50 years on: the crush syndrome

E G L Bywaters

In this year ofmajor earthquakes in Iran, Romania, thePhilippines, and Peru-not forgetting a small one nearBishop's Castle in Shropshire-it is well to rememberthe events of 50 years ago when, during the Blitz andthe Battle of Britain, many hundreds of civilians wereburied beneath the debris of their own houses (fig 1).Much was learnt then and during the course of the warabout what we called "crush injury" and later the crushsyndrome"2 that is relevant in the rescue and treatmentof earthquake casualties.3 Fifty years ago bombingoccurred in built up urban areas provided with aprepared and relatively efficient hospital service andaffected few patients compared with the vast numberin the often rural and neglected zones of tectonic platecollisions, where logistics loom large in rescue work.4Knochel, for instance, estimated that 80% of thoseaffected die of head injuries and asphyxia, leavingonly 20% of immediate survivors; half of these haveuraemia.5

This paper presents a personal and very briefaccount of crush syndrome from 1940, seen in the lightof later developments, enabling us to draw conclusionshelpful today. Our first experience of this challengingtype of injury came on 16 September 1940 at theHammersmith Hospital in west London, thenthe British Postgraduate Medical School. JohnMcMichael, reader in medicine, was in charge afterProfessor Francis Fraser's appointment as supremo of

the emergency medical service. The team includedSheila Sherlock, Peter Sharpey-Schafer, Otto Edholm,Henry Bancroft, and Professor Gask: in the previousmonths of the "phoney war" they had undertaken aprogramme of work on shock and the physiologicaleffects of blood loss and replacement using themselvesas experimental subjects. This took on a nmore practicaland serious aspect after the capitulation of France(10 May 1940) and the miracle of Dunkirk. (26 May to4 June 1940).

Britain was alone and Winston Churchill's call, "Weshall fight on the beaches: we will never surrender,"was echoed throughout the country. After Hitler's finaldemand for our surrender (19 July 1940) Germanattacks on airfields and docks preparatory to theinvasion of England (Operation Sea Lion) were greatlystepped up. Although London had been spared so far,a retaliatory attack on Berlin ordered by Churchill(25 August) for some erring bombs on London afew days earlier brought the full force of Goering'sLuftwaffe on London starting on 7 September. We atHammersmith in Wormwood Scrubs were far awayfrom the initial fiery holocaust in the docks and the eastend, although we could see it in the night sky, but bySunday 15 September a massive and more widespreadattack was launched, in which, as was to be usual, farmore enemy aircraft were brought down than those ofours. This and later raids resulted in saturation of thebed capacity of central hospitals and transfer of lessurgent casualties to less central hospitals.On 16 September we received several casualties

at Hammersmith-the usual lacerations, bums,fractures, and shell shock-and also two patients withno apparent external injury. ' They had been buried inthe debris of their houses for a number of hours, andwhen dug out seemed to the front line casualty doctorsto be unscathed and have a normal blood pressure. Inthe melee they received little attention for an hour orso, when they suddenly collapsed without sign ofeitherexternal or internal bleeding but with gross limbswelling and skin wheals. Haemoconcentration waspresent, as was low blood pressure; this was restored tonormal by serum and saline transfusions, but oliguriaset in. Uraemia and death occurred on the 3rd day(case 3) and 6th day (case 4).' Two similar patients wereadmitted on 4 December. They were more carefullystudied, were reported to the Medical ResearchCouncil shock committee, and the details published inMarch 1941 with 13 other cases from London.'Both died of uraemia, and more complete studies atnecropsy confirmed not only muscle necrosis butmajor, specific changes in the kidneys.6Many other casualty teams began to recognise

similar cases, always after compression under debrisfor several hours. We assisted at necropsies in severalsuch cases, occasionally having to shelter beneath thenecropsy table: the results were notified in memoranda

^to the Medical Research Council's subcommittee ontraumatic oedema, which first met in December 1940.Theories abounded and remedies too. The analogy,clinical and histological, with mismatched transfusionkidney was close. This had been characterised byBaker and Dodds in 1925 as due to haemolysis, witholiguria and acid urine leading to blood pigmentobstruction of the renal tubules.7

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Royal PostgraduateMedical School,Hammersmith Hospital,LondonE G L Bywaters, FRCP,emeritus professor

