Sports Med 2008; 38 (11): 881-891 0112-1642/08/0011-0881/$48.00/0
LEADING ARTICLE
ª 2008 Adis Data Information BV. All rights reserved.
Strategies for Improving Performance in Long Duration Events Olympic Distance Triathlon Christophe Hausswirth1 and Jeanick Brisswalter2 1 Institut National du Sport et de L’Education Physique (INSEP), Research Mission, Laboratory of Biomechanics and Physiology, Paris, France 2 Sport Ergonomics and Performance Laboratory, University of Toulon-Var, La Garde, France
Abstract
This review focuses on strategic aspects that may affect performance in a long-duration Olympic event, the Olympic distance triathlon. Given the variety of races during the Olympic Games triathlon, strategic aspects include improving technological features as well as energetics factors affecting overall triathlon performance. During the last decade, many studies have attempted to identify factors reducing the metabolic load associated (or not) with the development of fatigue process by analysing the relationship between metabolic and biomechanical factors with exercise duration. To date, a consensus exists about the benefit of adopting a drafting position during the swimming or the cycling part of the triathlon. Other potential strategic factors, such as the production of power output or the selection of cadence during the cycling or the running leg, are likely to affect the overall triathlon performance. Within this approach, pacing strategies are observed by elite athletes who swim or cycle in a sheltered position, inducing several changes of pace, intensity or stochastic shifts in the amplitude of the physiological responses. The analysis of these parameters appears to arouse some experimental and practical interest from researchers and coachers, especially for long-distance Olympic events.
In human locomotion, theoretical best performance times are set by the product of the energy cost of the locomotion (i.e. the amount of metabolic energy spent to move over one unit of distance) and the maximal metabolic power (i.e. a . function of maximal oxygen uptake [VO2max] and maximal anaerobic capacity).[1,2] Thus, the energy cost of locomotion represents the efficiency of athletes and appears to contribute to the variation found in distance performance among top-level athletes. Endurance events such as triathlon or
marathon running are known to modify athletes’ biological constants and should have an influence on their efficiency. This has classically been shown to be important in sports performance, especially in events such as long-distance running, cycling or triathlon.[1-3] In competition events, the energy cost for a given power output is dependent on both the energy needed to overcome the external resistance (adenosine triphosphate) and the energy used in the production of external energy (internal energy). Consequently, the energy cost
Hausswirth & Brisswalter
882
ª 2008 Adis Data Information BV. All rights reserved.
45 40 35 30 25 20 15 10 5 0
L1, L2 L3, L4 L5, L6
†† †* †
†
†
†* †*
AP M %
>1 30
% 30 30%.[2,3] Low back pain is one of the most common reasons for missed playing time in professional athletes, yet the prevalence among recreational athletes is not well known. In the athletic population, the majority of low back pain is mechanical and is thought to be related to muscle strain or sprains of the ligamentous structures of the lower back. Disc herniation, compression fracture, spinal stenosis, and degenerative disease can occur in the mature athlete. In young athletes, the most common diagnosis is spondylolysis.[4] Sports Med 2008; 38 (11)
Rheumatic Diseases and Sports-Related Injuries
It is interesting to note that disorders simulating athletic injury, including tumours and inflammatory connective tissue disease, may be encountered.[5] It has been estimated that about 5% of patients with chronic low back pain seen in the primary care setting are classified as having spondyloarthritis.[6] Another study in the US found that of all patients with back pain in primary care clinics, 0.3% have a diagnosis of ankylosing spondylitis (AS).[1] AS is a chronic inflammatory disease that belongs to the group of diseases called spondyloarthritis. Besides AS, which is the most frequent, spondyloarthritis comprises reactive arthritis or Reiter’s syndrome, arthritis/spondylitis associated with inflammatory bowel disease (enteropathic arthritis), arthritis/spondylitis with psoriasis or psoriatic arthritis, and undifferentiated spondyloarthritis. The leading clinical symptoms for all subsets of spondyloarthritis are inflammatory back pain and/or asymmetrical arthritis, predominantly of the lower limbs.[6] The European Spondyloarthropathy Study Group published a study aimed at developing classification criteria for the entire group of spondyloarthritis, with the specific intention of including patients with undifferentiated spondyloarthritis. The following classification criteria for spondyloarthritis were proposed: inflammatory spinal pain or synovitis (asymmetric or predominantly in the lower limbs), together with at least one of the following: positive family history, psoriasis, inflammatory bowel disease, urethritis, acute diarrhoea, alternating buttock pain, enthesopathy, or sacroiliitis as determined from radiography of the pelvic region.[7] Inflammatory low back pain is the hallmark of AS and is defined as pain associated with significant stiffness (especially morning stiffness for >1 hour), present for at least 3 months’ duration that improves with exercise, but is not relieved by rest.[8] Axial manifestations are seen less frequently in the other diseases and occur in 40% of patients with reactive arthritis, 10% in those with inflammatory bowel disease, and only 5% in persons with psoriatic spondyloarthritis.[6] Evaluating the incidence of AS in athletes, Wordsworth and Mowat[9] performed a review of ª 2008 Adis Data Information BV. All rights reserved.
919
100 patients with AS and found that 61% of them had participated in regular athletic activity in their youth. The authors found that 30 of 45 male AS patients who exercised regularly had to reduce their activity level at an average age of 23 years. In contrast, the 30 healthy controls in this study continued to engage in their sports to an average age of 29 years. The most frequent initial symptoms of the patients with AS were low back pain (41%) and sciatica-like pain (25%). Given these symptoms, a physician might easily initially mistake AS for a sport-related injury. It has become increasingly evident that in many patients with AS, it takes years from the onset of inflammatory low back pain until the appearance of radiographic sacroiliitis. This is especially true in women, who may never develop radiographic changes. For example, Dick Tayler, a winner of the 10 000-m race at the 1974 Commonwealth games, had been continually plagued by low back pain and Achilles tendon disorders. He was later diagnosed as having AS, the consequences of which forced him to stop running.[10] The absence of radiographic sacroiliitis in the early stage of disease does not necessarily indicate absence of inflammation in the sacroiliac joint or other parts of the axial skeleton. Recent application of magnetic resonance imaging (MRI) techniques have demonstrated (and confirmed) that ongoing active inflammation does in fact occur in the sacroiliac joint or the spine prior to its appearance on plain radiographs. In light of this, some authors have proposed new or revised criteria to allow the early diagnosis of AS, especially since more effective treatment options have become available. New or revised criteria may comprise all parameters relevant to axial spondyloarthritis including inflammatory back pain, heel pain (enthesitis defined as the inflammation of the enthuses, which are any point of attachment of skeletal muscles or ligaments to bone), peripheral arthritis, dactylitis, acute anterior uveitis, family history of spondyloarthritis, good response to NSAIDs, elevated acute-phase reactants, human leucocyte antigen B27 (HLA-B27), sacroiliitis Sports Med 2008; 38 (11)
Jennings et al.
