Aetiology of Skeletal Muscle 'Cramps' During Exercise: a Novel Hypothesis

Journal of Sports Sciences

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Aetiology of skeletal muscle ‘cramps’ during exercise: A novel hypothesis

M. P. Schwellnus , E. W. Derman & T. D. Noakes

To cite this article: M. P. Schwellnus , E. W. Derman & T. D. Noakes (1997) Aetiology of skeletal muscle ‘cramps’ during exercise: A novel hypothesis, Journal of Sports Sciences, 15:3, 277-285, DOI: 10.1080/026404197367281 To link to this article: http://dx.doi.org/10.1080/026404197367281

Published online: 01 Dec 2010.

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Download by: [Australian Catholic University] Date: 24 September 2017, At: 18:51 Journal of Sports Sciences, 1997, 15, 277-285

Aetiology of skeletal muscle `cramps’ during exercise: A novel hypothesis

M .P. SCH WELLN US,* E.W. D ERM AN and T.D. N OAKES

M RC/UCT B ioenergetics of Exercise Research Unit, University of Cape Town M edical School, Sports Science Institute of South Africa, PO B ox 115, Newlands 7725, South Africa

Accepted 3 September 1996

The aetiology of exercise-associated muscle cramps (EAMC), de® ned as `painful, spasmodic, involuntary contractions of skeletal muscle during or immediately after physical exercise’ , has not been well investigated and is therefore not well understood. This review focuses on the physiological basis for skeletal muscle relaxation, a historical perspective and analysis of the commonly postulated causes of EAMC, and known facts about EAMC from recent clinical studies. Historically, the causes of EAMC have been proposed as (1) inherited abnormalities of substrate metabolism (`metabolic theory’ ), (2) abnormalities of ¯ uid balance (`dehydration theory’ ), (3) abnormalities of serum electrolyte concentrations (`electrolyte theory’ ) and (4) extreme environmental conditions of heat or cold (`environmental theory’ ). Detailed analyses of the available scienti® c literature including data from recent studies do not support these hypotheses for the causes of EAMC. In a recent study, electromyographic (EMG) data obtained from runners during EAMC revealed that baseline activity is increased (between spasms of cramping) and that a reduction in the baseline EMG activity correlates well with clinical recovery. Furthermore, during acute EAMC the EMG activity is high, and passive stretching is effective in reducing EMG activity. This relieves the cramp probably by invoking the inverse stretch re¯ ex. In two animal studies, abnormal re¯ ex activity of the muscle spindle (increased activity) and the Golgi tendon organ (decreased activity) has been observed in fatigued muscle. We hypothesize that EAMC is caused by sustained abnormal spinal re¯ ex activity which appears to be secondary to muscle fatigue. Local muscle fatigue is therefore responsible for increased muscle spindle afferent and decreased Golgi tendon organ afferent activity. Muscles which cross two joints can more easily be placed in shortened positions during exercise and would therefore decrease the Golgi tendon organ afferent activity. In addition, sustained abnormal re¯ ex activity would explain increased baseline EMG activity between acute bouts of cramping. Finally, passive stretching invokes afferent activity from the Golgi tendon organ, thereby relieving the cramp and decreasing EMG activity.

Keywords: Exercise, fatigue, muscle cramps. Downloaded by [Australian Catholic University] at 18:51 24 September 2017

Introduction gnosis and management of this condition is, however, not well understood. Skeletal muscle cramps are one of the most common Muscle cramps can occur in a variety of medical con- clinical problems encountered by medical staff attend- ditions (Table 1). The majority of these conditions are ing to athletes at endurance events including marathons rare and, in our experience, most athletes with exercise- (Robertson, 1988) and triathlons (Hiller et al., 1987). associated muscle cramping (EAMC) do not suffer The lifetime prevalence of skeletal muscle cramping in from the congenital or acquired medical conditions marathon runners and triathletes has been reported to listed in Table 1. In this review, we will de® ne and clas- be as high as 30-50% and 67% respectively (Manjra, sify skeletal muscle cramping, and then discuss the 1991; Kantarowski et al., 1990). The aetiology, dia- pathophysiology of EAMC. Historical perspectives on the aetiology of EAMC will be reviewed, and a summary of recent research data pointing to the aetiology * Author to whom all correspondence should be addressed. of EAMC will be presented. Based on these recent

