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OESO©2015
 
Volume: The Esophageal Mucosa
Chapter: Endoscopy
 

The "MUSE" system

D. Armstrong (Hamilton)

Ph. Monnier, M. Nicolet, A.L. Blum, M. Savary (Lausanne)

The reflux of gastric contents into the esophagus can produce mucosal lesions ranging from esophagitis, which may be evident only on histological examination of biopsies, through erosive esophagitis, ulceration and stricture formation to the development of columnar metaplasia (Barrett's esophagus, endobrachyesophagus). The histological features of esophagitis are still the subject of debate as are the endoscopic features of "early" esophagitis [1], but there is general agreement that mucosal erosions [2,3] constitute unequivocal evidence of esophageal mucosal damage. There is also good evidence that multiple or more extensive erosions are a manifestation of more severe erosive esophagitis and that disease severity is, to a large extent, predictive of the likely response to treatment [4-7], This evidence is based on semiquantitative assessments of disease severity used to grade esophagitis in the conduct of therapeutic trials. In principle, the use of such grading systems should assist practising physicians in their efforts to tailor treatment regimens to the needs of individual patients and to predict the likelihood that treatment will be successful. Unfortunately, there is now a plethora of grading systems, many attributed to Savary and Miller despite the incorporation of modifications, some more subtle than others, which render them incompatible with the original proposal [3].

The original grading system proposed by Savary and Miller is based on the isolated epithelial erosion or touche peptique [2] as the fundamental lesion in grade I reflux esophagitis. Grades II and III are indicative of more extensive, more severe disease whilst grade IV esophagitis includes all complications whether or not they are accompanied by acute erosions (Table 1). Since its initial formulation, however, grade IV has been taken, by some, to indicate only columnar metaplasia with (grade IVb) or without (grade IVa) acute erosive and/or ulcerative changes. On the other hand, a recently-proposed grading system [8], based on the Savary-Miller system, includes discrete erythematous lesions, without further qualification, as a feature of grade I esophagitis. Circumscribed erythematous spots or streaks on mucosal folds are,

Table 1. .The Savary-Miller grading system for reflux esophagitis and its complications

Grade I

Single or isolated erosive lesion(s), oval or linear, but affecting only one longitudinal fold

Grade II

Multiple erosive lesions, noncircumferential, affecting more than one longitudinal fold, with or without confluence

Grade III

Circumferential erosive lesions

Grade IV

Complications: columnar epithelium, ulcer(s), stricture(s) and/or short esophagus. Alone or associated with lesions of grades I- III

indeed, very suggestive of erosions and close inspection, using an endoscope with good optics, may reveal a thin, pale film indicative of true erosions. However, erythematous areas may be difficult to distinguish from a nonspecific, age-related finding of diffuse esophageal erythema [9,10]. Such erythema may be transient or noninflammatory [11] and its presence does not predict either the healing rate in response to treatment or the relapse rate after healing [unpublished data]. It is important, therefore, to define precisely those lesions which are pathognomonic of esophagitis, those which are "soft" signs, and those which are irrelevant (Table 2).

The definition of grade IV in the original Savary-Miller classification has also made it difficult to describe accurately the progress of the esophagitis or its response to treatment, since grade IV esophagitis encompasses lesions which can develop and regress independently of each other. Thus, complete healing of active inflammatory lesions may lead to different apparent outcomes depending on the presence of complications: grade III with erosions alone and grade IV with erosions complicated by an ulcer would both become grade 0, whereas grade IV with erosions complicated by a scarred stricture would remain grade IV.

To address the problems which have arisen with current grading systems, a new classification system was developed with the preconditions that it should:

1. differentiate between premalignant lesions (columnar metaplasia), active lesions which might be expected to respond readily to therapy (erosions, ulcers and inflammatory strictures) and active lesions which would be unlikely to respond to medical therapy (scarred strictures);

2. allow the classification of multiple grades of erosive esophagitis and its sequelae as a basis for clinical practice and for clinical trials covering all aspects of esophagitis;

3. employ standard assessment criteria and a standard nomenclature in the interest of an objective and reproducible description of esophagitis severity; and

4. incorporate accepted wisdom, based on the concept of increasingly severe erosive esophagitis in Savary-Miller grades I-III (Table l)or Hetzel's grades II-IV (Table 3).

