Supracondylar Process of The Humerus Study On 375

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Supracondylar process of the humerus: Study on 375 Caucasian subjects in


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Article  in  Clinical Anatomy · March 2008


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Clinical Anatomy 20:267–272 (2007)

ORIGINAL COMMUNICATION

Correlation Between the Four Types


of Acromion and the Existence
of Enthesophytes: A Study on 423 Dried
Scapulas and Review of the Literature
K. NATSIS,1* P. TSIKARAS,1 T. TOTLIS,1 I. GIGIS,1 P. SKANDALAKIS,2
H.J. APPELL,3 AND J. KOEBKE4
1
Department of Anatomy, Medical School, Aristotle University of Thessaloniki, Greece
2
2nd Preparatory Surgical Clinic, Medical School, Athens University, Greece
3
Institute of Physiology and Anatomy, German Sport University Cologne, Germany
4
Department of Anatomy, University of Cologne, Germany

The purpose of this study was to correlate the four types of acromial shape
with the existence of enthesophytes, which together comprise two important
parameters for subacromial impingement syndrome and rotator cuff tears. In
addition, a review of the literature was carried out. Four hundred twenty-three
dried scapulas were studied at the Department of Anatomy in the University of
Cologne, Germany. Four types of acromion were found: the three classical
ones as described by Bigliani et al. ([1986] Orthop Trans 10:216) and a fourth
one, where the middle third of the undersurface of acromion was convex
(Gagey et al. [1993] Surg Radiol Anat 15:63–70). The correlation between the
four types of acromion and the presence of enthesophytes at its anterior
undersurface was also recorded. The distribution of acromial types was as
follows: type I, flat, 51 (12.1%); type II, curved, 239 (56.5%); type III,
hooked, 122 (28.8%); and type IV, convex, 11 (2.6%). Enthesophytes were
found in 1 of type I (2%), in 19 of type II (7.9%), in 46 of type III (37.7%),
and in 0 (0%) of type IV acromions. Overall, 66 (15.6%) out of 423 scapulas
had enthesophytes. In all cases, they were localized at the site of the coracoa-
cromial ligament insertion on the acromion. Enthesophytes were significantly
(P < 0.05) more common in type III acromions and this combination is partic-
ularly associated with subacromial impingement syndrome and rotator cuff
tears. In type I and in type IV acromions, the incidence of enthesophytes is
very small and, according to other studies, with these two acromial types rota-
tor cuff tears are also rare. Clin. Anat. 20:267–272, 2007. V 2006 Wiley-Liss, Inc.
C

Key words: classification; acromioclavicular joint; rotator cuff tears; impingement


syndrome; shoulder pathology; osteology

*Correspondence to: Konstantinos Natsis, MD, PhD, Department


INTRODUCTION of Anatomy, Medical School, Aristotle University of Thessaloniki,
In various studies on acromial morphology, the two pa- P.O. Box 300, 541 24, Thessaloniki, Greece.
E-mail: natsis@med.auth.gr
rameters that are mainly studied are the shape of the acro-
mion and the existence of acromial enthesophytes (Neer, Received 19 May 2005; Revised 28 November 2005; Accepted
1972; Bigliani et al., 1986; Morrison and Bigliani, 1987; 24 January 2006
Ozaki et al., 1988; Ogata and Uhthoff, 1990; Epstein et al., Published online 8 May 2006 in Wiley InterScience (www.
1993; Gagey et al., 1993; Chun and Yoo, 1994; Farley interscience.wiley.com). DOI 10.1002/ca.20320

V
C 2006 Wiley-Liss, Inc.
268 Natsis et al.

Fig. 3. Lateral aspect of a type III, hooked, acro-


mion without enthesophyte.
Fig. 1. Lateral aspect of a type I, flat, acromion
without enthesophyte.
In 1986, Bigliani et al. classified acromial shape into
three types: type I, flat (Fig. 1); type II, curved (Fig. 2);
et al., 1994; Getz et al., 1996; Nicholson et al., 1996;
and type III, hooked (Fig. 3). In 1993, Gagey et al.
Bigliani and Levine, 1997; Chambler and Emery, 1997; Hir-
observed a fourth type of acromion, with a convex inferior
ano et al., 2002). The reason for this special interest is the
surface (Fig. 4). The most commonly used term in the
association between these features of acromial morphology
literature about enthesophytes is an ‘‘acromial spur.’’
and subacromial impingement syndrome and rotator cuff
‘‘Enthesophyte,’’ however, is a more correct anatomical
tears (RCTs), which are frequently seen in orthopedic prac-
term, coming from enthesis, the site of attachment of a lig-
tice.
ament or a muscle to a bone and -ophyte, meaning an
excrescence or outgrowth (Chambler and Emery, 1997). In
the literature and in all our specimens, as well, these bony
spurs are localized to the anterior undersurface of the acro-
mion in the area of the coracoacromial ligament insertion.
Acromial enthesophytes are thought to be the consequence
of ossification of fibers of the coracoacromial ligament

Fig. 2. Lateral aspect of a type II, curved, acromion Fig. 4. Inferior aspect of a type IV, convex, acro-
without enthesophyte. mion without enthesophyte.
Four Acromial Types and Enthesophytes 269

insertion (Getz et al., 1996) due to tensile forces (Neer,


1972; Nicholson et al., 1996; Shah et al., 2001). These
tensile forces on the ligament may result from flexion and
internal rotation at the shoulder, during which the anterior
acromion is pressed upwards by the humeral head, while
the coracoacromial ligament functions as a buffer against
the superior humeral translation. It is thus logical to infer
that the ligament bears a load (Neer, 1972; Nicholson
et al., 1996; Shah et al., 2001). The enthesophytes were
first described as etiologic factors in subacromial impinge-
ment and associated tears of the rotator cuff by Neer
(1972), who described them as ‘‘spurs and excrescences,’’
which protrude into the subacromial space.
Although many authors subsequently studied acromial
shape and enthesophytes, only one group (Getz et al., 1996)
has examined the relationship between the three types of
acromion and the occurrence of enthesophytes. No study
has ever dealt with the relationship between the four types
of acromion and enthesophytes. The purpose of this study is
to correlate the four types of acromial shape with the exis- Fig. 5. Lateral aspect of a type I, flat, acromion
tence of enthesophytes and to perform a literature review. with an enthesophyte (arrow).

MATERIALS AND METHODS


vex, with a convex middle third of the undersurface, 11
Four hundred twenty-three dried scapulas from the (2.6%) (Fig. 4).
Department of Anatomy in the University of Cologne were Enthesophytes were found in 1 (2%) of type I acromions
examined. They were from male and female cadavers of var- (Fig. 5), in 19 (7.9%) of type II acromions (Fig. 6), and in 46
ious ages and there were right and left scapulas. The bones (37.7%) of type III acromions (Fig. 7); there were no enthe-
were macerated, i.e., they were left for 3 weeks in warm sophytes in type IV acromions. Overall, enthesophytes were
water (358C) to remove soft tissues. Fat was then removed in present in 66 out of 423 scapulas (15.6%), and in all speci-
ethanol (70%) and following this, the bones were left to dry. mens they were localized in the area of the coracoacromial
We examined the shape of the acromion process of every ligament insertion on the acromion, at the anterior under-
scapula and documented the presence or absence of enthe- surface. The results are summarized in Table 1.
sophytes on the anterior undersurface. The various types of In reviewing the findings of the study, we noted the stat-
acromial shape were classified by visual inspection of the lat- istically significant (P < 0.05) high prevalence of entheso-
eral aspect of acromion process. Enthesophytes were identi- phytes in type III acromions, the low incidence of them in
fied by visual inspection of the anterior acromion. If bone for- type I acromions, and their absence in type IV acromions.
mation extended anterior, inferior, or lateral to the borders
of the acromion, an enthesophyte was considered to be present.
First, we classified the scapulas into types based on their
acromial shape. We then recorded the existence of entheso-
phytes in each type of acromion. Care was taken when
defining a hooked acromion and we heeded the warning
given by Chambler and Emery (1997). Although a hooked
acromion may co-exist with an enthesophyte, a flat or
curved acromion with a large enthesophyte should never be
described as hooked because of the enthesophyte.
Researchers must classify the acromions into types, but
ensure that this is independent of the decision on the form of
the enthesophyte. It was the same researcher that exam-
ined all scapulas.
Our findings were recorded and photographs were taken
of all specimens. We used the 95% confidence interval (P <
0.05) to determine significant differences in the prevalence
of enthesophytes among the acromial types.

RESULTS
Four types of acromion were observed: type I, flat, with-
out any curve, 51 (12.1%) (Fig. 1); type II, curved, without
any abrupt change in the angle of curvature, 239 (56.5%)
(Fig. 2); type III, hooked, with an abrupt change in the Fig. 6. Lateral aspect of a type II, curved, acromion
angle of curvature, 122 (28.8%) (Fig. 3); and type IV, con- with an enthesophyte (arrow).
270 Natsis et al.

of enthesophytes, as observed in the present study.


Another possible explanation is that the critical area for ten-
don rupture, according to Neer (1972), is centered at the
anterior third of the acromion and not at the middle or pos-
terior thirds, where the curvature of the type IV acromions
is found.
Neer (1972) was the first to suggest that enthesophytes
protrude into the subacromial space causing subacromial
impingement and RCTs. Several subsequent authors
observed a relationship between enthesophytes and rotator
cuff pathology (Bigliani et al., 1986; Chun and Yoo, 1994;
Farley et al., 1994). Others considered that enthesophytes
are not the cause but the result of RCTs (Ozaki et al.,
1988; Ogata and Uhthoff, 1990; Shah et al., 2001), con-
curring with microvascular studies that have shown dimin-
ished vascularity of the ‘‘critical zone’’ in the rotator cuff
with age (Rothman and Parke, 1965). These tears may be
primary, initiated by intrinsic degenerative tendinopathy,
and this incompetent cuff allows a proximal humeral migra-
tion with increased tension on the ligament that causes the
Fig. 7. Lateral aspect of a type III, hooked, acro- growth of enthesophytes and impingement. This mecha-
mion with an enthesophyte (arrow). nism creates a vicious cycle leading to full-thickness tears
(Ozaki et al., 1988; Ogata and Uhthoff, 1990; Shah et al.,
2001). This point remains a controversial issue in the litera-
DISCUSSION ture. At any rate, either as the cause or as the result, acro-
mial enthesophytes are an important factor for subacromial
Hooked acromions have been correlated with shoulder impingement syndrome and RCTs.
impingement syndrome and RCTs. Bigliani et al. (1986) In the literature, the percentages of acromial types vary
found 66% type III acromions among 33 cadavers with to a great extent: 5.4%–67.7% for type I, 24.2%–83% for
RCTs, although this type of acromion was present in only type II, 0%–42.4% for type III, and 1.6%–13.3% for type
38.6% of all specimens. The majority of studies have sub- IV (Bigliani et al., 1986; Morrison and Bigliani, 1987; Epstein
sequently confirmed this correlation (Morrison and Bigliani, et al., 1993; Gagey et al., 1993; Farley et al., 1994; Toivo-
1987; Epstein et al., 1993; Chun and Yoo, 1994; Farley nen et al., 1995; Vanarthos and Monu, 1995; Yazici et al.,
et al., 1994; Toivonen et al., 1995; Shah et al., 2001; Wor- 1995; Getz et al., 1996; Nicholson et al., 1996; Schippinger
land et al., 2003). The study by Hirano et al. (2002) is the et al., 1997; Wang and Shapiro, 1997; Wang et al., 2000;
only one that questions this association, as they found that Shah et al., 2001; Speer et al., 2001; Hirano et al., 2002;
the correlation between RCTs and type III acromions was Worland et al., 2003). These findings are compared in Table 2.
not statistically significant. They concluded that the rela- Differences may reflect the subjective nature of the classifica-
tionship between RCTs and type III acromions is not as tion method, the type of sample, and the method used for the
strong as it has been described in the literature, but that examination.
acromial shape has a bearing on the extent of the RCT. The various types of samples described in the literature
Concerning the relationship of the fourth (convex) acro- for the identification of acromial types were as follows:
mial type with RCTs and shoulder impingement, Gagey dried scapulas, cadaveric scapulas, and living subjects.
et al. (1993) noted that this acromial type seemed to have Dried scapulas were examined either visually (Getz et al.,
no association with RCTs. Farley et al. (1994) confirmed 1996), as in our study, or by radiographs (Nicholson et al.,
this, but considered it important in acromioplasty. Acromio- 1996). Some authors examined cadaveric scapulas visually
plasty in patients with this type of acromion should include (Yazici et al., 1995; Shah et al., 2001), while others used radi-
the mid-portion of the acromion to achieve the desired ographs (Bigliani et al., 1986; Shah et al., 2001). Living sub-
decompression of the subacromial space. Although it is logi- jects were examined either by radiographs (Morrison and
cal to expect that a convex distal undersurface might cause Bigliani, 1987; Toivonen et al., 1995; Wang and Shapiro,
narrowing of the acromiohumeral space and result in 1997; Wang et al., 2000; