee DJ, Quillen WS (eds) Athletic injuries and
rehabilitation. WB Saunders Co, Philadelphia pp. 27-53

Jarvinen M, Jozsa L, Kannus P et al (1997) Histopathological findings
in chronic tendon disorders. Scan J Med Sci Sports 7: 86-95

Khan KM, Cook JL, Bonar F, Harcourt P, Astrom M (1999) Histopathology
of common tendinopathies. Sports Med 27: 393-408

Kvist M, Jozsa L, Jarvinen M (1992) Vascular changes in the ruptured
Achilles tendon and paratenon. Int Orthop 16: 377-382

Kvist M (1994) Achilles tendon injuries I athletes. Sports Med 18:
173-201

Leach RE, Dilovio E, Harney RA (1983) Pathologic hindfoot conditions
in the athlete. Clin Orthop 177: 116-121

Malone TR, Garrett WE, Zachasewski JE (1996) Muscle: injury and
repair. In: Zachasewski JE et al (eds) Athletic Injuries and
Rehabilitation. WB Saunders Co., Philadelphia

Norkin CC and Levangie PK. (1992) Joint stucture and function. A
comprehensive analysis. Philadelphia Press.

Subotnick SI (1989) (ed) Sports medicine of the lower extremity. New
York, Churchill Livingstone

Williams JG (1986) Achilles tendon lesions in sport. Sports Med 3:
114-135

Competing interests:
None declared

I concur with the points Lantos makes regarding the judicious and
brief use of NSAIDs in “occupational athletes” and problems of
distinguishing tendinitis from tendinopathy in the early stages.

Whilst Khan appears to focus on sports injuries, understandably
given that he is a Sports Physician, the principles he outlines in
relation to embracing “treatments that respect collagen damage” are
already commonplace in occupational health settings. Instead of “modifying
excessive training” one seeks to reduce the workload and ensure
appropriate breaks and in dealing with “aberrant limb biomechanics” one
advises on ergonomic adjustments to the workplace. The practical
difficulties arise in the early stages in relation to mobilization and
pain control. The main problem with “professional athletes” is stopping
them doing too much too soon whereas the main problem with “occupational
athletes” is exactly the opposite. In the latter group good pain control
and mobilization, along with the measures detailed above, is essential for
an effective and sustainable return to optimal working capacity. Personal
experience with Work Related Upper Limb Disorders suggests that if these
conditions are detected early enough most cases, if managed appropriately,
will resolve in less than 3 months.

TREATMENT FOR TENDINOPATHY

Practitioners who adopt the ‘tendinopathy’ paradigm underpin their
management with solid patient education – explaining that the condition
takes 3-6 months to resolve and why NSAIDs or corticosteroid therapy are
not likely to provide long-term benefit. 1 2 In addition to this
invaluable counselling they:

1. Prescribe strength training. In patients with tendinopathy,
various forms of strength training have resulted in improved outcomes in
several randomized controlled trials 3-8and a large controlled trial. 9
The training should focus on improving the strength, power and endurance
of the entire muscle-tendon unit in question, such the gastrocnemius-
soleus-Achilles tendon complex in Achilles tendinopathy. Regular
stretching is also a part of well-planned strength training program.
Patient education is crucial as the duration of all of the strength
training treatment protocols referenced was at least 12 weeks.

You are probably asking how strength training might work? 2 10 11.
This remains largely unknown but in animal experiments loading improved
collagen alignment of the tendon and stimulated collagen cross-linkage
formation, to improve tensile strength. 12 Tendon cells communicate their
response to mechanical loading with upregulation of gene expression
important for synthesis of the collagen protein. 13 14 Therefore, the
clinically-evident success of tendon strengthening programs has a sound
biological basis. 15

2. Embrace treatments that respect collagen damage. Appropriate
treatment may require some or all of: (a) modifying excessive training
to reduce absolute musculotendinous overloading; (b) reducing the relative
muscle-tendon overloading that results from aberrant limb biomechanics
(for example, strengthening the calf and hip muscles to reduce the forces
at the knee in a patient with patellar tendinopathy; 16 prescribing in-
shoe orthotics in Achilles tendinopathy or 17 elbow braces in lateral
epicondylar tendinopathy); (c) using modalities such as ice to minimize
pain and excessive tissue neovascularization. 18 We emphasise that more
research is needed to test all of these therapies – research that was
stymied while ‘tendinitis’ remained the culprit.