Table 1 Classi® cation of the causes of skeletal muscle ® ndings, a novel hypothesis for EAMC will be pro- cramps posed. Congenital abnorm alities 1. Metabolic abnormalities De® nitions and terminology (a) Carbohydrate metabolism (glycogen storage diseases) c Type I: glucose-6-phosphatase de® ciency It is dif® cult to de® ne muscle `cramping’ , but it has c Type II: lyposomal alpha-glucosidase de® ciency been suggested that a cramp is a `spasmodic painful c Type III: debrancher enzyme de® ciency (muscle involuntary contraction of a muscle’ (Layzer and Row- and liver) land, 1971). For the purposes of this review, the defini- c Type IV: myophosphorylase de® ciency tion can be modi® ed to exclude cramps occurring in c Type V: phosphorylase kinase de® ciency smooth muscle as well as skeletal muscle cramping that (b) Fat metabolism may occur at rest. Exercise-associated muscle cramping c Carnitine palmityl transferase de® ciency is therefore de® ned as a `painful spasmodic involuntary (c) Purine neucloetide de® ciency c Myodenalate deaminase de® ciency contraction of skeletal muscle that occurs during or 2. Other congenital abnormalities immediately after muscular exercise’ . (a) Myotonia congenita (b) Autosomal dominant cramping disease Acquired medical diseases Classi® cation of skeletal muscle cramps

1. Neuromuscular diseases Skeletal muscle cramps can occur as part of the general (a) Lower motor neuron disease symptom complex of a variety of congenital and (b) Myotonic dystrophy (c) Nerve root compression acquired abnormalities (Table 1). There are also spe- (d) Peripheral neuropathy ci® c clinical syndromes where skeletal muscle cramping 2. Endocrine diseases is the principal symptom. These syndromes are EAMC, (a) Thyroid disease occupational cramps, nocturnal calf muscle cramps (b) Diabetes mellitus and pregnancy-associated cramps. A detailed discus- 3. Fluid and electrolyte abnormalities sion on the aetiological factors, clinical presentation (a) Hypocalcaemia and management of these conditions, with the excep- (b) Hypomagnasaemia tion of EAMC, is beyond the scope of this paper. (c) Hypokalaemia Aspects of these conditions have recently been reviewed (d) Hyperkalaemia (e) Hyponatraemia (Layzer and Rowland, 1971; McGee, 1990; Riley and 4. Pharmaceutical agents Suresh, 1995). (a) Nifedipine (b) Beta-agonists: terbutaline, salbutamol (c) Ethanol Physiology of skeletal muscle relaxation (d) Clo® brate (e) Pencillamine Skeletal muscle cramping is an abnormality of skeletal (f) Nicotinic acid muscle relaxation (Layzer and Rowland, 1971). An (g) Diuretics understanding of the physiological requirements for

Downloaded by [Australian Catholic University] at 18:51 24 September 2017 (h) Phenothiazines 5. Toxins skeletal muscle relaxation should therefore form the (a) Strychnine poisoning basis of any hypothesis which could explain the aeti- (b) Lead toxicity ology of EAMC. The physiological requirements for (c) Tetanus skeletal muscle relaxation can be categorized as fol- (d) Black widow spider bite lows: 6. Other acquired medical conditions (a) Cirrhosis of the liver (b) Neoplastic disease Adenosine tri-phosphate (c) Diarrhoea (d) Sarcoidosis Adenosine tri-phosphate (ATP) is required for two pro- cesses that are essential for skeletal muscle relaxation. Speci® c acquired skeletal m uscle cramp syndromes First, ATP is required for the detachment of the myosin 1. Exercise-associated muscle cramps (EAMC) head from the actin molecule and, secondly, for the 2. Occupational cramps pumping of Ca2+ from the cytoplasm into the longitu- 3. Nocturnal calf muscle cramps dinal portion of the sarcoplasmic reticulum (Ganong, 4. Pregnancy-associated cramps 1993). Adenosine tri-phosphate depletion has been Aetiology of skeletal muscle `cramps’ during exercise 279