Table 2. .Endoscopic features of the esophageal mucosa which have been used as signs of esophagitis

Diagnostic criteria for esophagitis

"Hard"

"Soft"

Irrelevant

Erosions with fibrin deposit

Circumscribed erythema without white film

Generalized diffuse erythema

Junctional ulceration (Wolf or Savary)

Pseudopapilloma at the Z-line

Visible vessels near the cardia

Cobblestone appearance

Loss of normal vascular pattern

Mucosal friability

Mucosal edema

Table 3. .The Hetzel grading system for reflux esophagitis

Grade 0

No mucosal abnormalities

Grade I

No macroscopic erosions but erythema, hyperaemia or mucosal friability

Grade II

Superficial erosions, involving <10% of the mucosal surface of the last 5 cm of esophageal squamous mucosa

Grade III

Superficial erosions or ulceration involving 10-50% of the mucosal surface of the last 5 cm of esophageal squamous mucosa

Grade IV

Deep peptic ulceration anywhere in the esophagus or confluent erosion of >50% of the mucosal surface of the last 5 cm of esophageal squamous mucosa

Basis for development of the "MUSE" classification system

A detailed, standardized description of the esophagus and all lesions, required in both clinical practice and in clinical research, is best achieved using a formal report form with an accurate diagrammatic representation of all lesions [12] and, in particular, a precise indication of their extent and position in relation to the diaphragmatic hiatus rather than to the teeth (Fig. 1). This approach is particularly important for studies of the long-term progression of columnar metaplasia and dysplasia which necessitate accurate mapping and repeated biopsies. In general, however, the findings of a study must be classified so that only a small number of variables are analyzed and the predefined aims of the study can be tested without loss of statistical power. Thus, for shorter-term studies and multicenter trials with many investigators, reporting is facilitated by pictorial representation of possible lesions (Fig. 2). In general, the findings must then be classified so that only a small number of variables are analyzed statistically: this allows the predefined aims of the study to be tested without loss of statistical power.

Studies of the treatment and progression of esophagitis commonly look at four variables: columnar metaplasia (M), ulceration (U), stricture formation (S) and erosions (E). These variables are related to each other developmentally, the erosion being the primary lesion of reflux esophagitis. However, the variables are also independent in the sense that the presence of one lesion type does not indicate perforce the presence of any other lesion type. For the purposes of a clinical trial protocol, for example it would be essential that these variables be graded independently to permit assessment of the differing responses of each lesion type to therapy. The "MUSE" classification system proposed recently was designed to facilitate the identification and grading of these four independent variables [1]; the initial letter of each lesion type provides the acronym M.U.S.E., upon which to muse when describing the esophagus. In this context, the acronym is simply an aide memoire; it does not imply that the lesions of erosive esophagitis will develop in any particular chronological order.

0073F1.JPG

Figure 1. .Endoscopic report form for detailed diagrammatic description of esophageal abnormalities. Left: pictorial representation of the esophagus, the position and extent of all lesions, including hiatus hernia, may be sketched with reference to the diaphragmatic hiatus; middle: planimetric representation of the esophagus, opened about its longitudinal axis, to show the anterior (A), right (R), posterior (P) and left (L) quadrants, divided vertically into 1 cm segments to allow detailed mapping of metaplastic lesions and an exact record of all biopsy sites; right: axial view of the esophagus at three levels, the endoscopic appearance can be sketched and the level indicated by an arrow to the appropriate level on the middle panel.

