arterioesclerosis clasificacion

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Arch Pathol Lab MedVol 133, August 2009 Arteriosclerosis ClassificationFishbein & Fishbein 1309

Review Articles

Arteriosclerosis

Rethinking the Current Classification

Gregory A. Fishbein, BS; Michael C. Fishbein, MD

Context.Arteriosclerosis is the vascular disease that isthe leading cause of mortality in industrialized countries.Currently, there are 3 lesions within the broader categoryof arteriosclerosis: atherosclerosis, Monckeberg medial cal-cific sclerosis, and arteriolosclerosis.

Objective.In this review, we discuss the history of theterminology and current classification of arteriosclerosisand problems with the current classification. We also dis-

cuss recently described new arterial lesions that are not inthe current classification.

Data Sources.In spite of the prevalence and impor-tance of arteriosclerotic vascular disease, and the wide-

spread use of the current terminology, there are majorproblems with the current classification: (1) the currentclassification has an inconsistent naming convention, (2)the classification fails to use terms that accurately describethe lesions, and (3) important arterial lesions are absentfrom the classification. In addition, although the terms ar-teriosclerosis and atherosclerosis describe different lesions,these terms are often used interchangeably.

Conclusion.Consideration should be given for a newmore inclusive and accurate classification of arterioscle-rotic lesions that more accurately reflects the pathologyof these important vascular lesions.

(Arch Pathol Lab Med. 2009;133:13091316)

Arteriosclerosis is literally the hardening of an artery.Standard textbooks of pathology and numerous oth-er resources consistently list 3 lesions under the term ar-teriosclerosis: (1) atherosclerosis, (2) Monckeberg medialcalcific sclerosis, and (3) arteriolosclerosis.13 These lesionsgenerally share 3 features: (1) they result in stiffening ofarterial vessels; (2) they cause thickening of the arterialwall; and (3) in the past, they have been considered de-generative diseases. Herein we review the history of ar-teriosclerosis nomenclature, the current classification of ar-teriosclerosis, and the shortcomings of this classification.Finally, we review the subtypes of arteriosclerosis withemphasis on how future classification could more accu-rately and comprehensively categorize these lesions. Thisdiscussion includes examples of lesions that could qualifyas arteriosclerosis yet are not currently classified as such.We exclude consideration of vasculitides, malformations,vascular dysplasia, connective tissue disorders, and neo-plasms involving arterial vessels; the nomenclature ofthese lesions is already sufficiently complex and confus-ing.

HISTORY OF THE TERMINOLOGY ANDCLASSIFICATION OF ARTERIOSCLEROSIS

The name arteriosclerosis is a term of Greek origin mean-ing hardening of the arteries. Though arteriosclerosis is

Accepted for publication October 16, 2008.From the Department of Pathology and Laboratory Medicine, David

Geffen School of Medicine at UCLA, Los Angeles, California.The authors have no relevant financial interest in the products or

companies described in this article.Reprints: Michael C. Fishbein, MD, Department of Pathology and

Laboratory Medicine, Room 13-145H, UCLA Center for the Health Sci-ences, 10833 Le Conte Ave, Los Angeles, CA 90095 (e-mail:[email protected]).

a phenomenon believed to be prevalent since ancientEgypt,4 it only began to catch the attention of investigatorsin the latter half of the last millennium. In 1575, Fallopiuswrites of a degeneration of arteries into bone. Theseossified arteries were commonly noted by anatomists ofthat period. Johann Friedrich Crell, in 1740, elucidated thephenomenon by asserting that the coronary artery hard-enings were, in fact, not bony, but derived from pus.5 Fif-teen years later, von Haller was first to identify such alesion as an atheroma, a term used in Greek literatureto describe a space filled with gruellike matter.6 The firstuse of the term arteriosclerosis, however, can be attributedto Jean Frederic Martin Lobstein7 in his critical analysis ofthe composition of calcified arterial lesions.

By the 20th century, the word arteriosclerosis describeda disease state of multiple known etiologies. George John-son8 can be awarded the distinction of being first to de-scribe noncalcified, nonatheromatous stiffening of smallvessels in his review of Bright disease, published in 1868.His contemporaries, Gull and Sutton,9 introduced the termarterio-capillary fibrosis to characterize this phenome-non, which would soon thereafter be referred to as arte-riolosclerosis.