postulated as the mechanism for persistent skeletal Normal motor neuron activity muscle contraction in the following conditions (Layzer Persistent spontaneous motor neuron depolarization and Rowland, 1971): rigor mortis, experimental use of will result in a sustained muscle contraction. This ATP blockers (iodoacetate, dinitro¯ uorobenzene), mechanism for abnormal sustained muscle contraction myophosphorylase de® ciency, phosphofructokinase is observed in the rare hereditary syndrome of hyper- de® ciency (Layzer et al., 1967), carnitine palmityl excitable motor neuron (also known as myokymia, neu- transferase de® ciency (Bank et al., 1975) and myoade- romyotonia, pseudomyotonia, continuous muscle ® bre nylate deaminase de® ciency (Ashwal and Peckham, activity, armadillo syndrome) (Layzer and Rowland, 1985; Fishbein, 1985). Intracellular ATP depletion will 1971). Disturbances of serum electrolyte concentra- result in a persistent state of skeletal muscle contraction tions may also result in abnormal skeletal muscle con- that is electrically silent on electromyographic (EMG) traction by altering motor nerve function. testing. This condition is known as rigor.

Normal spinal re¯ ex activity Normal transport of free calcium ions from the sarcoplasm to the sarcoplasmic reticulum Normal control of the alpha motor neuron at the spinal level is essential for muscle relaxation to occur. Excita- Decreased sarcoplasmic calcium ion concentrations tory input from the motor cortex, the extrapyramidal prevent actin-myosin attachment. Decreased sarco- system and the muscle spindle must be decreased plasmic calcium ion concentrations are maintained by before skeletal muscle relaxation can occur (Ganong, an ATP-dependent calcium pump situated in the walls 1993). Decreased gamma efferent input to the muscle of the longitudinal sarcoplasmic reticulum (Pette and spindle will reduce the sensitivity of the muscle spindle Urbova, 1985). Decreased calcium transport into the and this will result in decreased Ia afferent input to the sarcoplasmic reticulum will therefore result in a persist- alpha motor neuron cell body. Activation of the Golgi ent contractile state of the skeletal muscle. Abnormal- tendon organ by stretching the tendon will increase Ib ities of calcium transport into the sarcoplasmic afferent activity. This will inhibit alpha motor neuron reticulum can be induced experimentally by exposing activity via an interneuron. Spinal re¯ ex and supra- mammalian muscle to caffeine or ryanodine (Layzer spinal input to the alpha motor neuron, and control of and Rowland, 1971). This mechanism is also postu- alpha motor neuron activity, are represented in Figs 1 lated for the delayed muscle relaxation observed in and 2 respectively. hypothyroid rats. Abnormalities of the Ca2+ -ATPase enzyme have recently been described in humans (Tay- lor et al., 1988). Aetiology of exercise-associated muscle cramping Normal muscle resting membrane potential Historical background Persistent depolarization of the muscle membrane will The interest in skeletal muscle cramping associated cause sustained muscle contraction. This mechanism with physical exercise was ® rst stimulated at the turn of has been proposed for the sustained muscle contraction in patients with myotonia (Layzer and Rowland, 1971) and in medical conditions associated with disorders of Downloaded by [Australian Catholic University] at 18:51 24 September 2017 serum electrolyte concentrations, including hyponatraemia, hyperkalaemia and hypocalcaemia.

Normal motor end plate function In abnormalities where there is a reduced rate of degra- dation of the chemical neurotransmitter acetylcholine, or where there is a persistent stimulation of the acetylcholine receptor through pharmacological means, a failure of normal muscle relaxation can be observed (Layzer and Rowland, 1971). Pharmacological agents that stimulate the acetylcholine receptor (metacholine, carbachol, nicotine) or that inhibit the enzyme acetyl- cholinesterase (neostigmine, physostigmine) result in Figure 1 Diagrammatic representation of spinal and supra- persistent muscle contraction. spinal input to the alpha motor neuron. 280 Schwellnus et al.