920
(demonstrated on radiograph), and relevant MRI findings.[11] Until recently, the options available to clinicians for treating AS have been limited, with patient education, physical therapy, and NSAIDs being the mainstay of effective therapy. The advent of tumour necrosis factor-a (TNFa) antagonists represents a breakthrough in treating AS. Etanercept, infliximab and adalimumab, the three TNFa antagonists currently approved for the treatment of AS, have been demonstrated as being rapid and consistently effective in reducing the axial and peripheral symptoms and improving patients’ ability to function and their quality of life.[12,13] The physician assisting young athletes with low back pain with inflammatory characteristics must take into consideration the differential diagnosis with spondyloarthritis, especially AS. A high index of suspicion, early diagnosis and prompt treatment are crucial for slowing disease progression and enabling the athlete to maintain the greatest physical function. 2. Neck Pain Although the most common causes of neck pain are mechanical, the differential diagnosis for neck pain in athletes may be quite extensive and difficult. One should consider atypical cases of early rheumatoid arthritis (RA) and AS that may present with neck pain as the main symptom and when the symptoms appear to be more inflammatory than typically seen with soft-tissue or degenerative disorders. The polyarthropathy of RA affects the joints of the spine, and particularly the upper cervical spine.[14] Several studies of patients with RA suggest that the cervical spine becomes involved early in the course of disease, often within the first 2 years following the diagnosis. However, rheumatoid involvement of the cervical spine is often asymptomatic.[15] Patients with obvious arthritis in the hands are at increased risk for symptomatic cervical spine abnormalities. When the disease is unquestionably established, cervical spine radiographic abnormalities may include atlantoaxial (C1–2) subluxation, superior migration of the odontoid, subaxial ª 2008 Adis Data Information BV. All rights reserved.
arthritis, and collapse of the lateral masses of C1 from erosion at the facet joints.[16] Patients with diagnosed RA are at increased risk of spinal cord injury while participating in collision sports because of the increased incidence of cervical instability. Cervical subluxation may be found in 15% of RA patients within 3 years of diagnosis; 17% of RA patients with radiographic abnormalities have neurological symptoms.[17] Thus, a high index of suspicion is important for RA diagnosis when athletes complain of inflammatory neck pain especially with peripheral joint involvement. As cited above, spondyloarthritis, especially AS, usually affects men and starts in the lumbar spine and sacroiliac joints and subsequently spreads up to the thoracic and cervical spine. However, the disease may present with neck pain as the first manifestation without lower back pain or tenderness of sacroiliac joints, especially in women. Clinically, AS may present as gradual neck pain, stiffness and deformity that can cause great difficulty in performing everyday tasks and lead to a predisposition to fracture, dislocation and atlantoaxial subluxation.[18] Because of the mass fusion process of AS and altered biomechanical state, these patients are at high risk for sustaining spinal fractures that frequently occur after minor trauma and occasionally after no apparent or identifiable trauma. They are common in the lower cervical spine and occur frequently through the intervertebral disc.[19,20] There have also been case reports of cervical fracture in patients with AS following chiropractic manipulation.[21] 3. Hip and Groin Pain Hip or groin pain seems to occur frequently in sports involving twisting and turning, such as football, soccer, ice hockey, or basketball as well as in sports such as running with repetitive impact.[22] Pain may originate from the hip joint and its surrounding structures, as is seen with a labral tear, osteochondral defect, hip-joint synovitis, stress fractures of the femoral neck, and trochanteric bursitis. It also may arise from the adductor muscles where chronic muscle strain or tendinopathy Sports Med 2008; 38 (11)
Rheumatic Diseases and Sports-Related Injuries
occur. Injury to the pubic bones may result in a pubic ramus fracture or osteitis pubis and can be the cause of a patient’s symptoms. Likewise, the lower abdominal muscles may be implicated in iliopsoas strain, rectus abdominis tendonopathy, or sports hernia. The lower thoracic spine, lumbar spine, and sacroiliac joint may refer pain to the groin. However, less common causes of pain in this region, such as some rheumatic disorders, must be considered.[23] The rheumatic diseases that can present as arthritis of the hip are spondyloarthritis (especially AS), RA, gout and pseudogout. Lovell[23] reviewed the case notes of 189 athletes with chronic groin pain. Diagnoses were determined following a review of their history, clinical examination, local anaesthetic infiltration, radiological investigation, surgical exploration, and clinical progress. The most common pathology was incipient hernia (50%). Other common diagnoses were adductor lesions, osteitis pubis, pubic instability, iliopsoas injuries, spinal nerve compression (referred to groin), rectus abdominis tendonopathy, and stress fractures. Only one patient was diagnosed as having AS, as he presented with sacroiliitis on a bone scan and tested positive for the HLA-B27 antigen. An example of a difficult and rare diagnosis of the hip and groin pain was described by Doward and co-workers.[24] They reported a case of a 34-year-old Olympic-calibre cyclist who presented with a 1-year history of progressive left hip and groin pain. Her symptoms initially began when she was running, but progressed to the point where they occurred with walking, cycling and lying on the hip. Clinical examination revealed moderately decreased internal rotation, external rotation, forward flexion, and abduction of the left hip compared with the right; and subjective complaints of deep hip pain with internal or external rotation. A radiograph of the left hip revealed slight hip joint narrowing centrally. An MRI arthrogram revealed a small anterior labral tear and innumerable small intermediateintensity filling defects situated diffusely within the joint fluid thought to be consistent with extensive reactive synovitis in the left hip. Arthroscopic removal of loose bodies was performed ª 2008 Adis Data Information BV. All rights reserved.
921
and operative evaluation revealed no real labral tear, but damage at the labral cartilaginous junction anteriorly, some damage to the femoral head, and hundreds of cartilaginous loose bodies within the joint. After histological examination, the diagnosis of synovial chondromatosis was made. Seventeen months after surgery, this patient was able to return to her previous athletic activities. The authors suggested that with the increased awareness of labral tears as a source of hip pain in athletes it is important for physicians to keep other causes of hip synovitis in mind. McCurdie and Perry[25] reported two cases of haemochromatosis in patients who presented with exercise-related joint pain especially in the hip/groin initially attributed to their running. The patients were a 51-year-old female recreational runner, and a 34-year-old male keen road runner. In addition to hip pain, both subjects progressed with pain and stiffness over the second and third metacarpophalangeal joints. The female runner had no symptoms or signs of chronic liver disease or endocrine disturbance. She did, however, have plain radiographs showing degenerative changes in her hands, with hooked osteophytes at second and third metacarpals and both subtalar and talonavicular joints, as well as minor degenerative changes in both hips. The male runner presented with mild hepatomegaly and persistently increased liver function tests, with early fibrosis and heavy iron staining (but no cirrhosis) on liver biopsy. Also, plain x-ray films showed degenerative changes of the hips. In both cases, ferritin concentration was >1000 mg/L. They had a diagnosis of haemochromatosis and were referred to treatment with venosection. Their joint pains and arthropathy continued despite treatment, and they had bilateral total hip replacement. The authors conclude that the diagnosis of haemochromatosis is easily overlooked in patients presenting with exercise-related joint pain if the symptoms are attributed solely to their exercise and sporting activities. Idiopathic haemochromatosis is an inherited disorder of iron metabolism in which excess iron absorption leads to tissue damage associated with characteristic arthropathy. As many as 64% of patients with haemochromatosis develop arthropathy that has been recognized as an early manifestation and predominant clinical factor Sports Med 2008; 38 (11)
Jennings et al.
922
affecting the quality of life of these patients.[26] Phlebotomy, the metal depletion treatment of choice in haemochromatosis, markedly improves survival and prevents complications.[27]
4. Peripheral Arthropathy With rare exceptions, any joint disorder is capable of presenting initially as monoarthritis.
Nonetheless, it is almost always possible to identify patients who need prompt evaluation and treatment to prevent rapid disease progression such as those with suspected septic arthritis. The physician must first attempt to localize the anatomical site of the abnormality. Joint pain may be the result of abnormalities of the joint itself, adjacent bone, surrounding ligaments, tendons, bursae, or soft tissue.[28] The range of disorders causing monoarthritis is listed in table I.
Table I. Differential diagnosis of peripheral arthritis (reproduced from McCune and Golbus,[28] with permission. Copyright ª Elsevier 2005) Usually monarticular
Often polyarticular
Common Septic arthritis bacterial
Rheumatoid arthritis Osteoarthritis
tuberculosis
Psoriatic arthritis
fungal
Reactive arthritis
Lyme disease Crystal disease
Calcium pyrophosphate deposition disease Most juvenile rheumatoid arthritis and juvenile spondylitis
gout
Systemic lupus erythematosus
pseudogout
Erythema nodosum
Internal derangement
Acute hepatitis B/C
Ischaemic necrosis
Rubella
Haemarthrosis
Lyme disease (usually £4 joints)
Trauma or overuse
Parvovirus
Pauciarticular juvenile rheumatoid arthritis
Other crystal-induced arthropathies
Congenital hip dysplasia
Enteropathic arthritis
Osteochondritis dissecans
HIV
Haemoglobinopathies Loose body Paget’s disease involving joint Stress fracture Osteomyelitis Osteogenic sarcoma Metastatic tumour Synovial osteochondromatosis Rare Pigmented villonodular synovitis
Whipple’s disease
Familial Mediterranean fever
Chronic sarcoidosis
Intermittent hydrarthrosis
Still’s disease
Behc¸et’s disease
Pulmonary hypertrophic osteoarthropathy
Regional migratory osteoporosis
Chondrocalcinosis-like syndromes due to ochronosis,
Amyloidosis (associated with myeloma or renal failure)
haemochromatosis, Wilson’s disease Rheumatic fever Paraneoplastic syndromes Polymyalgia rheumatica
ª 2008 Adis Data Information BV. All rights reserved.
Sports Med 2008; 38 (11)
Rheumatic Diseases and Sports-Related Injuries
Of utmost importance is evaluation for septic arthritis, which is uncommon in the normal joint, but the possibility should be considered in joints recently drained or in patients with arthritis, diabetes mellitus or impaired immune function.[29] Synovial biopsy may play a role in the diagnosis of chronic, unexplained monoarticular arthritis, especially tuberculous synovitis.[28] Once infection is ruled out, certain rheumatic conditions must always be considered. Common diseases such as RA, gout, and pseudogout, or rarer diseases such as pigmented villonodular synovitis (PVNS) and intermittent hydrarthrosis may present as an acute monoarthritis. The patient history and physical examination are essential in determining the diagnosis. Inflammatory arthritis is characterized by stiffness of the affected joint that is most noticeable in the morning (morning stiffness of >1 hour) or after a period of inactivity (gelling) and that improves with motion. Also, inflammatory arthritis may often be associated with constitutional symptoms, such as fever or malaise, and involvement of multiple joints.[28] Occasionally, patients may attend the sports medicine clinic with multiple joint pains (polyarthralgia) or multiple joint pains with synovitis (polyarthritis). In many of these conditions, the diagnosis is clinical. A key diagnostic feature is the onset and pattern of joint involvement along with the extra-articular manifestations. For example, RA typically affects the small joints symmetrically, while reactive arthritis has a propensity to asymmetric involvement of large joints of the lower limb.[29] In table I, we summarize the conditions that present as polyarthritis. 4.1 Autoimmune Arthritis
Autoimmune arthritis such as RA and AS have been described to present as a sports-related injury in athletes. Jari and Noble[30] reported five cases of patients presenting with meniscal tears that were subsequently found to have RA. All five patients were middle-aged men who presented with a history and physical signs suggestive of medial meniscal tearing. These signs included a sudden twisting episode, medial joint line tenderness, and ª 2008 Adis Data Information BV. All rights reserved.
923
a positive McMurray’s sign. Because MRI scans showed effusion and synovial thickening in addition to the medial meniscal tear, full blood count, erythrocyte sedimentation rate, and rheumatoid factor (RF) were also performed. In all patients, the erythrocyte sedimentation rate was raised and the RF was positive. In the three patients who had undergone surgery prior to their RF results being known, the surgical outcome was poor and results of the synovial biopsies were positive for RA. In two patients, surgery was deferred. These patients were successfully treated by a rheumatologist, and surgery was unnecessary. The authors suggest a policy of medical therapy to reduce inflammation in patients clinically suspected or diagnosed with RA before arthroscopic surgery is undertaken. Juvenile idiopathic arthritis is another diagnosis that should considered in athletes under the age of 16 years. Juvenile idiopathic arthritis identifies subtypes such as systemic arthritis, oligoarthritis, polyarthritis (RF-positive or -negative), enthesitisrelated arthritis, psoriatic arthritis and undifferentiated arthritis. Of special interest is the subtype enthesitis-related arthritis, which mainly affects males over the age of 6 years and is characterized by the association of enthesitis and arthritis. This arthritis commonly affects the joints of the lower extremity, especially the hips. The most common sites of enthesitis are the calcaneal insertions of the Achilles tendon, plantar fascia, and tarsal area. In some cases, arthritis could progress to affect the sacroiliac and spinal joints, thus producing the clinical picture of AS.[31] Although AS is known and named for spinal involvement, it can initially involve a peripheral joint, especially the shoulders and hips. Hill and Lombardo[32] described a case of AS presenting as shoulder pain in a 22-year-old athlete. This patient denied significant back pain and had been treated earlier with anti-inflammatory agents for the diagnosis of tendonitis. However, upon further questioning, the patient described intermittent episodes of iritis affecting both eyes. Results of his laboratory analyses revealed an elevated erythrocyte sedimentation rate, negative reactions to a RF test and antinuclear antibodies, and a positive test for HLA-B27. A pelvic roentgenogram Sports Med 2008; 38 (11)
Jennings et al.
924
revealed fused sacroiliac joints bilaterally and ischial periostitis with normal hip joints. Roentgenograms of his shoulder showed marked jointspace narrowing, osteoporosis, and joint erosions. Six months after treatment with indomethacin and exercises, the patient had improved range of motion in the shoulder, decreased pain, and he was playing racquet sports with minimal discomfort. Arthritis is one of the most common manifestations that patients with systemic lupus erythematosus (SLE) exhibit over time. SLE is most often associated with female gender. The symmetric polyarticular pattern is the most common presentation and typically there is no evidence of erosive disease despite a spectrum of inflammatory synovitis and soft tissue swelling around the joints. However, it is usually the associated fatigue that patients complain of as the most debilitating symptom.[33] Besides arthritis and fatigue, the physicians can confirm diagnosis based on the other systemic signs and symptoms of SLE such as malar or discoid rash, photosensitivity, serositis, haematological, neurological or renal disorders, and positive autoantibodies. 4.2 Crystal-Induced Arthritis
Another aetiology of peripheral arthritis in athletes is gout. Gout is a metabolic disorder characterized by deposition of uric acid crystals in connective tissues and articular cartilage. The onset of gout usually occurs between the ages of 30 and 50 years.[10] More than 90% of patients with primary gout are men, and the age of peak incidence in men is earlier than that of affected women, who rarely develop the disorder before menopause.[34] One case exists of a 33-year-old male marathon runner who was admitted to hospital with a 6-day history of fever, chills, malaise and pain in his right knee and ankle following a 10-mile (16-km) run. A similar episode 2 years earlier had occurred, but instead of knee and ankle, his elbow was affected and was treated with antibacterials. He attributed chronic musculoskeletal back and groin pain to running and often took ibuprofen, aspirin (acetylsalicylic acid), or inª 2008 Adis Data Information BV. All rights reserved.