In 1903, J. G. Monckeberg published a discussion of anarterial lesion he asserted was distinct from the forms ofarteriosclerosis mentioned in the previous paragraphs. Hisname has since been associated with medial calcification,though, it is not clear whether the condition modern pa-thologists call Monckeberg calcific medial sclerosis is thesame pathology he described.10 Around the same time, Fe-lix Marchand11 believed arteriosclerosis to be an inade-quately general description of a disease that had now be-come the focus of much attention. He presented the termatherosclerosis, one he believed was more descriptive of


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1310 Arch Pathol Lab MedVol 133, August 2009 Arteriosclerosis ClassificationFishbein & Fishbein

the lesions of interest. Oskar Klotz12 was quick to pointout that, although more specific, Marchands designationwas not applicable to all arteriosclerotic lesions, like thosedescribed by Monckeberg, in which no true atheroma ispresent.

In January of 1954, the American Journal of Clinical Pa-thology published a letter to the editor, written by S. M.Rabson,3 entitled, Arteriosclerosis: Definitions. In it,Rabson alludes to an article he had recently read featuringarteriosclerosis in its title but nowhere in its text. Thisprompted Rabson to send letters to various heads of uni-versity pathology departments, inquiring as to the mean-ing of words such as arteriosclerosis and atherosclerosis.The results of his survey were definitions that lacked spec-ificity, uniformity, and consistency, a situation that we feelcontinues to this day. In his letter, a frustrated Rabsonsuggests that arteriosclerosis be a generic label used todescribe any of the arterial pathologies we have discussedpreviously. The term atherosclerosis, he asserts, can rea-sonably be defined as arteriosclerosis with atheromato-sis, and its use should be restricted to that specific con-dition. This definition, provided by Rabson, has perse-vered and remains the definition pathologists operate withtoday.

CURRENT CLASSIFICATION

It appears that Rabsons brief editorial became the foun-dation of the classification of arteriosclerosis that is usedtoday. Currently, arteriosclerosis is classified into 3 le-sions: (1) atherosclerosis, (2) Monckeberg medial calcificsclerosis, and (3) arteriolosclerosis.

Atherosclerosis is a disease of elastic and large musculararteries in which the atheroma is the characteristic lesion.The lesions of atherosclerosis enlarge the arterial intimawith variable amounts and types of lipids, connective tis-sues, inflammatory cells, and a variety of extracellularcomponents including matrix proteins and enzymes and

calcium deposits.6,13,14 As atherosclerosis is the number onekiller in industrialized countries, this lesion has been stud-ied extensively, with great progress in understanding itspathogenesis, risk factors, natural history, treatment, andprevention. There are existing subclassifications of athero-sclerosis, including one adopted by the American HeartAssociation.15 Although this classification is not withoutshortcomings,14 it has been generally accepted, so the sub-categories of atherosclerosis are not discussed in this ar-ticle.

Monckeberg medial calcific sclerosis, as its name im-plies, is a calcification process that affects the media oflarge and medium-sized arteries. It is said to be a diseaserarely seen in patients younger than 50 years. According

to our German translators, Monckebergs calcific lesionsinvolve only the tunica media of arteries, without anycompromise of the arterial lumen.16 However, Monckebergsclerosis and atherosclerosis may coexist.

Arteriolosclerosis, as its name implies, is a lesion of ar-terioles, small arterial vessels with 1 or 2 layers of smoothmuscle cells. Arteriolosclerosis affects arterioles through-out the body and is most typically associated with hyper-tension and diabetes mellitus. There are 2 undoubtedlyrelated, yet histologically distinct, subtypes of arteriolo-sclerosis: the hyperplastic type and the hyaline type.17

PROBLEMS WITH THE CURRENT CLASSIFICATION

There are 3 major problems with the current classifica-tion: (1) it has an inconsistent naming convention, (2) itfails to use terms that accurately describe the lesions, and(3) major sclerotic arterial lesions are absent from the clas-sification. Another problem is that although the terms ar-teriosclerosis and atherosclerosis describe different le-sions, these terms are used interchangeably. This inappro-priate use of these terms has been pointed out by Aschoff18

almost 100 years ago, Rabson3

more than 60 years ago,and by others more recently.6

The first problem of inconsistent naming is evident bythe fact that the first 2 types of arteriosclerosis, athero-sclerosis and Monckeberg medial sclerosis, are defined bytheir gross and histopathologic features. On the otherhand, arteriolosclerosis is defined by the size of the in-volved vessel. The term arteriolosclerosis does not de-scribe any pathologic characteristics. Clearly, a classifica-tion should be consistent. That is, the classes should havesimilar descriptors, either based on the pathology, orbased on the anatomic site of the lesion, but not one orthe other. Arteriolo is not a pathologic lesion but rathera prefix that qualifies the lesion to very small arteries.Only the terms for the subtypes of arteriolosclerosis, hy-

aline arteriosclerosis and hyperplastic arteriolosclerosis,elucidate the histopathology.