At its simplest, the "MUSE" classification system can indicate the presence of a lesion-type with the suffix "+" and its absence with "-". Thus, a patient with columnar metaplasia, ulceration and erosions would be classified as "M+U+S-E+" whereas a patient with only a stricture would be "M-U-S+E-". However, in most instances, a more precise assessment of the severity or extent of a lesion is required. In this case, the classification system has been extended, by analogy to the TMN classification of malignant tumors [13], to allow all lesion types to be graded according to their degree of severity. Erosions, for example, are graded as "E0", (absent), or "E1", "E2" or "E3", corresponding to Savary-Miller grades I-III (Table 1). With four independent classes and four grades of severity (0-III), it is possible, in theory, to classify up to 256 (44) different combinations of reflux lesions without providing so many individual categories that the system becomes unwieldy. In practice, there are fewer potential combinations since Barrett's and Savary ulcers, for example, are, by definition, accompanied by columnar metaplasia.

The rationale for the definitions of the different grades in the MUSE classification is as follows:

M: Islands of metaplasia (M,) may be congenital and may not be premalignant whereas both noncircular metaplasia (M2) (fingerlike or starlike lesions extending up from the Z-line) and circumferential metaplasia (M3) are definitely premalig-

0073F2.JPG

Figure 2. .Endoscopy report form based on the "MUSE" esophagitis classification system. Metaplasia, ulceration, stricture formation and erosions (MUSE) are assessed and graded independently according to the degree of severity: 0: absent; I: mild; II: moderate; III: severe. For each lesion type, the appropriate box is ticked and, if relevant, the extent of a lesion such as columnar metaplasia may be marked with reference to the diaphragmatic hiatus. Examples of some "MUSE" classifications and the corresponding endoscopic features are: M3U0S1E3 - active peptic stricture, diameter >9 mm, situated at the upper pole of a circumferential area of columnar metaplasia; M0U0S2E3 - active junctional stricture, diameter <9 mm, situated at the level of the normal Z-line; M3U3S0E() - circumferential columnar metaplasia (endobrachyesophagus) with a Barrett's ulcer and a junctional Savary ulcer; M0U0S0E2 -multiple erosions, confluent, affecting more than one longitudinal fold but noncircumferential.

nant [14]; since M3 indicates more extensive metaplastic change, it is associated with a greater risk of malignancy [15].

U: A junctional ulcer (U1: Wolf's ulcer or Savary's ulcer) is less likely to bleed than a Barrett's ulcer (U2) whilst the combination of a junctional ulcer and a Barrett's ulcer (U3) is the rarest and most severe form of ulceration.

S: The severity of stricturing is difficult to assess, but, pragmatically, an "S1" stricture may be differentiated from a more severe "S2" stricture on the basis that the former will allow the passage of a small diameter (9.0-9.2 mm) fiberoptic endoscope. More severe stricturing, leading to a short esophagus (S3) poses considerable problems for both medical and surgical long-term management.

E: There is good evidence that the severity of erosive esophagitis is correlated with the area of mucosa affected, isolated erosions affecting only one longitudinal fold (E1) heal more readily than confluent erosions (E2) and the extensive, circumferential erosive lesions (E3) often progress to stricturing. A quantitative grading system similar to that used by Hetzel et al. [4] was also considered, but it was decided that it is easier to base a judgement on anatomical features such as mucosal folds than on the percentage of lower esophageal mucosal surface area covered by erosions or ulcers.

With the "MUSE" system, the result of an endoscopy may be written directly with a grade for each lesion type (M3U1S0E2), or it may be recorded by ticking the relevant boxes on a diagrammatic report form (Fig. 2); data recorded in this way can be entered readily into a computerized database and then retrieved for subsequent analysis.

Summary

The "MUSE" system for the endoscopic classification of reflux esophagitis provides a description of the esophagus suitable for clinical practice or research-orientated applications. It differentiates clearly between acute erosive lesions, potentially reversible complications and premalignant changes which have, to date, proved irreversible, and it eschews soft, equivocal signs of esophagitis such as erythema. It provides standardized assessment criteria and a standardized nomenclature which, in the absence of generally-accepted diagnostic criteria derived from an international consensus conference, form the basis for an accurate, objective report format consistent with the original Savary-Miller classification. Finally, an accurate description of esophageal lesions is facilitated by the use of a standardized report form which will permit an accurate, diagrammatic record of all abnormalities.