Talbot, 1935). These abnormalities include hyperkalaemia, hypomagnesaemia and hypocalcaemia. These reports are anecdotal, and no explanation of the mechanism whereby abnormalities of serum electrolyte concentrations could result in skeletal muscle cramping was offered. The association between serum electrolyte abnormalities and skeletal muscle cramping at rest has also been documented. Experimentally induced hyponatraemia, if accompanied by sodium loss, has been associated with generalized skeletal muscle cramping (McCance, 1936a, b). In contrast, hyponatraemic Figure 2 Diagrammatic representation of spinal and supra- states associated with a normal or increased total body spinal control of alpha motor neuron activity. sodium, such as in the syndrome of inappropriate ADH secretion (Bartter and Schwartz, 1967; De Troyer and Dermanet, 1976), water intoxication (Bartholomew the century by reports of muscle cramping occurring and Scholz, 1956), congestive cardiac failure or urae- while performing physical work in hot, humid environ- mia (Arieff et al., 1976), are usually not accompanied ments, including steamships and mines (Edsall, 1908; by skeletal muscle cramping. Chronic disorders of Talbot, 1935). In these early studies, the proposed sodium and chloride depletion such as in Addison’s pathophysiology for EAMC was a systemic disturbance disease are also not commonly associated with skeletal of ¯ uid and electrolyte balance. These early observa- muscle cramping (McCance, 1936b). The direct tions have led to the `serum electrolyte’ and `dehydra- extrapolation of ® ndings in studies examining the rela- tion’ theories for the aetiology of EAMC. These tionship between serum electrolyte abnormalities theories are still commonly accepted and will be dis- observed in systemic diseases and skeletal muscle cussed below. In the early 1950s, the ® rst case of myo- cramping in the resting state may not be applicable to phosphorylase de® ciency was described (McArdle, EAMC. Furthermore, it is well known that EAMC 1951). Numerous other metabolic abnormalities of occurs only in muscle groups that were involved in muscle cell substrate metabolism were subsequently repetitive contraction, whereas systemic abnormalities described (Tarui et al., 1965; Layzer et al., 1967; Bank associated with altered serum electrolyte concentra- et al., 1975; Fishbein, 1985), giving rise to the `meta- tions cause generalized skeletal muscle cramping. bolic abnormality’ theory for the aetiology of EAMC. More recently, two prospective clinical trials were Finally, case reports of skeletal muscle cramping during conducted among marathon runners to examine the exercise in extreme environmental conditions of heat relationship between serum electrolyte abnormalities and cold have given rise to the `environmental’ theory and EAMC. In the ® rst study, serum electrolytes for the aetiology of EAMC. A critical analysis of cur- (sodium, potassium, calcium, phosphate) were not dif- rent scienti® c evidence to support these theories of the ferent between control runners (n = 67) and those with aetiology of EAMC is warranted. EAMC (n = 15) both before and immediately after the

Downloaded by [Australian Catholic University] at 18:51 24 September 2017 race (Maughan, 1986). This ® nding suggests that Serum electrolyte theory EAMC is not due to gross disturbances of serum elec- Abnormalities of serum electrolyte concentrations in trolyte abnormalities. patients with EAMC were ® rst reported in the early In a more recent study, Nicol (1996) documented no part of the twentieth century as case series (Edsall, differences in serum electrolyte concentrations 1908; Oswald, 1925). Patients exposed to physical (sodium, potassium, magnesium, calcium) pre-race, exercise in hot, humid conditions developed hypo- immediate post-race and post-recovery from EAMC natraemia and hypochloraemia. The intake of alcohol (60 min after the race) between runners with EAM C before physical exercise was reported to aggravate the (n = 21) and control runners (n = 22). In this study, condition (Derrick, 1934). Treatment by oral sodium there was also a complete dissociation between the chloride administration was reported to decrease the post-race recovery from EAMC and changes in serum symptoms (Oswald, 1925). Other serum electrolyte electrolyte concentrations. abnormalities have subsequently been described in The ® ndings of these two studies do not support the relationship to skeletal muscle cramping (Brockbank, hypothesis that EAMC is associated with abnormalities 1929; Talbott and Michelson, 1933; Derrick, 1934; in serum electrolyte concentrations. In summary, there Aetiology of skeletal muscle `cramps’ during exercise 281

is little support for the theory that abnormalities in Metabolic abnormality theory serum electrolyte concentrations are associated with Various inherited metabolic abnormalities are associ- EAMC. ated with skeletal muscle cramping during exercise. These include abnormalities of carbohydrate metab- Dehydration theory olism (McArdle, 1951; Tarui et al., 1965; Layzer et al., 1967; Brownell et al., 1969; Viskoper et al., 1975; Dehydration is a common theory for the cause of Brumback, 1980; Kuwabara et al., 1986; Hagberg et EAMC. The earliest reports linking dehydration and al., 1990), lipid metabolism (Bank et al., 1975; Di EAMC in mine workers, stokers, cane-cutters and fire- Donato et al., 1981) and purine nucleotide metabolism men were published in the early part of the twentieth (Kelemen et al., 1982) (Table 1). A detailed discussion century (Talbot, 1935). These studies were case series, of the pathophysiology and clinical features of each of and no direct measure of hydration status was docu- these conditions is beyond the scope of this review. mented. As the management of these patients included However, it is important to note that there are signi® - administration of both ¯ uid and electrolytes simultane- cant differences between the clinical features of these ously, it is therefore not possible to link dehydration inherited metabolic abnormalities and EAM C (Table directly to EAMC. 2). There is little support for the hypothesis that the Only recently, scientists documented the relationship most common form of EAMC is caused by inherited between hydration status and EAMC in prospective metabolic abnormalities of skeletal muscle metab- clinical trials. In the ® rst study, no relationship between olism. changes in body mass, blood volume and plasma volume in marathon runners with EAM C (n = 15) and Environmental theory control runners (n = 67) were noted (Maughan, 1986). These ® ndings were con® rmed by a recent study by The environmental theory for the aetiology of EAM C Nicol (1996) documenting percentage changes in body has its roots in the original description of the condition mass, plasma volume and blood volume in ultra- and the term `heat cramps’ by Talbot (1935). Since then, it has become apparent that physical exercise per- distance runners with EAM C (n = 22) and control run- formed in a hot, humid environment can be associated ners (n = 21) (Fig. 3). Runners in these two groups with the development of EAMC. However, the devel- were matched for age, sex, body mass and ® nishing opment of EAMC is not directly related to an increased times. The ® ndings of these two studies do not support core temperature (Maughan, 1986). Further evidence the hypothesis of a direct relationship between dehy- to support the lack of a direct association between heat dration and EAMC. and EAMC is that heat stroke is not characterized by EAMC. Furthermore, passive heating alone (at rest) does not result in skeletal muscle cramping and cooling does not relieve EAMC - indeed, it may even aggravate it. It is therefore likely that exercise in the heat may result in secondary physiological changes which can cause EAMC, but heat alone is not a direct cause of EAMC. Exposure to cold environments has also been Downloaded by [Australian Catholic University] at 18:51 24 September 2017 associated with EAMC in swimmers and runners (Jones et al., 1985).

A novel hypothesis for the aetiology of EAMC

It is clear from the preceding discussion that there is a lack of scienti® c support for current theories which attempt to explain the aetiology of EAMC. A critical analysis of (1) factors associated with EAMC that have Figure 3 The percentage change in pre- versus post-race body mass, blood volume and plasma volume in runners suf- been identi® ed from recent epidemiological studies, (2) fering from EAMC (n = 22) and control runners (n = 21). observations from animal experimentation on spinal Values are mean ± S .D. No signi® cant differences were re¯ ex activity during muscle fatigue, and (3) recent observed between the two groups. electromyographic data obtained during EAMC from 282 Schwellnus et al.

Table 2 Differences between EAMC and inherited metabolic abnormalities causing skeletal muscle cramping

Exercise-associated muscle cramping Inherited metabolic abnormalities

1. Lifetime prevalence reported as 30-67% 1. Rare: only a few case series reported 2. Intermittent and variable severity during exercise 2. Recurrent and usually severe during exercise 3. Usually no myoglobinuria 3. Commonly associated with myoglobinuria 4. Usually no myalgia or rhabdomyolsis 4. Associated with myalgia and rhabdomyolsis 5. Electrical activity during cramping 5. Can be electrically silent (rigor) 6. Weak familial tendency 6. Strong familial tendency