The second problem is that the current system of nam-ing does not describe these lesions accurately. Even theterm arteriosclerosis is perhaps a misnomer; many quin-tessential arteriosclerotic lesions are not in fact hardenedarteries. In recent years, researchers have paid much at-tention to so-called vulnerable atherosclerotic plaques, orthin fibrous cap atheromasplaques in which a thinsheath of fibrous tissue envelops a large lipid core.19 In-deed, these are often soft plaques yet we describe them assclerotic or hardened.

Furthermore, the term Monckeberg medial sclerosis ismost likely being used incorrectly. The lesion that is gen-

erally regarded as Monckeberg medial sclerosis, ironically,may not be the lesion that Monckeberg himself described.On review of the medical literature, we found 25 articlesor texts that described Monckeberg medial sclerosis. In10 of these publications the authors state that Monckebergsclerosis involves the internal elastic lamina (IEL); in theother 15 publications the authors stated that the IEL is freeof calcification.10 In our own experience, and formal reviewof 14 specimens with calcification of the arterial media, allcases also had calcification of the IEL.

Often there were portions of the artery with only IELcalcification.20 Thus, the weight of evidence indicates thatthe lesion inaptly regarded as medial sclerosis actuallyinvolves the IELregarded by anatomy textbooks as in-tima2123and may or may not involve the media.

The third, and perhaps the most important, problem isthat there are important arterial lesions of which everyoneis aware that are not yet part of the current classification.These include transplant arteriopathy, restenosis lesionsafter balloon angioplasty and stenting, intimal nonathero-sclerotic proliferative lesions in arterial vessels larger thanarterioles, and a variety of disorders associated with vas-cular calcification, not generally regarded as Monckebergsclerosis.

Transplant arteriopathy, generally a nonatherosclerotichyperplastic fibromuscular intimal proliferation, occurs in


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Figure 1. Terminology of arteriosclerosis.The current classification of arterioscleroticlesions organized categorically. Abbreviation:IEL, internal elastic lamina.

virtually all types of solid organ transplants. Transplantarteriopathy affects large and small muscular arteries andveins as well. Early on, there is inflammation in the vesselthat can be mild or marked which may involve 1 or moreof the 3 layers. Usually, the intima is affected more thanthe media or adventitia, but sometimes even a transmural,necrotizing arteritis may occur. Following the inflamma-tory stage is the typical intimal fibromuscular prolifera-tion. With time, the lesions become less cellular and more

fibrotic. Calcification, thrombosis, and atheroma formationcan also occur in the setting of transplant arteriopathy. Inthe heart, where this lesion is most damaging, transplantcoronary artery disease affects large and small epicardialcoronary arteries and intramyocardial arteries.

Another now common iatrogenic form of intimal hy-perplasia is that associated with restenosis after balloonangioplasty24 or after intravascular stent placement.25 Theintimal proliferation in restenosis lesions is histologicallythe same as in transplant arteriopathy and the hyperplas-tic form of arteriolosclerosis.

There are a number of other situations in which arteries,not arterioles, show lesions histologically similar to thoseseen in the hyperplastic type of arteriolosclerosis lesions.

One commonly encountered site for such lesions is thetemporal artery. In elderly patients in whom biopsy isnegative for temporal arteritis, these intimal lesions areoften observed.26 Indeed, in the American Heart Associa-tion classification of atherosclerosis, the atheroma-pronelesion is not the fatty streak but rather a region of intimalfibromuscular hyperplasia, referred to as adaptive inti-mal thickening.13 Identical lesions may be seen through-out the body as a nonspecific finding in muscular arteries.

Although the term intimal hyperplasia is often used todescribe intimal thickening with smooth muscle cells, col-lagen, and other components present, we recognize that

this phrase may not be completely accurate. Becausesmooth muscle cells in the intima may have migratedfrom the media or adventitia, or have been deposited fromcirculating progenitor cells, the process in the intima isnot simply hyperplasia. Furthermore, there are a varietyof other terms used synonymously to describe intimalthickening, such as neointima, fibromuscular hyperplasia,adaptive intimal thickening, hypertrophy, and fibroplasia,just to name some. Whether or not these are appropriatefor specific lesions, or truly synonymous, requires addi-tional study.