3. Interact closely with an expert physiotherapist. It is essential
that both physiotherapist and patient have a realistic time frame for
rehabilitation of patients with tendinopathy. 19 An experienced
physiotherapist can modify the patient’s training to effectively reduce
demand on a tendon without resorting to absolute rest, progress patients’
strengthening programs appropriately, implement the type of biomechanical
(and technical) corrections outlined and supervise successful return to
sport.

4. Refer to surgery as a last resort. If the initial prognosis the
patient receives is realistic, it is less likely that the patient will
attempt to return to sport prematurely, suffer re-injury, and thus, “fail”
conservative management. Tendinosis surgery permits around 60% of patients
to return to sport at the previous level, 20 21 and recovery takes several
months. Thus, surgery should be reserved for failure of a high-quality
program of rehabilitation and conservative management.

5. Anticipate new treatment options that will flow once the correct
pathology of tendon pain is addressed. These may include imminent
therapies such as growth factors to stimulate collagen synthesis 22and
somewhat more distant treatment such as nitric oxide synthase isoform
treatments 23 and gene therapy.

We agree with Dr Glaser that the road to successful treatment of
tendinopathy is not yet clearly marked. Nevertheless, acknowledging that
‘tendinitis’ is the wrong pathway for treating tendinopathy is essential.
Doing so encourages clinicians and researchers to seek novel solutions to
the problem of collagen breakdown.

Karim Khan, Pekka Kannus, Jill Cook, Nic Maffulli, Fiona Bonar

1. Cook JL, Khan KM, Maffulli N, Purdam C. Overuse tendinosis, not
tendinitis: Part 2. Applying the new approach to patellar tendinopathy.
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2. Józsa L, Kannus P. Human tendons. Champaign, Illinois: Human Kinetics,
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3. Mafi N, Lorentzon R, Alfredson H. Superior short-term results with
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6. Cannell LJ, Taunton JE, Clement DB, Smith C, Khan KM. A randomized
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9. Alfredson H, Pietila T, Jonsson P, Lorentzon R. Heavy-load eccentric
calf muscle training for the treatment of chronic Achilles tendinosis.
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10. Khan KM, Cook JL. Overuse tendon injuries: Where does the pain come
from? Sports Medicine and Arthroscopy Reviews 2000;8(1):17-31.

11. Khan KM, Cook JL, Maffulli N, Kannus P. Where is the pain coming from
in tendinopathy? It may be biochemical, not only structural, in origin.
BJSM 2000;34:81-84.

12. Vilarta R, de Campos Vidal B. Anisotopic and biomechanical properties
of tendons modified by exercise and denervation: aggregation and
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13. Banes AJ, Horesovsky G, Larson C, Tsuzaki M, Judex S, Archambault J,
et al. Mechanical load stimulates expression of novel genes in vivo and in
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14. Banes AJ, Weinhold P, Yang X, Tsuzaki M, Bynum D, Bottlang M, et al.
Gap junctions regulate responses of tendon cells ex vivo to mechanical
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and ligaments. II. The relationship between immobilization and exercise on
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16. Cook JL, Khan KM, Purdam CR. Conservative treatment of patellar
tendinopathy. Physical Therapy in Sport 2001;2:54-65.

17. McCrory JL, Martin DF, Lowery RP, Cannon DW, Curl WW, Read HM, et al.
Etiologic factors associated with Achilles tendinitis in runners. MSSE
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18. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles
tendons with painful tendinosis but not in normal tendons: an
ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc
2001;9(4):233-8.

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20. Coleman BD, Khan KM, Maffulli N, Cook JL, Wark JD. Studies of surgical
outcome after patellar tendinopathy: Clinical significance of
methodological deficiencies and guidelines for future studies.
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21. Tallon C, Coleman BD, Khan KM, Maffulli N. Outcome of surgery for
chronic achilles tendinopathy. A critical review. Am J Sports Med
2001;29(3):315-20.

22. Aspenberg P, Forslund C. Bone morphogenetic proteins and tendon
repair. Scand J Med Sci Sports 2000;10(6):372-5.

23. Lin J, Wang MX, Wei A, Zhu W, Murrell GA. The cell specific temporal
expression of nitric oxide synthase isoforms during achilles tendon
healing. Inflamm Res 2001;50(10):515-22.