Gut 1996; 38: 196-200

Cholesterol crystal embolisation to the alimentarytract

W Moolenaar, C B H W Lamers

AbstractThe features of cholesterol crystal emboli-sation (CCE) to the alimentary tract werestudied by retrospective analysis of theclinical and pathological data of96 patients(70 men, 26 women, mean age 73.8 (58-95)years) with this diagnosis in the Dutchnational pathology information system(Pathologisch Anatomisch LandelijkGeautomatiseerd Archief (PALGA)) from1973-92. In the 96 patients, 130 CCE siteswere found throughout the alimentarytract, mostly in the colon (42.30/o). Mostpatients had a history of atheroscleroticdisease and presented with abdominalpain, diarrhoea, or gastrointestinal bleed-ing, sometimes after surgical or radiologi-cal vascular procedures. A number weretaking oral anticoagulant treatment. Thediagnosis of CCE had been consideredbefore the histological diagnosis in only 11patients. In the remaining cases, ischaemiccolitis, tumour, and inflammatory boweldisease were suggested in the differentialdiagnosis. A premortem diagnosis ofCCEwas made in 70X8% ofthe cases. In 24 ofthe35 necropsy examinations, CCE seemed tobe directly or indirectly related to the causeof death. It is concluded that in this unse-lected, homogenous group of patients,CCE sites were most frequently found inthe colon. They generally presented withabdominal pain, diarrhoea, and gastroin-testinal blood loss. CCE often mimickedcommon gastrointestinal disease, leadingto incorrect diagnosis.(Gut 1996; 38: 196-200)

Keywords: cholesterol crystal, embolisation,alimentary tract, gastrointestinal tract.

Department ofInternal Medicine,Wilhelmina Hospital,Assen, TheNetherlandsW Moolenaar

Department ofGastroenterology andHepatology, UniversityHospital, Leiden, TheNetherlandsC B H W Lamers

Correspondence to:Dr W Moolenaar,Department of InternalMedicine, WilhelminaHospital, Postbus 30001,9400 RA Assen, TheNetherlandsAccepted for publication15 August 1995

The phenomenon of cholesterol crystalembolisation (CCE) is defined as dislodgementof separate cholesterol crystals (<200 ,um), asopposed to large atheromatous particles,(>200 gum), from atheromatous plaques, aftererosion of their intimal surfaces. These crystalscan occlude downstream arterioles. A throm-bus subsequently forms and organises aroundthis embolus.1 The blood clot is removed, butthe cholesterol crystals remain and are encasedby intimal tissue and foreign body giant cells.Recanalisation of the thrombus takes placebetween or beside the crystals, forming slit likevascular spaces. In a completely organisedlesion the artery is occluded by cholesterolcrystals, often surrounded by foreign bodygiant cells, slit like vascular spaces, and hyper-plastic intimal tissue.

This is the general picture of CCE in histo-logical sections ofbiopsy specimens, of surgicalspecimens, and of post mortem tissue, in all ofwhich both more and less advanced lesions canbe seen at the same time. The cholesterolcrystals are dissolved during the histotechnicalprocedure, leaving the pathognomonic needleshaped lacunae in the lumina of arterioles inthe histological sections (Fig 1).The disseminated or local obstruction of

small vessels gives rise to a highly variableclinical presentation due to the ensuingischaemia, infarction, possible perforation, orrepair reaction.2 The effects of CCE range inseverity from transient local ischaemia of theskin to failure of multiple organs in themultiple cholesterol emboli syndrome. Innecropsy studies the prevalence ofCCE rangesfrom 3%3 to 17-6%.4

After we had initially misdiagnosed a patientwith CCE to the large bowel and gall bladderas having Crohn's disease with maranticacalculous cholecystitis,5 we reviewed thepublished reports on the clinical presentationof gastrointestinal CCE.6 In this study weanalysed the features of the patients with CCEto the alimentary tract recorded in the Dutchnational pathology information system(PALGA) from 1973-92.

MethodsIn 1971, Dutch pathologists founded acomputerised database for pathologicalanatomical reports in The Netherlands, knownas PALGA. This network gradually expandeduntil in 1989 all 70 Dutch pathology depart-ments were participating. Thus PALGAbecame a permanent body in Dutch healthcare and a unique source of pathologicalanatomical information covering a populationof 15 million. Standardised abstracts from

m.t _ee %*shwnHistological examination of the colon wal showing thetypical needle shaped clefts in the lumen ofa submucosalarteriole, corresponding to cholesterol crystals, dissolvedduring the histotechnical procedure. (Originalmagnification X1OO).