our laboratory, have led to the development of a novel The consequences of muscle fatigue at the spinal level hypothesis for the aetiology of EAM C. would be to increase alpha motor activity. The exact mechanism by which fatigue alters afferent activity in the muscle spindle and Golgi tendon organ is not Factors associated with EAMC known. It has been documented that muscle fatigue is In a recent epidemiological study of over 1300 mara- associated with prolonged relaxation time in skeletal thon runners, certain risk factors for EAMC were iden- muscle (Edwards et al., 1975; Bigland-Ritchie et al., ti® ed (Manjra, 1991). The risk factors for EAMC 1983). included older age (years), longer history of running In addition, it is well documented that the muscles (running years), higher body mass index, shorter daily most prone to cramping are those that span across two stretching time, irregular stretching habits and a posi- joints (Manjra, 1991; Nicol, 1996). These are also the tive family history of cramping. In addition, runners muscles that are often contracted in a shortened posi- identi® ed speci® c conditions which were associated tion during exercise. Contraction in the shortened with EAMC. These conditions were high-intensity run- position would result in decreased tension in the ten- ning (racing), long duration of running (most cramps dons of the muscles during contraction. Golgi tendon occur after 30 km in a standard marathon), subjective activity in this position would therefore be decreased. muscle fatigue, hill running and poor performance in The best example would be a swimmer developing a the race. The two most important observations from cramp in the calf muscle. During swimming, the ankle these data are that EAMC is associated with running is plantar¯ exed maximally while the calf muscle con- conditions which can lead to premature muscle fatigue, and that poor stretching habits appear to increase the risk for EAMC.

Observations from animal experimentation on spinal re¯ ex activity during muscle fatigue Spinal re¯ ex activity has been studied under control conditions and after the induction of muscle fatigue. In Downloaded by [Australian Catholic University] at 18:51 24 September 2017 a series of experiments, Type Ia and II afferent activity from the muscle spindle (Nelson and Hutton, 1985) and Type Ib afferent activity from the Golgi tendon organ (Hutton and Nelson, 1986) have been studied in response to a ramp stretch protocol both under normal conditions and after muscle fatigue was induced. In these studies, fatigue to 50-60% of maximum tetanic tension was induced and afferent activity in the Type Ia, Ib and II ® bres in response to the ramp stretch protocol was documented. The results from the Type Ia (muscle Figure 4 The Type Ia afferent ® ring rate from the muscle spindle) and the Type II (Golgi tendon organ) afferent spindle in response to a ramp stretch protocol in the control response are shown in Figs 4 and 5, respectively. These muscle and the fatigued muscle. A = onset of the dynamic data show that in response to muscle fatigue, the mus- stretch, B = sustained tension, C = release of tension. cle spindle afferent ® ring rate increases, while the Golgi Adapted from Nelson and Hutton (1985). j , Control; 1 , tendon organ afferent ® ring rate decreases dramatically. fatigue. Aetiology of skeletal muscle `cramps’ during exercise 283

Electromyographic data during EAMC Fine-needle electromyographic activity was ® rst recorded during spontaneous and induced muscle cramping in the 1950s (Norris et al., 1957). In that study, it was demonstrated that (1) EMG activity can be recorded during spontaneous skeletal muscle cramping, (2) the action potentials were similar to those recorded during normal motor activity (different from those recorded in denervated muscle), (3) EMG activity was similar in induced and spontaneous cramping, (4) total EMG activity appeared to be related to the degree of pain, and (5) contraction of the antagonist muscle on the same side (ipsilateral) decreased pain and EMG activity. Electromyographic activity has also been recorded by other authors during skeletal muscle cramping at rest (Von Reis, 1954; Helin, 1985) and has shown sim- Figure 5 The Type Ib afferent ® ring rate from the Golgi ilar features. tendon organ in response to a ramp stretch protocol in the It was only recently that surface EMG activity was control muscle and the fatigued muscle. A = onset of the recorded in runners presenting to the medical facility dynamic stretch, B = sustained tension, C = release of ten- with severe EAM C following an ultra-marathon run- j sion. Adapted from Nelson and Hutton (1986). , Control; ning event (Nicol, 1996). In this study, baseline surface 1 , fatigue. EMG activity immediately after the race and 60 min later was recorded in a group of runners with EAMC (n = 9) and control runners (n = 14). The changes in tracts. The tension in the Achilles tendon would be baseline surface EMG activity (immediately following decreased compared to the ankle in full dorsi¯ exion. vs 60 min post-exercise) in runners with EAM C and Golgi tendon activity would therefore be decreased in controls is depicted in Fig. 7. Baseline EMG activity plantar¯ exion compared with dorsi¯ exion. This would decreased signi® cantly in the EAM C group compared result in less inhibition of the alpha motor neurons of with the control group. The change in activity corre- the gastrocnemius muscle. The treatment of acute mus- lated well with recovery from EAMC. cle cramps is passive stretching. This results in almost In four runners, EMG activity was recorded during immediate relief of the cramp with subsequent reduc- an acute muscle cramp, and in response to passive tion in EMG activity (Fig. 6). This phenomenon would be compatible with the hypothesis that abnormal spinal re¯ ex activity appears to be an important aetiological factor in EAMC. Downloaded by [Australian Catholic University] at 18:51 24 September 2017