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Myoglobin was suggested as the important nephro-toxic agent,' and we soon showed this in urine as

myoglobin, metmyoglobin, or finally acid haematin,and later even in serum.' We crystallised humanmyoglobin for the first time at Hammersmith,serendipitously having left a solution in the refrigeratorovernight. The low renal threshold of myoglobincompared with haemoglobin made its detection inserum, except in the most severe cases, impossibleat that time. Later technological advances andradioimmunoassay have made nanogram amountsdetectable, even in normal controls, who have a regularcircadian rhythm.Back in 1941, when we had only the benzidine

test and the spectroscope, we were able to clinch theBaker-Dodds haemoglobin hypothesis for myoglobinby producing muscle ischaemia in rabbits witha pressure bandage applied under anaesthesia.9These leg muscles contained no myoglobin, and we

reproduced the "shock" phenomenon but not the renalconsequences. The renal consequences were finallyproduced in rabbits by injecting human myoglobinsolution-but only in acidotic animals, not in controls,whether compressed or normal. "°Thus the sequence of events began to be clarified.

Air raid victims not dying from direct trauma,suffocation, blood loss, burns, or fat embolism,rescued from burial and compressed for more than twoand a half hours (fig 2) suffered irreversible ischaemicmuscle necrosis dependent to some extent on circum-ambient temperature as cooled tissue has a longerischaemic survival time. When the victim was dug out,the returning circulation brought blood to the necroticmuscle. This absorbed sodium chloride, becameswollen, and released myoglobin, lactic acid, creatine,creatine kinase, phosphate, and potassium into thecirculation. Potassium disrupted cardiac rhythm, andcalcium was later absorbed, leading to hypocalcaemiaand sometimes local calcification. The releasedmyoglobin filtered at the glomerulus into an acidand concentrated urine, precipitated in the distalconvoluted tubules of the kidney, reduced reabsorp-tion, and led to greatly increased intrarenal pressure(and of course many other mechanisms have beeninvoked). The kidneys that we examined were almostalways overweight and oedematous (fig 3), immediatelybulging out when the capsule was incised, except inpatients who died early. The distal tubules rupturedinto the interstitial tissue and into the renal venules.'These tubulovenous aneurysms are similar to thechanges in acute hydronephrosis" and those in

sulphapyridine and sometimes uric acid crystalblockage.By July 1941 the temporary cessation of raids on

London allowed us to look back at the records of thefirst world war. None of six British war surgery bookspublished in 1918-9 nor any up to 1941 mention thissyndrome, nor did the American medical history of thefirst world war.'2 It was, however, given a considerablemention, citing 126 cases, in the official GermanHandbook on Medical Studies in the World War. 13

Originally described by Von Colmers in the Messinaearthquake of 1909, the syndrome was first reported inwar injuries by Frankenthal in 1916 and followed byseveral other German publications, subsumed byMinami in 1923, who added three original caserecords. He suggested the possibility of myoglobin as anephropathic agent. History, it is frequently said,teaches us that man does not learn from history.Although it may be true that the military machinebegins war prepared for the previous one, the medicalmachine in 1939 was not as fully prepared for even aprevious war as it might have been had it consulted itsopponent's publications.

Treatment and preventionBy 1941, on the analogy of the mismatched trans-

fusion kidney lesion, we began to advocate preventionof renal damage by copious oral administration offluids containing sodium bicarbonate before releasingburied victims. This advice was eventually issued inMarch 1943 as a Ministry of Health memorandum byFrancis Fraser. These measures were often impossibleto implement because of local circumstances ormore often by the poor instruction and knowledge ofrescuers. Some at least survived the initial few hoursafter release, and once they were in medical hands-inhospital or in first aid posts -intravenous infusion withM/6 sodium lactate with glucose saline, as advised,was sometimes achieved; often it was too late but

FIG 3-Kidney ofpatient who died ofuraemia nine days afler release;gross swelling (weight 192 g) and pigmented casts

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FIG 2-Muscle ofpatient buriedfor six hours and surviving71/2 days showing oedema andnecrotic lateral muscles ofthe leg(courtesy ofMetal BoxCompany; reproduced fromBywvaters and McMichael'")