In addition to what Monckeberg described, there are anumber of other patterns of arterial calcification. We re-cently reported calcification limited to the IEL observedin the coronary arteries of human immunodeficiency virus(HIV)positive patients and HIV-negative elderly patientswith a variety of chronic diseases.27 These patients hadnormal renal function. In patients who do have renal dys-function, alterations in calcium metabolism may causewidespread tissue calcification that affects the arterial bed,so-called vascular tachyphylaxis.28 Renal failure can alsoresult in more extensive calcification within atheroscleroticplaques and/or extensive medial calcification that affect

arteries throughout the body. In patients with secondaryhyperparathyroidism, x-rays of the hands may reveal suchcalcification in digital arteries. In diabetic patients withsevere peripheral vascular disease, arteries in amputatedlimbs frequently show heavily calcified atheroscleroticplaques and marked medial calcification. Importantly,electron beam computed tomography of coronary arteriesin patients with chronic renal disease yields higher calci-um scores than in individuals with normal renal func-tion.29 Whether this calcification is in the atheroscleroticlesions or the arterial media has not been addressed.


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Figure 2. A and B, Atherosclerosis. A, Characteristic eccentric lesion with large lipid-rich (necrotic) core covered by a fibrous cap (F) (hematoxylin-eosin, original magnification 2). B, Oil red O stain showing lipid (L-red) within the lipid-rich core (original magnification 40). Smaller darkerred dots are lipid-laden macrophages. C, So-called Monckeberg medial calcific sclerosis. Note that although there is prominent medial calcificationthe internal elastic lamina is also involved (arrow) (hematoxylin-eosin, original magnification 40). D through F, Primary arterial calcification. D,Early lesion with interrupted linear calcification limited to the internal elastic lamina (hematoxylin-eosin, original magnification 100). E, vonKossa stain of early lesion with interrupted linear calcification limited to the internal elastic lamina (original magnification 100). F, Linear andnodular calcification of the internal elastic lamina (arrows) (hematoxylin-eosin, original magnification 20).


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Figure 3. A through D, Fibromuscular intimal thickening. A, Adaptive intimal thickening in proximal coronary artery (trichrome, originalmagnification 40). B, Transplant coronary artery disease (trichrome, original magnification 40). C, Intimal hyperplasia in temporal artery(hematoxylin-eosin, original magnification 40). D, Arteriolonephrosclerosis, hyperplastic type (hematoxylin-eosin, original magnification200).E and F, Hyalinosis (hematoxylin-eosin, original magnification 200 [E] and periodic acidSchiff, original magnification 200 [F]).

CATEGORIES OF ARTERIOSCLEROSIS

Figure 1 shows the subtypes of arteriosclerosis orga-nized into what we believe are the various categoriesbased on the major light-microscopic pathology of the le-sions. In the following we describe each subtype in greater

detail and explain, in our opinion, how each could be rep-resented in future classifications of arteriosclerosis.

Atherosclerosis

Atherosclerosis (Figure 2, A and B) is clearly the mostimportant arteriopathy. Although the suffix sclerosis is


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Figure 4. A and B, Vascular amyloidosis causing stenosis of intramyocardial arteries from a patient who died suddenly (hematoxylin-eosin, original

magnification 100 [A] and Congo red, original magnification 100 [B]). C and D, Coronary artery of a patient with oxalosis; crystal depositsare subtle by routine light microscopy but prominent under polarized light (hematoxylin-eosin, original magnifications100 [C and D]). E, Oxalatewas also present within a calcified (C) atherosclerotic plaque (hematoxylin-eosin, original magnification 40).

derived from the Greek word meaning hardening, athero-sclerotic vessels may not be harder than normal and, in-deed, may even be softer. One might even consider ath-erosclerosis an oxymoron. Although sclerosis denoteshardening, athero literally means gruellike. Atheroscle-rosis is therefore literally, and rather unintuitively, definedas arteries hardened by a thin chunky liquid. Alternate

terms for some of the lesions might include atheromatousarteriomalacia or atheromatous arteriopathy. However,historically these are referred to as sclerotic lesions, nothard lesions, as they have become semantically distinctterms. In addition, it is quite common for the definition ofa term to semantically deviate from its Greek derivation.Indeed, though hippocampus literally means sea horse,


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we accept that this historical nomenclature is not to betaken literally. Furthermore, the word sclerosis is com-monly applied in other pathologies in which hardening isnot the characteristic change, such as multiple sclerosisand hippocampal sclerosis. Therefore, it is not difficult toaccept atherosclerosis as a worthy subtype of arterioscle-rosis.