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TABLE I Distnbution of 130 cholesterol crystalembolisation sites in the alimentary tract of 96 patients

Site No (%/.)

Oesophagus 2 (1-5)Stomach 16 (12-3)Small bowel 43 (33-0)Colon 55 (42.3)Appendix 1 (0.8)Rectum 12 (9.2)Anus 1 (0.8)Total 130 (100)

local clinical and pathological data (maximumof 360 characters) and diagnoses (maximum of1000 characters) are submitted for eachpatient at regular, daily intervals, according tothe Systmatized Nomenclature of Medicine(SNOMED) and the SystematizedNomenclature of Pathology (SNOP). Withinthis data reduction process the patient'sprivacy is protected by encryption ofvital itemslike name and date ofbirth. A scientific councilhas to approve each search before it is to beexecuted.Our search was directed to all patients filed

with a histologically proved diagnosis of CCEto the alimentary tract between January 11973and December 31 1992. Subsequently, therespective pathologists were asked by PALGAto issue (through PALGA) the unabbreviatedversions of the pathological, anatomical, andclinical reports, after erasing the names of thepatients. Privacy protection rules prevented us

from obtaining full reports on all patients,since we were not allowed to contact pathol-ogists, clinicians, or hospital departmentsdirectly to ask for further information.From the material gathered all pertinent

data regarding demography, history, provoca-tive factors, clinical presentation, CCE sites,pathological anatomy, source of tissue, extra-intestinal CCE sites, clinical differential diag-nosis, applied therapy irrespective of diagnosis,outcome, and general data source were enteredby the first author into a computerised database, from which the following results wereextracted.

ResultsWe reviewed the pathological, anatomical, andclinical data of 96 patients (70 men, 26women, mean age 73.6 years, distributedbetween 58 and 95 years), with a histologicallyproved diagnosis of CCE to a total of 130 sitesthroughout the alimentary tract (Table I). Thehistological diagnosis was made on tissue from46 resections, 35 necropsy examinations, and24 biopsies. In two patients, CCE was seen inbiopsy specimens as well as in subsequentresected tissues. In another two, CCE was seen

both in biopsy specimens and in material fromsubsequent necropsy examinations, and in fivesubjects in both resected tissues and inmaterial from necropsy examination. Themaximum interval between the first andsecond report of CCE in these nine patientswas two months. The seven patients whounderwent necropsy examination died withinone month of the first report of CCE.

Abstracts from PALGA along with fullpathological-anatomical reports were obtainedfor 40 of the 96 patients (41.7%). In 31patients (32-3%), a full clinical report wasreceived as well, but in 25 patients (26.0%)only a PALGA abstract was available. Fortyseven (49°/O) patients were reported between1990 and 1992, while none were reportedbefore 1982. In 35 patients (36.5%) no pre-vious history was specified. Of the remaining61 patients, 15 were known to have had hyper-tension, 13 had had a myocardial infarction, 1 1had signs of coronary insufficiency, ninehad intermittent claudication, eight had anaortabifurcation prosthesis, four suffered fromdiabetes mellitus, four had undergone anepisode of ischaemic colitis, and three hadearlier had blue toes.

In 59 patients (61-4%) no possibly provoca-tive factors were mentioned. Among theremaining 37, 15 were taking oral anticoagu-lants, 15 had undergone aortic angiography,12 had had surgery for rupture of an abdomi-nal aneurysm, four had received coronaryartery bypass grafts, and one had had thrombo-lytic therapy, all within eight weeks of thesymptoms of CCE, These presenting symp-toms are listed in Table II.Of 12 patients in whom differentiation of

white blood cells was reported, one showedeosinophilia of 15%.Three of the eight patients in whom total

serum cholesterol was reported had slightlyraised values (7.0, 7.3, and 8.0 mmoIIl).Complement status was determined in onepatient, and reported to be normal. All otherreported laboratory findings were non-specificrepresentatives of tissue damage and inflam-mation.The diagnoses put forward by the respective

clinicians as the most probable in advance ofthe histological confirmation of the presence ofCCE, are listed in Table III.

Specifications of the endoscopic and patho-logical appearance at the CCE site are listed inTable IV. No CCE sites outside the alimentarytract were mentioned in the reports of 63patients (65.6%). In the other 33 patients, 77sites were located, distributed over the kidneys(n=25), the spleen (n=12), the skin (n=9),

TABLE II Distribution ofpresenting clinical signs andsymptoms in 71 patients with cholesterol crystal embolism(CCE) to the alimentary tract. None were specified in theremaining 25 patients

Symptom No (%)

Abdominal pain 24 (33.8)Rectal bleeding 18 (25.4)Renal failure 15 (21-1)Diarrhoea 9 (12.7)Haematemesis/melaena 9 (12-7)Anaemia/occult blood loss 7 (9.9)Livedo reticularis 6 (8.5)Blue toe(s) 5 (7.0)Septic shock 4 (5.6)Weight loss 4 (5.6)Acalculous cholecystitis 2 (2.8)Fistula 2 (2.8)Intra-abdominal bleeding 2 (2.8)Anal tumour 1 (1-4)Dyspepsia 1 (1-4)CCE in fundo 1 (1-4)Ileus 1 (1-4)Pancreatitis 1 (1-4)

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TABLE III Diagnoses made before histological examinationin 70 patients with cholesterol crystal embolisation (CCE)to the alimentary tract. Among these, four cases ofmalignancy were histologically confirmed as well as twocases of radiation enteritis. All other diagnoses wereeventually dismissed and replaced by CCE only. None wereputforward in the remaining 26 patients

Diagnosis No (Go)

Of unknown cause 12 (17.1)CCE 11 (15-7)Ischaemic colitis 9 (12-9)Malignancy 8 (11-4)Ruptured aneurysm 4 (5.7)Mesenterical thrombosis 3 (4.3)Crohn's disease 3 (4-3)Amyloid 2 (2.9)Diverticulitis 2 (2.9)Angiodysplasia 2 (2.9)Vasculitis 2 (2.9)Radiation enteritis 2 (2.9)Peptic ulcer 2 (2.9)Amoebiasis 1 (1-4)Primary fistula 1 (1-4)Ulcerative colitis 1 (1-4)Rectal polyp 1 (1-4)Periarteritis nodosa 1 (1-4)Ischaemic enteritis 1 (1-4)Appendicitis 1 (1-4)

the liver (n=7), the pancreas (n=7), theadrenals (n= 3), the prostate (n= 3), theurinary bladder (n= 3), the gall bladder (n= 2),the muscles (n=2), the brain (n=2), the eye(n= 1), and the uterus (n= 1).No specific treatment in relation to CCE

was described in 14 patients (14.6%). Ofthe remaining 82 patients, 48 were treated sur-

gically by resection of the damaged tissue and34 received only supportive care. Of the 40patients known to have died (41-6%), 35underwent necropsy. Seven patients had diedof septic shock after bowel perforation at theCCE site, eight of multiple organ failurecaused by the multiple cholesterol emboli syn-drome, four of ongoing blood loss from theCCE sites, three of CCE induced renal failure,one of pancreatitis, and one of diffuse intesti-nal necrosis both caused by CCE. In theremaining 11, a cause of death unrelated toCCE was identified.

DiscussionCCE occurs when cholesterol crystals dis-lodged from eroded large vessel atheromas are

taken downstream and enter the microcircula-tion. This occurs either spontaneously4 5 or

after pharmacological7 8 or mechanical9 10provocation. The position of the nidus, theamount of launched crystals, and the allotmentof the bloodstream, along with its capacity forcollateral formation will determine the damagedone to a particular organ once arterioles are

blocked. A study of collected cases'1 showedthe skin and the kidneys to be the mostcommon targets of CCE, along with the spleenand the pancreas. Next came involvement ofthe alimentary tract - this was present in 9 1%of the necropsy cases in whom CCE was

found.Blood loss was the most frequently occur-

ring gastrointestinal symptom. The anatomy ofthe arterial supply, particularly that of theintra-abdominal alimentary tract by way ofthree major unpaired arteries, should make the