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occasionally it was rewarded by recovery. Such a casewas MR (not previously published). The case notesreported:This woman of 44 (R61 in our recovery series) was pinneddown in her house by her legs following a bomb at 12.37 am on5 July 1944. She was given I1/2 pints of fluid before being dugout and admitted (Miss Louden FRCS at the South LondonHospital for Women) at 7.10 am. The right leg was blisteredwith pressure marks, swollen, and weak. 900 ml intravenousM/6 sodium lactate was given and repeated at 4.00 and5.40 pm. Blood pressure fell from entry level of 142/90 to100/70 by 5 pm and urine by then was dark red and showedstrong bands of oxymyoglobin and the met-compound;pH jugular venous pressure remained low. Oral citrate andbicarbonate with intravenous glucose-saline and lactate werecontinued over the next three days. Leg circumferencemeasurements were made on both legs at five points andshowed maximum swelling between the 7th and 12th day, butfluid intake was good and she maintained good urinaryvolume. Myoglobin excretion continued until the 6th day anda total of 10 g was measured, equivalent to the total lysisof 2 kg of muscle [fig 4]. Recovery was followed in detailfor 131/2 months, when blood pressure, urine, blood, andsedimentation rate had returned to normal, leaving somenumbness, wasting and loss of power. There was no residualcalcification.

This woman's life was saved by prompt and early fluidand alkali administration orally and intravenously.Such an amount of muscle necrosis untreated wouldhave led to irreversible renal failure in those daysbefore dialysis.A team was formed by the Medical Research Council

to try to implement such treatment during the Baedekerraids on provincial towns and cities. Its team leader, SirJames Walton, the eminent surgeon at The LondonHospital, and such others tharwe could muster set off,usually in the dead of night, on priority calls from theMinistry of Home Security to the scenes of disaster-Norwich, Ashford, Weston super Mare, etc, throughroads without lighting or signposts, piloted by gallantgirls from the services. When we finally arrived at thebombed town with our bottles of citrate, lactate, andglucose-saline, with our syringes and specimen jars andour hand spectroscope, ready to document and treatany buried victims, we found as often as not that thepatients were either dead or safely tucked up in bedasleep-"not to be disturbed"-as well as the doctors,

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after long and arduous hours of duty. This was not asuccessful operation. Altogether, however, during thewar we recorded a total of 95 recoveries and 98 fatalcases of crush syndrome, largely due to the effortsand cooperation of physicians and surgeons of theemergency medical service. Few were published; therewere undoubtedly very many more than we were ableto ascertain.A tragic variant of crush injury happened on the

evening of 3 March 1943 when, in an air raid, over200 people became jammed together for over two hourson the stairs of an underground bombshelter.'4 Manydied, and of the 60 who survived and were quicklyremoved to local hospitals, we recorded 12. One diedwithin 45 minutes of admission from pulmonaryand cerebral haemorrhage due to suffocation withwidespread ischaemic muscle necrosis but withouthistological renal change; one showed a blood urea of380 mg/100 ml (63-46 mmol/l) on day 14 when we sawher but recovered with considerable muscle loss;another of these patients had 1I3 kg ofdamaged muscle(calculated from her myoglobin output); and othersshowed lesser degrees of damage and little residualdisability.

Other types of anuria associated with myoglobinnephropathy came under renewed scrutiny during thisearly period of crush consciousness. One woman hadfemoral artery thrombosis related to cancer and legmuscle necrosis,' and there was a young man with"acute post-streptococcal nephritis" in whom autopsyrevealed unsuspected muscle necrosis and "crushkidney"; a later elucidated history was compatible withacute and recurrent spontaneous myoglobinuria.'6As the result of this work on crush syndrome, and

with the temporary cessation ofattacks on London, theopportunity arose in 1944 to investigate the extent towhich such mechanisms operated in civilian industrialand accidental trauma. The MRC had sent the lateRonald Grant and his "shock research" team fromGuy's to Newcastle on Tyne in 1941 to study shock inminers, dockers, and other industrial workers. Histeam included Basil Reeve, Erasmus Barlow fromUniversity College Hospital, and Ludwig Wittgensteinwho, resigning his chair of philosophy at Cambridge,had opted for a job as mortuary porter at Guy's. Theywere concerned with blood loss measurements andreplacement, blood pressure, and fat embolism-andWittgenstein cut beautiful frozen sections of lung.After two or three years they then elected to go abroadto the actual battle scene, at that time Italy; the resultsof their studies, published later by the MRC,'7emphasised blood and fluid replacement.We replaced this team in Newcastle in January 1944.

Local good will was already established. In our teamwere physicians F J Nattrass, C N Armstrong, and F JOgilvie, surgeons and pathologists, of whom the lateProfessor Bernard Shaw was the most cooperative andendearing and in whose department our team worked.Perhaps I should particularly mention Miss J K Stead,a hardworking and conscientious chemist whoseanalyses not only of blood and urine but of dissectedindividual muscles were essential to our programme.In that brief year by intensive study of 55 cases weestablished that muscle necrosis played a big part in theshock syndrome that characterised severe industrialaccidents. Replacing essential blood does not obviateadditional measures to maintain an alkaline urinaryflow and to prevent the deposition of acid haematin inthe kidney, as is well attested by more recent studies.'8One case (notable because it was well followed

clinically and biochemically and not hidden under astultifying diagnosis of"shock" or "traumatic anuria"),was a cholecystectomy patient; both she and thesurgeon were considerably obese. The house surgeons,pulling on the retractors for over two hours, produced

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POTASSIUM - ,MG./ HRPHOSPHORUS-----,MG/ HR

FIG 4-Chartfrom case notes ofcase MR: urine excretion duringrecovery of10 g myohaemoglobin(equal to 2 kg ofmuscle)

I ---------------------------------------

ultiftARY tW.KT*N AFTERISCO41W MUSCLE NECAMS

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necrosis of one rectus abdominis, a comparativelysmall weight of muscle, and from this the patient diedof uraemia a few days later. Compartmental musclenecrosis may have a similar outcome."9The most important finding of this work in New-

castle, however, was the very high incidence ofdeath and of uraemia after resuscitation in patientswith fractures of the pelvis. Many muscle fibres (ascontrasted with muscle tendons) are attached tothe pelvis, and traumatic ruptures of muscle belliesproduce considerable ischaemic muscle necrosis duemostly to damage to small blood vessels. ErasmusBarlow and I thought that such cases should be givenadequate alkaline fluid on admission, both by mouthand by vein.By early 1945 we were back in London, then under

intensive attack by Vi bombs (doodlebugs) and laterby V2s, the silent and stealthy big ones, to put intopractice the lessons we had learnt in Newcastle.During these later years we recognised also that renaldamage associated with abuse ofalcohol or barbiturateswas due not to specific kidney toxins but to musclenecrosis from the weight of the unconscious body, as itwas in carbon monoxide poisoning. Now 86 causes ofmyoglobinuria with nephropathy as a contingency arerecognised.5

In the 50 years since these wartime experiences theincidence of traumatic injuries has increased because ofmining, industrial, and automobile traffic accidents,even despite enhanced safety precautions, andearthquakes continue to contribute their regularif sporadic challenge, to which we have offeredtherapeutic guidelines. The use of simple dialysis byKolff in his general practice in Kampen during theGerman occupation ofThe Netherlands revolutionisedthe treatment of these potentially reversible renallesions.20 The Borst dietary regimen, which spares cellbreakdown and potassium release by supplyingadequate calories, and our introduction of measuresto lower potassium, such as insulin and glucose,have helped. The management of these potentiallypreventable and reversible cases of anuria after traumais now well secured by modern dialysis technology (andconsiderably better than our first struggles with theKolff machine at Hammersmith in 1946, when only

two out of 12 patients survived2). The lesson for todayis that many of these dialyses for traumatic anuriaare avoidable by adequate first aid hydration andalkalinisation as well as by an adequate dietary regimenduring recovery.

Finally, tribute should be paid to the MedicalResearch Council, its scientific workers, and theenthusiastic physicians, surgeons, pathologists, andnurses of the emergency medical service and of thearmed forces during the war years-they contributedso much to our knowledge of this subject.

1 Bywaters EGL, Beall D. Crush injuries and renal function. BM7 1941;i:427-32.

2 Bywaters EGL. Ischaemic muscle necrosis.JAMA 1944;124:1103-9.3 Richards NT, Tattersall J, McCann M, Samson A, Mathias P, Johnson A.

Dialysis for acute renal failure due to crush injuries after the Armenianearthquake. BMJ 1989;298:443-5.

4 Collins AJ. Kidney dialysis treatment for vtcttms of the Armenian earthquake.N Englj Med 1989;320:1291-2.

5 Knochel JP. Rhabdomyolysis and myoglobinuria. In: Ednoyan S, ed. 7hekidney in systemnic disease. 2nd ed. New York: Wiley, 1981:263-84.

6 Bywaters EGL, Dible JH. The renal lesion in traumatic anuria. Journal ofPathology and Bacteriology 1942;54:111-20.

7 Baker SL, Dodds EC. Obstruction of the renal tubules during the excretion ofhaernoglobin. Brj Exp Pathol 1925;6:247.

8 Bywaters EGL, Delory GE, Rimington C, Smiles J. Myohaemoglobin in theurine of air raid casualties with crushing injury. BiochemJ 1941;35:1164-8.

9 Bywaters EGL, Popjak G. Experimental crushing injury. Surg Gvnecol Obstet1942;75:612-27.

10 Bywaters EGL, Stead JK. The production of renal failure following injectionof solutions containing myohaemoglobin. QJ Exp Physiol 1944;33:53-70.

11 Bywaters EGL. Hydronephrosis: histological resemblances to late changes inthe crush syndrome kidney. Journal of Pathology and Bacteriology1945;57:394-5.

12 Coupal JF. History of the medical department of the US army. Vol 12.Washington, DC: United States Government Printing Office, 1920:407-577.

13 Bywaters EGL, McMichael J. Crush syndrome. In: Cope Z, ed. Medical historyof the second world war. Surgery. London: HMSO, 1953:673-88.

14 Bywaters EGL, Crooke AC, Morris CJOR. Limb compression in the tubeshelter disaster. Lancet 1943;ii:373-93.

15 Bywaters EGL, Stead JK. Thrombosis of the femoral arterv with myo-haemoglobinuria and low serum potassium concentration. Clin Sci1945;5: 195-204.

16 Bywaters EGL, Dible JH. Acute paralytic myohaemoglobinuria in man.Journal ofPathology and Bacteriology 1943;55:7-15.

17 Grant RT, Reeve EB. Observations on the general effects of injury in man withspecial reference to wound shock. London: HMSO, 1951. (MRC special reportservices No 277.)

18 Better OS, Stein JH. Early management of shock and prophylaxis of acuterenal failure in traumatic rhabdomyolysis. N Englj Med 1990;322:825-9.

19 Fleischman AH. Ischaemic necrosis of tibialis anticus muscle with renalinvolvement. Bulletin ofthe Hospitalf rJoint Diseases 1961;22:146.

20 Kolff WJ. First clinical experience with the artificial kidney. Ann Intern Med1965;62:608-19.

21 Bywaters EGL, Joekes AM. The artificial kidney: its clinical application in thetreatment of traumatic anuria. Proceedings of the Royal Society of Medicine1948;41:420-6.

Bell ringers' bruises and broken bones: capers and crises incampanology

A C Lamont, N J M London

All you that do intend to ringYou undertake a dangerous thing.

(Change ringers' rules, 1694;All Saints Church, Stamford)

AbstractObjective-To determine the incidence, aetiology,

and outcome of injuries due to bell ringing.Design-Retrospective review ofthe last six years'

issues of Ringing World, advertisement in RingingWorld, and a postal questionnaire sent to 20 activeringing towers.Subjects-Regular bell ringers.Results-Seventy nine injuries were identified

both from review and by advertisement in RingingWorld. The incidence of injury among 221 ringersidentified by postal questionnaire was 1-8% a year.Conclusion-Although sonerous, bell ringing can

be dangerous and occasionally even fatal. Doctorsshould be aware of the dangers to which campan-ologists expose themselves.

IntroductionChurch bell ringing in the British style is an art

peculiar to the English speaking world. It is estimatedthat there are 40 000 bell ringers in England alone andthat 3000 towers are rung regularly every Sunday.

Despite the considerable hazards associated with theactivity (even the most hardened activists hesitate tocall it a sport) little is known about the incidence orrange of injuries that occur. As previous medicalreports are limited to a single case report' and ahumorous but instructive article on coping with crisesin campanology2 our aim was to investigate theincidence, aetiology, and outcome of campanologicaL6trauma.

Departments of Radiologyand Surgery, LeicesterRoyal Infirmary, LeicesterLEI 5WWA C Lamont, FRCR,consultant paediatricradiologistN J M London, FRCS, lecturerin surgery

Correspondence to: DrLamont.

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