domethacin for relief. His usual alcohol consumption was about six beers a day. Laboratory data revealed a uric acid level of 10.0 mg/dL (normal 3.4–7.0 mg/dL). The diagnosis was made after aspiration of the knee, which yielded 50 mL of fluid that contained negatively birefringent intracellular crystals. A systolic murmur was also evident on cardiac examination, and an echocardiogram was performed, which revealed mild aortic regurgitation at the site of a nodule on the right coronary leaflet. The authors suggested that this nodule was visceral tophi. The patient was treated with intravenous colchicine and oral indomethacin, and all of his symptoms went into remission. He was discharged on 10 days of oral colchicine followed by allopurinol (300 mg/day) continuously, and 8 months later he was running without difficulty.[35] Mair and colleagues[36] described a case of gout as a source of sesamoid pain in an 18-yearold male intercollegiate wrestler, although gout is extremely rare in teenagers and young adults.[37] This patient presented with insidious pain in the region of the right first metatarsophalangeal joint and first metatarsal head without a specific prior injury. Radiographs revealed the medial sesamoid to be partitioned with minimal irregularity at the separated margins. It was thought that the patient might have had a stress fracture of the medial sesamoid. He was fitted with a carbon fibre insole and later an extended steel shank, and he refrained from wrestling for 8 weeks. The patient’s symptoms resolved, but when he resumed wrestling, he gradually began experiencing more pain. The decision was made to proceed with surgical exploration, which revealed a chalky, white material in the fragments of medial sesamoid that were cystic. Birefringent needles consistent with monosodium urate crystals were identified in the curetted material. The final pathological report confirmed the diagnosis of gout of the medial sesamoid. Following surgery, the patient did well and was able to resume wrestling without pain 3 months later. His serum uric acid level was 7.8 mg/dL (normal 3.5–8.0 mg/dL) and in retrospect, it was noted that his father had longstanding gout of the first metatarsophalangeal joint. It is important to emphasize that Sports Med 2008; 38 (11)
Rheumatic Diseases and Sports-Related Injuries
actual determinations of solubility of monosodium urate in human plasma (or serum) indicate that saturation occurs at concentrations of about 7 mg/dL.[37] Exercise may increase serum uric acid by three mechanisms: (i) adenosine released by exercising muscle may be metabolized by purine nucleoside phosphorylase and xanthine oxidizes to produce uric acid; (ii) intense exercise and thermal stress may decrease renal blood flow and clearance of uric acid; and (iii) dehydration decreases plasma volume and increases the concentration of uric acid. Adding the fact that some athletes drink alcohol and take low doses of aspirin for overuse injuries, they are at increased risk for gout.[35] Pseudogout is a condition associated with deposition of calcium pyrophosphate dehydrate (CPPD) crystals and characterized by joint effusions with marked neutrophilia and a form of secondary osteoarthritis (OA) with a pattern of joint involvement that differs from primary OA. ‘Chondrocalcinosis’ is the term used to define the asymptomatic radiographic finding of calcification of articular or fibrocartilage most frequently related to CPPD deposition.[38] The cause of chondrocalcinosis is unclear, but it has been associated with several medical and hereditary problems. It has been reported to be common in patients with haemochromatosis, primary hyperparathyroidism and gout.[39] In addition to familial cases, another cause of chondrocalcinosis in young adults is thought to be trauma. Trauma-induced chondrocalcinosis tends to be monoarticular, involving the traumatized joint with degenerative changes, and occurs in relatively young persons without any predisposing medical condition. Trauma-induced monoarticular chondrocalcinosis has been found in internal derangements of the knee, hypermobile joints, and after surgery.[39] Another case report describes a 20-year-old man with a history of left knee discomfort of several months’ duration while training for and participating in an 800-m run for intercollegiate varsity track. He could not recall an episode of significant trauma and had no history of effusion or locking. He denied any known medical ª 2008 Adis Data Information BV. All rights reserved.
925
problems, medications, steroid use, or familial history of arthritis. Radiographs revealed what appeared to be a 2- to 3-mm round, calcified, loose body in the lateral compartment of the knee. The differential diagnosis at this time was an osteochondral fracture or osteochondritis dissecans. A knee arthroscopy was performed and revealed thick, white, semisolid material of toothpaste consistency from a cavity at the tibial plateau articular cartilage. This material was excised and under microscope examination was found to be CPPD crystals. Radiographs taken 3 weeks postoperatively revealed that calcification was absent. He remained asymptomatic at 10 months’ follow-up and resumed his normal schedule. The authors suggested that chondrocalcinosis must be included in the differential diagnosis of intra-articular calcified lesions in young athletes with knee pain.[39] 4.3 Lyme Disease
Sportsmen, backpackers, and outdoor athletes may acquire unusual infectious diseases in the fields and forests of the US. One of these conditions, Lyme disease, is a tick-borne multisystem disorder caused by the spirochete Borrelia burgdorferi. It characteristically initiates with a particular lesion on the skin known as erythema migrans, which may be followed by neurological, cardiac, or articular abnormalities. Inflammatory arthritis is the most recognized feature of persistent infection, and approximately 60% of untreated patients develop monoarticular or asymmetric oligoarticular arthritis primarily in the large joints, with objective physical findings of synovial thickening or joint effusion. The diagnosis of Lyme disease is a clinical one. The serological test should be used to confirm the clinical diagnosis.[40,41] Seldes and colleagues[41] have described a 20-year-old male university football player who presented with an atraumatic spontaneous haemarthrosis of the left knee. This patient denied recent infection, fever, chills, night sweats, history of bleeding abnormalities, or sexually transmitted diseases. Eight months before his clinic visit, the patient noticed a ‘red splotchy rash’, which was diagnosed as an allergic reaction by a Sports Med 2008; 38 (11)
Jennings et al.
926
dermatologist. Laboratory examinations, radiographs, and MRIs were not helpful. The diagnosis of Lyme arthritis was made based on his clinical examination and an unequivocally positive serological testing. After the treatment, which consisted of intravenous ceftriaxone 1 g/day for 14 days, the patient was asymptomatic. 4.4 Pigmented Villonodular Synovitis (PVNS)
Another uncommon cause of monoarthritis is PVNS. This benign disorder results in an increased proliferation of synovium, causing villous or nodular changes of synovial-lined joints, bursae, and tendon sheaths. Most patients present with monoarticular swelling, haemarthrosis, and a gradual increase in pain. The knee is the most common location followed by the hip, ankle and shoulder. Radiographic evaluation of PVNS often depicts increased soft-tissue density and may show bony erosions. MRI reveals low-signal intensity on both T1- and T2-weighted images. Histological examination confirms the diagnosis of PVNS. Partial or complete synovectomies are considered the treatment of choice.[42,43] A 30-year-old sportsman presented with knee pain after several twisting episodes during a game of football. On examination, there was specific anteromedial joint line pain, and results of a McMurray’s test were positive. A diagnosis of a medial meniscal tear was made. Arthroscopy, however, revealed a large pedicular lesion originating from the insertion of the anterior horn of the medial meniscus. Mini-arthrotomy was performed, and the diagnosis of PVNS was made after histological examination.[42] Mitchell and colleagues[44] reported a case of an 18-year-old division III college football player with a previous history of chondromalacia patella, who sustained a twisting injury of the right knee 3 days before presentation. He had a negative Lachman’s test. As he had a moderate effusion, aspiration of the joint was performed and yielded serosanguineous fluid. The clinical diagnosis was chondromalacia patella with irritation. After 6 months he returned complaining of a 1-month history of swelling and tenderness in the peripatellar area and over the vastus medialis ª 2008 Adis Data Information BV. All rights reserved.