Monckeberg Medial Calcific Sclerosis

Because the term Monckeberg medial calcific sclerosis

(Figure 2, C) is probably only partially accurate and be-cause there are other forms of arterial calcification, we feelthis and other nonatherosclerotic forms of arterial calcifi-cation are better described as primary arterial calcifica-tion. We have observed primary arterial calcification in 3patterns.

Calcification limited to the IEL is a common phenome-non in temporal arteries.26 Internal elastic lamina calcifi-cation occurs infrequently in coronary arteries20 (Figure 2,D through F). We described 19 cases of coronary arteryIEL calcification; 10 patients were HIV-positive patientsand 9 HIV-negative patients had a variety of chronic ill-nesses. Sometimes, calcification encroached on adjacent in-timal or medial tissue and was associated with mild fi-

brosis. There was frequent disruption of the IEL but noinflammation. von Kossa, alizarin red S, and trichrome/elastic stains confirmed the findings. Patients with IEL cal-cification often had complex medical histories but did notsuffer from chronic renal failure or other conditionsknown to cause calcium dysregulation. The pathogenesisand clinical significance of this finding are unknown.However, this mysterious calcification could lead to arte-rial stiffening and increased pulse pressure and could bemistaken for intimal calcification on coronary imaging.IEL calcification may result from premature aging due toHIV disease and chronic illness or from metabolic disor-ders in HIV-positive patients. Because IEL calcification isnot part of any classification, IEL calcification is probablyunderreported.

Although Monckeberg medial calcific sclerosis is not en-tirely medial and probably begins in the IEL, it is not ourintention to rob Monckeberg of his namesake. Given thehistorical context, we feel Monckeberg will continue to beassociated with calcification limited to the arterial media.16

Incidentally, however, this pattern of calcification may beexceedingly rare or simply may not occur at all. We en-courage others to confirm our observations suggestingthat medial calcification is virtually always associated withcalcification of the IEL.10

The third pattern of primary arterial calcification wouldbe a combination of the first two; that is, calcification ofboth the IEL and the media. We believe this will eventu-ally prove to be the primary pattern of calcification in

which the arterial media is involved.Arteriolosclerosis

We feel the third category, arteriolosclerosis, which dis-tinguishes small artery sclerosis from large artery sclero-sis, is an unnecessary distinction. The subtype fibromus-cular intimal thickening (Figure 3, A through D) wouldinclude the hyperplastic form of arteriolosclerosis butwould similarly include fibromuscular hyperplasia in ar-teries, as seen in transplant vasculopathy, restenosis le-sions after balloon angioplasty or stenting, and nonspe-cific intimal thickening as occurs in temporal arteries with

aging. Although hyalinosis typically occurs in arterioles,similar changes can be seen in arteries. Thus, simply de-scribing these lesions as intimal hyalinosis would includesuch changes in arteries as well as arterioles (Figure 3, Eand F).30,31

Finally, there are those miscellaneous entities that sharefeatures of the lesions discussed so far in that they causethickening and stiffening of arteries. Two recent exampleswe have encountered that are not included in existing cat-egories of vascular diseases are amyloidosis, which can

involve arteries and arterioles, and vascular oxalosis (Fig-ure 4, A through E).

Vascular involvement by amyloid deposits is a well-known phenomenon. Amyloid deposits in large and smallarteries can cause ischemia and even sudden death wheneither the epicardial or intramyocardial coronary arteriesare involved.32

Oxalosis is a relatively rare metabolic abnormality thatmay be hereditary or acquired. Oxalate deposits most of-ten occur in the media of elastic and muscular arteries inpatients with chronic renal failure. However, we recentlyreported, for the first time, intimal deposition of oxalatesin atherosclerotic plaques, so-called atherosclerotic oxalo-sis.33 In a review of coronary arteries from 80 patients, we

found 4 cases in which there were prominent oxalate de-posits within the atherosclerotic plaques in coronary ar-teries. Oxalate deposits were also present in the media ofarteries, the thyroid gland, and other organs, but not thekidneys, and the patients surprisingly did not have renalfailure.

Another group of disorders that are associated with vas-cular lesions that could qualify as arteriosclerosis are sys-temic genetic disorders such as the mucopolysaccharido-ses (Hunter and Hurler syndromes) and Alagille syn-drome. These might also be included in a miscellaneouscategory along with other vascular lesions.

As mentioned, there are other categories of arterial dis-eases: vasculitides, neoplasms, malformations, angiodys-plasias, and inheritable disorders of connective tissue.

Whether or not these should be incorporated into an all-inclusive classification is beyond the scope of our editorial.

This work was supported in part by the generous endowmentprovided by the Piansky Family Trust. The authors have no po-tential conflicts of interest related to this work.

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