organ an easy target for CCE. Furthermore,taking into account that the collateral supplymay be only marginally adequate in certainareas, we would expect to find a considerableincidence of clinically relevant gastrointestinalCCE, especially in the elderly atheroscleroticpopulation, waylayed by ever more sophisti-cated pharmacological, radiological, andsurgical threats to atheroma integrity. To placethe condition in perspective we compared thefigures pertaining to CCE derived fromPALGA with those from the Dutch nationalmedical registry (Landelijke MedischeRegistratie (LMR)). The LMR records everydiagnosis for which patients were admitted toDutch hospitals according to the InternationalClassification of Diseases, 9th Revision,Clinical Modification (ICD-9-CM). Since1989 PALGA and LMR have filed everyhistology and autopsy report generated by all70 Dutch pathology laboratories, and everyadmission diagnosis to all 157 Dutch hospitals.Both are thus covering a population of 15million.From 1989-92, 1494 patients with clinically

diagnosed thromboembolic infarctions of thealimentary tract were admitted to Dutchhospitals,12 1146 of whom were recorded byPALGA to have a pathological diagnosis ofischaemic colitis. In 37 (322%) of these casesCCE was given as the most probable cause.Furthermore, over this period 2714 patientswere seen with ulcers, perforations, and/orfistulas in the alimentary tract. In 20 of thesepatients (0.74%) CCE was the given explana-tion. Of the 8495 patients who presented toDutch hospitals between 1989 and 1992 withgastrointestinal bleeding, we documented(through PALGA) 17 (0.2%) patients withgastrointestinal CCE. Sixty one of the 4685cases (1.3%) of renal failure, admitted tohospital between 1989 and 1992 could beattributed to CCE. From 1972-92 renal insuf-ficiency caused by CCE was reported in 17.8%of all cases in which CCE was present, whereasthe frequency of intestinal ischaemia due toCCE in these reports was 5.5%.

Except for ischaemic colitis no specificpathological diagnoses filed in PALGA couldbe connected with the clinical diagnoses men-tioned. From 1989-92, CCE to the alimentarytract was found at necropsy in only 17 patients.

TABLE IV Pathological anatomy at the cholesterol crystalembolisation (CCE) site as described in 100 out of all 105pathological anatomical reports on 96 patients with CCE tothe alimentary tract

Necrosis 33Ischaemic inflammation 24Ulceration 21Perforation 1 5Pseudopolyps 1 3Granuloma 12Purple spots 9Erosions 8Haemorrhagic gastritis 6Regeneration 5Stenosis 4Carcinoma 4Fibrosis 3Radiation stigmata 2Diverticulitis 1Duodenal ulcer 1Oesophagitis 1Telangiectasia 1

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With a mean of 129 850 deaths per year and amean necropsy rate of 7d1%, this would pointat a frequency of gastrointestinal CCE of0-046%. With regard to the prevalence ofatherosclerosis and the target positions of bothkidney and alimentary tract, as well as the factthat CCE is often a multisystem disease, onemight expect a higher incidence of renal CCEand a relatively higher incidence of gastroin-testinal CCE. However, all that can be statedat this point is that the figures mentioned canrepresent either a low incidence or lack ofawareness of clinically relevant CCE.

Addressing the latter issue we set out toincrease our familiarity with the phenomenonby investigating the ways in which CCE to thealimentary tract manifests itself. We did thisby reviewing unselected cases as they wereuniformly filed in the national database. Thefinding of an age and sex distribution similar tothat in patients with peripheral arterioscleroticdisease as a whole13 agrees with the suggestedpathophysiology of CCE.1 The distribution ofCCE sites in the alimentary tract (Table I)more or less represents the distribution ofblood flow once it has passed the atheromatouslarge vessels, picking up the cholesterol crystalson its way. Several case reports described CCEto the stomach1417 the small intestine,16-21and the colon.6 22-28 To our knowledge therehave been no published reports of oesophagealCCE. The emboli, probably originating fromthe coeliac trunk, taken downstream by the leftgastric artery and its oesophageal branches,caused an ulcer in one patient, and a chronicrefractory oesophagitis in another. Other as yetunreported sites are the appendix and theanus, for both of which we found one example- the former in the shape of a granulomatousappendicitis, the latter leading to the formationof an anal ridge initially believed to be a malig-nant tumour.