Figure 7 The percentage change in baseline electromyographic activity (60 min post-race vs immediately post-race) Figure 6 Electromyographic activity in a runner with acute in runners suffering from EAMC (n = 9) compared with exercise-associated muscle cramp. A = onset of the cramp, control runners (n = 4). *Signi® cant differences (P , 0.05) B = onset of passive stretching. between EAMC and control runners. 284 Schwellnus et al.

stretching. A typical EMG pattern in a runner during EAMC. A novel hypothesis for the aetiology of EAMC acute cramp is depicted in Fig. 7. The EMG activity is presented based upon recent scienti® c ® ndings. It is decreased dramatically within 15-20 s after the onset of postulated that EAMC is caused by muscle fatigue the passive stretch (Fig. 7). These EMG data indicate which alters alpha motor neuron control at the spinal that runners with EAM C show increased baseline level through abnormal re¯ ex activity. The precise EMG activity, which suggests that there is persistent mechanism involved in the altered re¯ ex activity is not alpha motor neuron activity. Furthermore, a decrease clear and warrants further investigation. in baseline EMG activity appears to be the best pre- dictor of clinical recovery and, ® nally, passive stretching results in a dramatic decrease in EMG activity References during an acute cramp episode. It therefore appears that EAMC is a result of an Ashwal, S. and Peckham, N. (1985). Myoadenylate deami- abnormality of sustained alpha motor neuron activity, nase de® ciency in children. Pediatric Neurology, 1, which is due to an abnormality of alpha motor neuron 185-191. control at the spinal level (Fig. 8). Muscle fatigue Arieff, A.I., Llach F. and Massry, S.G. (1976). Neurological appears to be the central factor in that it causes the lack manifestations and morbidity of hyponatraemia: Correla- of control through an excitatory effect on the muscle tion with brain and water electrolytes. Medicine, 55, spindle afferent activity (Type Ia and II) and an inhibi- 121-129. tory effect on the Type Ib Golgi tendon organ afferent Bank, W.J., DiMauro, S., Bonilla, E., Capuzzi, D.M. and Rowland, L.P. (1975). A disorder of muscle lipid metabo- activity. An additional factor which may decrease lism and myoglobinuria: Absence of carnitine palmityl inhibition of motor neuron activity by inhibiting affer- transferase. New England Journal of Medicine, 292, ent activity in the Type Ib afferents from the Golgi 443-449. tendon organ is a contraction of the muscle in its short- Bartholomew, L.G. and Scholz, D.A. (1956). Reversible est position (inner range), which may be the factor pre- postoperative neurological symptoms: Report of ® ve cases cipitating the cramp (Fig. 8). secondary to water intoxication and sodium depletion. Journal of the American Medical Association, 162, 22-26. Bartter, F.C. and Schwartz, W.B. (1967). The syndrome of Overview inappropriate secretion of antidiuretic hormone. American Journal of Medicine, 42, 790-801. In this review, we present theories on the aetiology of Bigland-Ritchie, B., Johannson, R., Lippold, O.C. and exercise-associated muscle cramps. A review of the evi- Woods, J.J. (1983). Contractile speed and EMG changes dence suggests strongly that metabolic abnormalities of during fatigue of sustained maximal voluntary contrac- substrate metabolism, alterations in serum electrolyte tions. Journal of Neurophysiology, 50, 313-325. concentrations, dehydration and extreme environmen- Brockbank, E.M. (1929). Miner’s cramp. B ritish Medical tal conditions cannot adequately explain the causes of Jour nal, 12 January, pp. 65-66. Brownell, B., Hughes, J.T., Goldby, F.S. and Woods, H.F. (1969). McArdle’s myopathy: A report of a case with observations on the muscle ultrastructure. Journal of Neu- rological Sciences, 9, 515-526. Brumback, R.A. (1980). Iodoacetate inhibition of glyceralde-

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