muscle. On physical examination, he had a moderate effusion and crepitus over the lateral aspect of the patella and a possible intra-articular mass in that region. The clinical diagnosis at that time include a possible loose body with chondromalacia patella and a possible medial meniscal tear. Besides chondromalacia patella, MRI showed diffuse synovitis with probable PVNS. Arthroscopy was performed with shaving chondroplasty of the patella, and subtotal synovectomy. Histological evaluation confirmed the diagnosis of PVNS. Saxena and Perez[43] published a review of ten athletic patients with PVNS about the ankle. Most of the patients were previously involved in lateral motion sports such as basketball, tennis, soccer, or aerobics. Two patients ran for exercise. Nine of ten patients had a history of ankle sprains, with pain laterally. Plain radiographs showed bony changes about the talus and adjacent bones in four of ten patients; MRI showed PVNS findings in all ten. PVNS was found in multiple sites about the ankle including three ankle joints and two subtalar joints. All patients had synovectomy and tenosynovectomy, and eight were able to return to sports participation 4–12 months after surgery. 5. Soft Tissue Disorders Musculoskeletal soft tissue injuries are a leading cause of pain and disability in both competitive and recreational athletes. Incidence estimates are as high as 50% in distance runners.[45] Many of these injuries are acute tears or strain or are provoked by chronic muscle-tendon overload or overuse and muscle fibre ‘microtrauma’. However, these disorders may occasionally be a manifestation of a systemic rheumatic disease. 5.1 Bursitis
Bursae are small fluid-filled sacs located between tendons, muscles and bones that serve to cushion and reduce friction. Bursitis is defined as inflammation of these superficial or deep bursal sacs. The most common sites of bursitis included the olecranon bursa over the elbow region, the Sports Med 2008; 38 (11)
Rheumatic Diseases and Sports-Related Injuries
trochanteric bursa in the hip, and the overlooked anserine bursa over the medial aspect of the knee. The presenting symptom is pain. Obvious swelling is seldom present except in the most superficial areas such as the elbow or knee. Besides local irritation and infection, bursitis can be associated with gout. Olecranon bursitis is especially more common in patients with gout or RA. In these cases, aspiration can be useful to determine the aetiology of the disorder.[46] Septic bursitis should always be considered for patients who have diabetes or who use intravenous drugs as well as for anyone who is immunocompromised. Patients with infected bursae usually have exquisite tenderness, redness, and heat over the bursal site and may have an elevated body temperature.[46] 5.2 Tendinopathies
Tendinopathies are often related to increased age, muscle imbalance, and anatomic malalignment. The most common sites are the supraspinatus, finger flexors, patellar and Achilles tendons.[46] Some tendinopathies, particularly lateral epicondylitis, have been associated with certain sports and occupational activities, in keeping with a presumed mechanical aetiology. One study found an increased prevalence of RF in patients with repeating lateral epicondylitis and wrist tenosynovitis suggesting that there may be an underlying predisposition to generalized rheumatic disease in some cases.[47] The frequency of tendon involvement in patients with RA has been reported to be as high as 64%, although most studies report lower frequencies. The most frequent sites for rheumatoid tendonitis are the hand extensors and flexors.[48] This is typically seen in the setting of synovitis and/or deformity. The number and incidence of tendon injuries in general have increased substantially during the last few decades, and this increase has been dominated by problems with the Achilles tendon. Because most Achilles tendon injuries take place in sports and there has been a common upsurge in sporting activities, the number and incidence of the Achilles tendon overuse injuries and complete ª 2008 Adis Data Information BV. All rights reserved.
927
ruptures have increased in industrialized countries. In general, Achilles tendon problems arise from two origins: (i) excessive loading-induced degeneration of the tendon; and (ii) the tendon becomes the site for a systemic disease (e.g. gout, pseudogout, spondyloarthropathies and RA).[48] Although there is no description of tendon rupture in athletes due to rheumatic disease, it is described that RA, gout, CPPD deposition and SLE can lead to tendon rupture in young individuals. Among all tendon ruptures in RA, the most frequently ruptured tendons are hand extensors; all the other locations are clearly less common.[48] In RA, tendon rupture may occur, possibly by the overproduction of matrix metalloproteinases.[49] Gout has been described as a cause of peroneus tendon rupture in the presence of tophaceous gouty infiltration.[50] Although rare, extensor tendon rupture at the wrist associated with CPPD deposition has been described.[51] SLE can cause nonerosive joint deformities, but rarely can lead to spontaneous tendon rupture.[52] 5.3 Enthesitis
Enthesitis is defined as any pathological condition involving the entheses. The entheses are any point of attachment of skeletal muscles or ligaments to bone, where recurring stress or inflammatory autoimmune disease can cause inflammation or occasionally fibrosis and calcification. Plantar fasciitis is considered an enthesitis, and it is a common diagnosis in athletes usually having a mechanical aetiology. Other common sites are the ischial tuberosities, greater trochanters, spinous processes, costochondral and manubriosternal junctions, and iliac crests.[8] Enthesitis is also one of the main diagnostic criteria of spondyloarthritis, especially AS. However, spondyloarthritis presents with other inflammatory features such as low back pain with stiffness, peripheral asymmetric arthritis and elevated acute-phase reactants.[8] 5.4 Carpal Tunnel Syndrome
Carpal tunnel syndrome (CTS) is the most commonly diagnosed compression neuropathy in Sports Med 2008; 38 (11)
Jennings et al.
928
the upper extremity. It usually begins as an isolated phenomenon, but symptoms of CTS can accompany many systemic diseases, such as congestive heart failure, amyloidoisis associated with multiple myeloma, hypothyroidism and tuberculosis. More commonly, CTS is associated with conditions such as pregnancy, diabetes, obesity, and any inflammatory arthritis affecting the wrist such as RA and gout.[53] The classic constellation of symptoms consists of weakness or clumsiness of the hand; paraesthesias in the thumb, index, and long fingers; and nocturnal paraesthesias in the affected digits. Patients may often complain of forearm and elbow pain that is aggravated by activities, but is poorly localized and aching in nature. The diagnosis of CTS is usually clinical. Bilateral electrodiagnostic tests should be used to confirm the diagnosis, particularly in patients with significant motor loss, atrophy or constant sensory loss or in patients with atypical signs or symptoms.[53]
The most common activities associated with the syndrome are those that require constant wrist flexion or use of vibrating tools. The symptoms of other disorders such as cervical disc disease, thoracic outlet syndrome, and more proximal entrapment of the median nerve may be confused clinically with CTS and need to be ruled out.[46]
6. Practical Recommendations Effective management of athletes presenting with musculoskeletal complaints requires a structured history, physical examination, and definitive diagnosis that distinguish the soft tissue problem from a joint problem and an inflammatory syndrome from a noninflammatory syndrome. Clues to a systemic inflammatory aetiology may include constitutional symptoms, morning stiffness, elevated acute-phase reactants and progressive
Table II. Clinical features and laboratory tests recommended to investigate rheumatic diseases Rheumatic disease
Clinical features
Laboratory tests
Rheumatoid arthritis
Small hand (MCP, PIP) and foot symmetric synovitis Tenosynovitis Carpal tunnel syndrome
Rheumatoid factor, anti-CCP antibody Radiographic changes (erosions or bony decalcification) Elevated ESR and CRP
Ankylosing spondylitis
Inflammatory low back pain, morning stiffness of >1 h Large joint synovitis Enthesitis Family history of spondyloarthritis Acute anterior uveitis/iritis
Radiographic sacroiliitis Elevated ESR and CRP HLA-B27 MRI findings of sacroiliitis
Gout
Arthritis of the first MTP joint Lower limb joint synovitis Tophi History of excessive alcohol ingestion
High uric acid levels Radiographic changes: bony erosion with ‘overhanging edge’ Synovial fluid analysis on compensated polarized microscopy
Chondrocalcinosis (CPPD deposition)
Small hand (MCP, PIP) and foot synovitis Family history History of repetitive trauma
Radiographic changes: typical calcifications Synovial fluid analysis on compensated polarized microscopy Ferritin levels (associated with haemochromatosis)
Systemic lupus erythematosus
Nonerosive arthritis Systemic manifestations: malar rash, photosensitivity, oral ulcers, serositis, renal disorder, neurological disorder, haematological disorder
Complete blood count: haemolytic anaemia, leucopenia, thrombocytopenia Proteinuria Antinuclear antibody test Anti-DNA/anti-Sm Antiphospholipid antibodies
CCP = cyclic citrullinated peptide; CPPD = calcium pyrophosphate dehydrate; CRP = C-reactive protein; ESR = erythrocyte sedimentation rate; HLA = human leucocyte antigen; MCP = metacarpophalangeal; MRI = magnetic resonance imaging; MTP = metatarsophalangeal; PIP = proximal interphalangeal.
ª 2008 Adis Data Information BV. All rights reserved.
Sports Med 2008; 38 (11)
Rheumatic Diseases and Sports-Related Injuries
symptoms despite modification of physical activity. Also, the lack of injury mechanism suggests an underlying disease. In these circumstances, more complete workup is reasonable including radiographs, MRI and laboratory testing for autoantibodies. Table II summarizes the main clinical features and laboratory tests in the most common rheumatic diseases. 7. Conclusion There are many case reports of rheumatic diseases masquerading as a sports medicine condition. In the athlete with complaints of swollen joints, low back pain with stiffness, systemic symptoms, and without a history of trauma, inflammatory causes should be considered. The astute sports medicine practitioner should maintain an index of suspicion for rheumatic diseases as adequate and prompt treatment can modify disease progression, allowing the athlete to continue with regular exercise programmes. Acknowledgements No sources of funding were used in the preparation of this review and the authors have no conflicts of interest directly relevant to its contents.
References 1. Koes BW, van Tulder MW, Thomas S. Diagnosis and treatment of low back pain. BMJ 2006; 332 (7555): 1430-4 2. Bono CM. Low-back pain in athletes. J Bone Joint Surg Am 2004; 86-A (2): 382-96 3. Tall RL, DeVault W. Spinal injury in sport: epidemiologic considerations. Clin Sports Med 1993; 12 (3): 441-8 4. Baker RJ, Patel D. Lower back pain in the athlete: common conditions and treatment. Prim Care 2005; 32 (1): 201-29 5. Harvey J, Tanner S. Low back pain in young athletes: a practical approach. Sports Med 1991; 12 (6): 394-406 6. Sieper J, Rudwaleit M, Khan MA, et al. Concepts and epidemiology of spondyloarthritis. Best Pract Res Clin Rheumatol 2006; 20 (3): 401-17 7. Dougados M, van der Linden S, Juhlin R, et al. The European Spondylarthropathy Study Group preliminary criteria for the classification of spondylarthropathy. Arthritis Rheum 1991; 34 (10): 1218-27 8. Van Der Linden S, Van Der Heijde D, Braun J. Spondyloarthropathies. In: Harris Jr ED, Budd R, Genovese M, et al., editors. Kelley’s textbook of rheumatology. 7th ed. Philadelphia (PA): Elsevier Saunders, 2005
ª 2008 Adis Data Information BV. All rights reserved.
929
9. Wordsworth BP, Mowat AG. A review of 100 patients with ankylosing spondylitis with particular reference to socio-economic effects. Br J Rheumatol 1986; 25 (2): 175-80 10. Smart GW, Taunton JE, Clement DB. Achilles tendon disorders in runners: a review. Med Sci Sports Exerc 1980; 12 (4): 231-43 11. Rudwaleit M, Khan MA, Sieper J. The challenge of diagnosis and classification in early ankylosing spondylitis: do we need new criteria? Arthritis Rheum 2005; 52 (4): 1000-8 12. Clegg DO. Treatment of ankylosing spondylitis. J Rheumatol Suppl 2006; 78: 24-31 13. Manadan AM, James N, Block JA. New therapeutic approaches for spondyloarthritis. Curr Opin Rheumatol 2007; 19 (3): 259-64 14. Choi D, Casey AT, Crockard HA. Neck problems in rheumatoid arthritis: changing disease patterns, surgical treatments and patients’ expectations. Rheumatology (Oxf) 2006; 45 (10): 1183-4 15. Kim DH, Hilibrand AS. Rheumatoid arthritis in the cervical spine. J Am Acad Orthop Surg 2005; 13 (7): 463-74 16. O’Dell JR. Rheumatoid arthritis: the clinical picture. In: Koopman WJ, editor. Arthritis and allied conditions. Vol. 1. Philadelphia (PA): Lippincott Williams & Wilkins, 2001: 1153-86 17. Dorshimer GW, Kelly M. Cervical pain in the athlete: common conditions and treatment. Prim Care 2005; 32 (1): 231-43 18. Chou LW, Lo SF, Kao MJ, et al. Ankylosing spondylitis manifested by spontaneous anterior atlantoaxial subluxation. Am J Phys Med Rehabil 2002; 81 (12): 952-5 19. Shen FH, Samartzis D. Cervical spine fracture in the ankylosing spondylitis patient. J Am Coll Surg 2005; 200 (4): 632-3 20. Smith MD, Scott JM, Murali R, et al. Minor neck trauma in chronic ankylosing spondylitis: a potentially fatal combination. J Clin Rheumatol 2007; 13 (2): 81-4 21. Rinsky LA, Reynolds GG, Jameson RM, et al. A cervical spinal cord injury following chiropractic manipulation. Paraplegia 1976; 13 (4): 223-7 22. Bradshaw C. Hip and groin pain. In: Brukner P, Khan K, editors. Clinical sports medicine. 2nd ed. Sydney (NSW): McGraw-Hill; 2001: 375-94 23. Lovell G. The diagnosis of chronic groin pain in athletes: a review of 189 cases. Aust J Sci Med Sport 1995; 27 (3): 76-9 24. Doward DA, Troxell ML, Fredericson M. Synovial chondromatosis in an elite cyclist: a case report. Arch Phys Med Rehabil 2006; 87 (6): 860-5 25. McCurdie I, Perry JD. Haemochromatosis and exercise related joint pains. BMJ 1999; 318 (7181): 449-51 26. Adams PC, Speechley M. The effect of arthritis on the quality of life in hereditary hemochromatosis. J Rheumatol 1996; 23 (4): 707-10 27. Aaseth J, Flaten TP, Andersen O. Hereditary iron and copper deposition: diagnostics, pathogenesis and therapeutics. Scand J Gastroenterol 2007; 42 (6): 673-81
Sports Med 2008; 38 (11)
930
28. McCune W, Golbus J. Monoarticular Arthritis. In: Harris Jr ED, Budd R, Genovese M, et al., editors. Kelley’s textbook of rheumatology. Vol. 1. 7th ed. Philadelphia (PA): Elsevier Saunders, 2005: 501-13 29. Carter N. Joint-related symptoms without acute injury. In: Brukner P, Khan K, editors. Clinical sports medicine. 2nd ed. Sydney (NSW): McGraw-Hill, 2001: 770-8 30. Jari S, Noble J. Meniscal tearing and rheumatoid arthritis. Knee 2001; 8 (2): 157-8 31. Ravelli A, Martini A. Juvenile idiopathic arthritis. Lancet 2007; 369 (9563): 767-78 32. Hill JA, Lombardo SJ. Ankylosing spondylitis presenting as shoulder pain in an athlete: a case report. Am J Sports Med 1981; 9 (4): 262-4 33. Petri MA. Systemic lupus erythematosus: clinical aspects. In: Koopman WJ, editor. Arthritis and allied conditions. Vol. 2. Philadelphia (PA): Lippincott Williams & Wilkins, 2001: 1455-79 34. Becker M. Clinical gout and the pathogenesis of hyperuricemia. In: Koopman W, editor. Arthritis and allied conditions. Vol. II. 14th ed. Philadelphia (PA): Lippincott Williams & Wilkins, 2001: 2281-313 35. Moore GE, Anderson AL. Runner with gout and an aortic valve nodule. Med Sci Sports Exerc 1995; 27 (5): 626-8 36. Mair SD, Coogan AC, Speer KP, et al. Gout as a source of sesamoid pain. Foot Ankle Int 1995; 16 (10): 613-6 37. Wortmann R, Kelley W. Crystal-induced inflammation. In: Harris Jr ED, Budd R, Genovese M, et al., editors. Kelley’s textbook of rheumatology. Vol. II. 7th ed. Philadelphia (PA): Elsevier Science, 2005: 1402-48 38. Molloy ES, McCarthy GM. Calcium crystal deposition diseases: update on pathogenesis and manifestations. Rheum Dis Clin North Am 2006; 32 (2): 383-400 39. LaPrade RF, Burnett II QM. Localized chondrocalcinosis of the lateral tibial condyle presenting as a loose body in a young athlete. Arthroscopy 1992; 8 (2): 258-61 40. Gove S, Slutkin G. Infections acquired in the fields and forests of the United States. Emerg Med Clin North Am 1984; 2 (3): 623-33 41. Seldes R, Glasgow SG, Torg JS. Atraumatic spontaneous hemarthrosis associated with Lyme arthritis: a case report. Clin Orthop Relat Res 1993 (297): 269-71 42. Roach R, dos Remedios I. Localised pigmented villonodular synovitis: an uncommon cause of knee pain mimicking a meniscal tear. Br J Sports Med 2003; 37 (4): 368-9
ª 2008 Adis Data Information BV. All rights reserved.
Jennings et al.
43. Saxena A, Perez H. Pigmented villonodular synovitis about the ankle: a review of the literature and presentation in 10 athletic patients. Foot Ankle Int 2004; 25 (11): 819-26 44. Mitchell IL, Martin DF, Pope TL, et al. Diffuse pigmented villonodular synovitis in a college football player. J South Orthop Assoc 1997; 6 (1): 73-7 45. Hart LE. Exercise and soft tissue injury. Baillieres Clin Rheumatol 1994; 8 (1): 137-48 46. Burckhardt CS, Jones KD, Clark SR. Soft tissue problems associated with rheumatic disease. Lippincotts Prim Care Pract 1998; 2 (1): 20-9 47. Malmivaara A, Viikari-Juntura E, Huuskonen M, et al. Rheumatoid factor and HLA antigens in wrist tenosynovitis and humeral epicondylitis. Scand J Rheumatol 1995; 24 (3): 154-6 48. Jarvinen TA, Kannus P, Paavola M, et al. Achilles tendon injuries. Curr Opin Rheumatol 2001; 13 (2): 150-5 49. Bourikas LA, Kritikos HD, Papakostantinou OG, et al. Chronic alcohol consumption as a predisposing factor for multiple tendon ruptures in unusual sites in a patient with rheumatoid arthritis. Clin Exp Rheumatol 2007; 25 (3): 461-3 50. Lagoutaris ED, Adams HB, DiDomenico LA, et al. Longitudinal tears of both peroneal tendons associated with tophaceous gouty infiltration: a case report. J Foot Ankle Surg 2005; 44 (3): 222-4 51. Ariyoshi D, Imai K, Yamamoto S, et al. Subcutaneous tendon rupture of extensor tendons on bilateral wrists associated with calcium pyrophosphate dihydrate crystal deposition disease. Mod Rheumatol 2007; 17 (4): 348-51 52. Cronin ME. Musculoskeletal manifestations of systemic lupus erythematosus. Rheum Dis Clin North Am 1988; 14 (1): 99-116 53. Swigart C, Scott W. Hand and wrist pain. In: Harris Jr ED, Budd R, Genovese M, et al., editors. Kelley’s textbook of rheumatology. Vol. I. 7th ed. Philadelphia (PA): Elsevier Science 2005: 623-36
Correspondence: Prof. Michael Fredericson, Division of Physical Medicine and Rehabilitation, Department of Orthopaedic Surgery, Stanford University School of Medicine, 300 Pasteur Drive, Edwards Building #R107, Stanford, CA 94305-5336, USA. E-mail:
[email protected] Sports Med 2008; 38 (11)
Sports Med 2008; 38 (11): 931-946 0112-1642/08/0011-0931/$48.00/0
REVIEW ARTICLE
ª 2008 Adis Data Information BV. All rights reserved.
Physiological Responses of Sickle Cell Trait Carriers during Exercise Philippe Connes,1 Harvey Reid,2 Marie-Dominique Hardy-Dessources,3 Errol Morrison4 and Olivier Hue1 1 Laboratory ACTES UPRES-EA 3596, Department of Physiology, University of the French West Indies, Campus de Fouillole, Pointe-a`-Pitre, Guadeloupe, French West Indies 2 Department of Basic Medical Sciences (Physiology Section), Faculty of Medical Sciences, University of the West Indies, Mona, Kingston, Jamaica, West Indies 3 Inserm, U763, University of the French West Indies, Pointe-a`-Pitre, Guadeloupe, French West Indies 4 University of Technology, Jamaica, Kingston, Jamaica, West Indies
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Sickle Cell Trait (SCT) and Anaerobic Performance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Epidemiological Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Laboratory Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. SCT and Aerobic Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Epidemiological Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Laboratory Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. The Paradox of Lactic Response: A Controversial Issue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Hypolactacidaemia, Normolactacidaemia or Hyperlactacidaemia during Exercise?. . . . . . . . 4. SCT, Clinical Risk and Exercise-Related Sudden Death . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Medical Complications and SCT: Fiction or Reality?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Exercise Sudden Death and SCT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Putative Causes of Exercise Sudden Death in SCT Carriers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
931 933 933 933 934 934 935 937 937 937 937 938 940 942
Growing evidence suggests that physiological responses during exercise in sickle cell trait (SCT) carriers might differ from persons with normal haemoglobin. Epidemiological and experimental results support the view that SCT carriers could be advantaged in certain anaerobic activities, but the underlying physiological and bio-cellular mechanisms remain unknown. Maximal aerobic physical fitness (i.e. maximal oxygen consumption and maximal aerobic power) is not affected by SCT; however, recent studies suggest that SCT carriers could be characterized by a lesser aerobic capacity. Discrepancies are frequently reported in the literature concerning lactate metabolism during exercise in this population. While some studies observed higher blood lactate concentration during exercise in individuals carrying SCT compared with subjects with normal haemoglobin, others described lower concentration, which suggests a paradoxical lower lactate production by exercising muscles and/or greater ability to clear circulating lactate in SCT
Connes et al.
932
carriers. One of the most debated topics is the clinically benign condition of SCT, particularly during strenuous exercise. SCT carriers are usually involved in physical exercise without developing medical complications; however, several authors have presented case reports of SCT carriers who have collapsed and died unexpectedly during or after exercise. Blood rheological, haemostatic and vascular adhesion mechanism abnormalities in combination with environmental factors, such as heat strain, might play a role in the occurrence of these fatal scenarios. Several physiological differences have been observed between SCT carriers and non-SCT carriers, which make it necessary to consider the former as a specific population in response to exercise.
Sickle cell anaemia (SCA or SS homozygous sickle cell disease) is an inherited blood disorder caused by a single point mutation in one of the genes encoding haemoglobin. This mutation results in the substitution of valine for glutamic acid in the sixth residue of the b chain leading to the presence of haemoglobin S (HbS), instead of HbA, in the red blood cells (RBCs). When RBCs from patients with SCA become deoxygenated in the capillaries, the HbS may polymerize, inducing the sickling process and giving rise to elongated crescent shape or sickled RBCs. Other factors such as lowered pH, RBC dehydration and hyperthermia are also known to prompt sickling. The sickled cells are rigid and hence poorly deformable, thus failing to negotiate the small channels of the microcirculation. The marked reduction in RBC deformability results in stasis in the microvasculature. The abnormal rheology of the sickle cells may be associated with inflammatory phenomena, which can contribute to the development of hypoxia, vaso-occlusive crisis and organ damage. Moreover, these rigid RBCs are more fragile than normal RBCs, and are prone to haemolytic episodes, often leading to anaemia. Sickle cell trait (SCT), in contrast, is the heterozygous form of SCA, which is marked by the presence of both HbS and HbA. Its prevalence is between 20% and 40% in the Black population of Africa,[1] 8–10% for African Americans[2] and 10% in the Caribbean Islands.[3] SCT, in contrast to SCA, is usually considered a benign disorder[4] and the longevity and morbidity of ª 2008 Adis Data Information BV. All rights reserved.
SCT carriers seems to compare favourably with subjects with HbA.[5] Although SCT is assumed to be benign, under unusual circumstances, more frequently in athletes and army recruits, it has been associated with the development of various forms of vasoocclusive events, often leading to death.[6-19] Therefore, several studies have been carried out to assess the ability of SCT carriers to perform different types of exercise of varying intensity and to compare the physiological responses with a control population who have the normal haemoglobin genotype HbAA. One of the first reports of SCT carriers participating in high-level sports was in the Mexico Olympic Games in 1968.[20,21] The authors investigated the association between athletic ability and single gene systems.[21] Although the study failed to demonstrate any relationships between athletic ability and a single gene system, the authors reported that ‘‘a sizeable number of Negroid Olympic athletes manifested the sickle cell trait.’’[21] Additionally, Le Gallais et al.[22] and Thiriet et al.[23] reported a prevalence of 13.7% and 18.6% SCT carriers in physical education and sports colleges in Ivory Coast and Cameroon, respectively. In other words, the percentages were similar to those observed in the general population of both countries. Therefore, SCT did not seem to be a limiting factor for participating in sports. However, different research findings support the view that SCT carriers could be advantaged or disadvantaged during exercise, depending Sports Med 2008; 38 (11)
Physiological Responses of Sickle Cell Trait Carriers
on the dominant energy pathway contributing to the re-synthesis of adenosine triphosphate (ATP).[24-30] This article reviews the physiological responses of SCT carriers during physical exercise. First, we focus on epidemiological and experimental results demonstrating an advantage of SCT carriers for certain anaerobic exercise. This is followed by the epidemiological and experimental works showing any limitation of SCT carriers in performing endurance exercise. Thirdly, we examine the paradox of lactic response in SCT carriers during exercise. Finally, the medical complications and possible mechanisms of exercise-related sudden death in SCT subjects are discussed. 1. Sickle Cell Trait (SCT) and Anaerobic Performance 1.1 Epidemiological Studies
Le Gallais et al.[31] reported the presence of one athlete with SCT during the semi-final of the 4 · 400 m in the Los Angeles Olympic Games of 1984. A large epidemiological study made on Ivory Coast track-and-field throw and jump champions between 1956 and 1995 demonstrated a higher percentage of SCT carriers, as compared with the percentage in the general population, suggesting that SCT might be a contributing factor for success in brief and explosive trackand-field events involving mainly anaerobic metabolism.[32] Thirty-four (27.8%) SCT carriers were identified among the 122 national champions studied; they won 78 national titles (24.5%) and established 37 national records (43.5%), distributed among the throw and jump events.[32] Interestingly, the women’s high-jump and men’s shot-put events had the highest percentages of SCT carrier record holders (90.9% and 87.5%, respectively). Indeed, it has been hypothesized that SCT could constitute an advantage in practicing anaerobic exercise at a very high competitive level. Le Gallais et al.[24] analysed the exercise performance in SCT carriers during the different National Ivory Coast athletic sports events and reported that SCT carriers established 32 of ª 2008 Adis Data Information BV. All rights reserved.
933
33 national records on running courses less than 400 m, suggesting a greater ability of SCT carriers to perform in short and intense running events than in endurance courses. Marlin et al.[33] observed a high prevalence of SCT carriers in the French National sprint team in 2000 (i.e. 18.75%), and the percentage of titles and records held by the SCT carriers was significantly higher than for the non-carriers (38.6% and 50% for men and women with SCT, respectively). These observations led several researchers to design laboratory studies to test whether anaerobic performance was greater in SCT carriers than in non-SCT carriers. 1.2 Laboratory Studies
A limited number of studies have examined anaerobic metabolism in SCT subjects using different exercise protocols. Overall, the findings have been controversial. Several authors hypothesized that the low affinity of HbS for oxygen within SCT carriers’ RBCs might cause repeated episodes of tissue hypoxia, causing exercising muscles to develop anaerobic capacity to compensate for the hypothetically low oxidative capacity.[29,34] It has been previously shown that repeated hypoxia may favour type II muscle fibre formation.[35] However, comparison of anaerobic performance and anaerobic metabolism (i.e. peak anaerobic power, maximal velocity, maximal braking force, blood lactate kinetics during exercise and recovery) during a force-velocity test between SCT carriers and a control group showed no significant difference between the two groups.[29] This result has been recently confirmed using another method to assess peak anaerobic power during a single 10-second cycling sprint.[27] The latter group of researchers also reported that the anaerobic work developed during the cycling sprint test did not differ between the two groups. Therefore, subjects with SCT and controls with normal haemoglobin seem to have similar anaerobic exercise performance and similar anaerobic exercise metabolism. These data do not confirm the hypothetical higher anaerobic metabolism suggested in subjects with SCT.[29] Sports Med 2008; 38 (11)
Connes et al.
934
In contrast, SCT carriers have been shown to reach higher performance during a jumpand-reach test than control subjects.[26] This result is in agreement with epidemiological studies showing greater percentages of SCT carriers as title holders (27.3%) and record holders (41.9%) in extremely brief and intense exercise,[32] but contrasts with the findings of Bile´ et al.[29] and Connes et al.[27] However, the exercise protocols used in these studies[27,29] are mainly dependent on the lactic anaerobic metabolism.[36] Jones et al.[37] noted that the energy required during fast-speed cycling was provided from instantly available ATP in muscle, the phosphocreatine system and anaerobic glycolysis. Despite the shortness of the force-velocity test, the anaerobic metabolism involved must be considered as both alactic and lactic.[37] The jump-and-reach test used in the study of Hue et al.[26] is considered as an exclusive alactic anaerobic test.[38] Thus, it appears that SCT carriers are not disadvantaged in extremely brief and intense exercise involving mainly alactic anaerobic metabolism. When exercise involves both alactic and lactic anaerobic metabolism, SCT carriers and subjects with normal haemoglobin had the same level of performance. Hue et al.[26] did not find any difference between SCT carriers and controls on a 100-m sprint, as previously shown by Le Gallais et al.[34] Many team sports require the participants to repeatedly produce maximal or near-maximal sprints of short duration (