In concordance with the pathophysiologyand with earlier reports most patients had ahistory of atherosclerotic disease. In 38.6% ofthe reports we studied, a provocative factorcould be identified, mostly oral anticoagulanttreatment and aortic angiography. The classicclinical presentation emerging from our studyis that of a patient with sudden abdominalpain, diarrhoea, gastrointestinal blood loss,renal failure, and skin abnormalities. This full-blown picture was mainly seen shortly aftervascular manipulation when massive choles-terol crystal showers must have harassed thedownstream tissues. Most patients, however,presented with isolated, often fluctuating,common gastrointestinal symptoms like a dullabdominal pain, dyspepsia, chronic anaemiadue to occult blood loss, weight loss, a palpablemass, fistula, or ileus (Table II). This is prob-ably a result of spontaneous, chronic, intermit-tent cholesterol crystal scattering, giving rise tomucosal dysfunction or damage, which may betransient.

In our study a diagnosis of CCE before thehistological examination was made in only 11patients (Table III). Another reason for this,beside a low index of suspicion or the presenceof another disease explaining the symptoms,

may be that the pathognomonic needle shapedclefts in the deeper submucosal arteries areeither easily overlooked in histological sectionsor missed in superficial biopsy specimens.22 Anearly diagnosis was greatly facilitated by thepresence of preceding or concomitant CCEmanifestations in skin or kidneys.We registered many gastro-intestinal

diseases as later dismissed differential diag-noses (Table III). Some of these were reportedearlier, like ischaemic colitis due to othercauses,29 malignancy,27 Crohn's disease,5angiodysplasia,15 vasculitis,30 periarteritisnodosa,31 and rectal polyp.22 Much of this isdue to the observed stages of mucosal damageand repair as well as granuloma formation(Table IV), that may lead the clinician furtherastray when the CCE clefts go unnoticed orescape superficial sampling. The macroscopiclesions such as pseudopolyps, purple spots,erosions, stenosis, ulcers, and telangiectasiawere noted at endoscopy, or by observing theresection specimen. Endoscopic photographsof purple discolourations and geographicwhitish macules of the mucosa and of sessilepolyps, all proved to be caused by CCE, havepreviously been published.32 33

In six patients, another cause (carcinoma infour and radiation effects in two) explained thesymptoms, suggesting that CCE was a coinci-dental finding. Eosinophilia, earlier reported toaccompany CCE to the kidneys,34 was seen inone of 12 patients in whom a white blood cellcount was reported. Similarly, hypocomple-mentaemia35 was not found in the one patienttested. The raised serum cholesterol valuesfound, probably represent a common riskfactor for the development of atheroscleroticplaques commonly present in the studiedpopulation. The locations of the extraintestinalCCE sites we observed follow the same distri-bution as described in an earlier study of casescollected from published reports.' 1

Since we only searched for CCE to thealimentary tract, the cases of gall bladder, liver,and pancreas CCE we found were restricted tothose in whom these were additional findings.Clinical expressions due to these locationswere limited to two cases of acalculous chole-cystitis in two patients with gall bladder CCEand one of pancreatitis in seven patients withCCE to the pancreas. The last finding suggeststhat CCE to the liver and the pancreas can beasymptomatic.The retrospective nature of our study

precludes a reliable statistical analysis of trueincidence, treatment, and outcome figures.Answers concerning true incidence, however,will be hard to come by owing to the ethicalobjections to taking multiple biopsy specimensprospectively from high risk patients. Once thediagnosis of CCE is made the patient can bespared further diagnostic efforts and treatmentcan be adjusted. Consequent location andexclusion or excision of the emboli source,although earlier described as a seldomlyreached objective,36 was recently reported togive excellent long term relief of embolisationin a series of 62 patients.37 Excision of thedamaged tissue may give considerable, albeit

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only temporary relief, due to the oftenundulant but relentless course of the disease.The latter is illustrated by our finding ofnecropsy rapidly following biopsies and resec-tions from the same patients.

In conclusion, studying clinical and patho-logical data of an unselected homogenousgroup of patients we found that commongastrointestinal symptoms can be caused byCCE. CCE was most seen in the colon. It wasalso observed as a coincidental finding. Itsearly diagnosis by prompt and deep biopsies ofendoscopically identified lesions or skin biopsymight obviate elaborate diagnostic proceduresand advance adequate care.The authors are indebted to Mrs UAMG Casparie - van VelsenMD, advisor of the PALGA scientific council, for executing thecomputer search.

Furthermore, they gratefully acknowledge the cooperation ofclinicians and pathologists. A full list of institutions participat-ing in the study is available from the authors.

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