References

1. Armstrong D. Monnier Ph. Nicolet M, Blum AL. Savary M. Endoscopic assessment of oesophagitis. Gullet 1991;1:63-67.

2. Savary M, Miller G. L'oesophage. Manuel et Atlas d'Endoscopie. Solothurn: Verlag Gassmann, 1977.

3. Savary M. Les hernies hiatales non compliquées. Endoscopie. Maladie peptique oesophagienne et gastrites herniaires. Med Hyg 1968;26:789-791.

4. Hetzel DJ, Dent J, Reed WD, Narielvala FM, MacKinnon M, McCarthy JH, Mitchell B, Beveridge BR, Laurence BH, Gibson GO, Grant AK, Shearman DJC, Whitehead R, Buckle PJ. Healing and relapse of severe peptic esophagitis after treatment with omeprazole. Gastroenterology 1988:95:903-912.

5. Koelz HR, Birchler R. Bretholz A, Bron B, Capitaine Y, Delmore G, Fehr HF, Fumagalli I, Gehrig J, Gonvers JJ, Halter F. Hammer B, Kayasseh L, Kobler E, Miller G, Munst G, Pelloni S, Realini S, Schmid P. Voirol M, Blum AL. Healing and relapse of reflux esophagitis during treatment with ranitidine. Gastroenterology 1986:91:1198-1205.

6. Zeitoun P, Rampal P, Barbier P, Isal JP, Eriksson S, Carlsson R. Omeprazole (20 mg/j) compare a ranitidine (150 mg 2 fois/j) dans le traitement de 1'oesophagite par reflux. Résultats d'un essai multicentrique franco-beige, randomise en double insu. Gastroenterol Clin Biol 1989; 13:457-462.

7. Siewert JR, Ottenjann R, Heitmann H, Neiss A, Dopfer H. Therapie und Prophylaxe der Refluxösophagitis. Ergebnisse einer Multizenterstudie mit Cimetidin. Teil I. Epidemiologic und Ergebnisse der Schubtherapie. Z Gastroenterol 1986;24: 381-395.

8. Colin-Jones DG Histamine-2-receptor antagonists in gastro-oesophageal reflux Gut 1989:30:1305-1308.

9. Schule A, Brandli H, Pelloni S, Koelz HR, Pirozynski WJ, Blum AL. Endoskopische Diagnose der Oesophagitis. Wo liegt der Grenze zum Normalen? Dtsch Med Wochenschr 1977:102:606-609.

10. Leu H, Schule A, Brandli H, Pelloni S, Blum AL. Glanzverlust, Farbveränderungen und erhöhte Lädierbarkeit der Speiseröhre: altersbedingte Normvarianten. Z Gastroenterol 1978:16:417-421.

11. Monnier Ph, Savary M. Contribution of endoscopy to gastro-oesophageal reflux disease. Scand J Gastroenterol 1984; 19(suppl 106):26-45.

12. Debongnie JC, Macchi H, Mainguet P. Schema planimétrique destine a la surveillance de 1'oesophage a haul risque. Acta Endoscopica 1981;11:353-356.

13. Hermanek P, Sobin LH. TNM classification of malignant tumors, 4th edn. Berlin: Springer, 1987.

14. Monnier Ph, Fontolliet C, Savary M, Ollyo J-B. Barrett's oesophagus or columnar epithelium of the lower oesophagus. Baillière's Clin Gastroenterol 1987; 1:769-789.

15. Ronsom JM, Patel GK, Cliff SA, Womble NE, Read R. Extended and limited types of Barrett's oesophagus in the adult. Ann Thorac Surg 1982:33:19-27.


Publication date: May 1994 OESO©2015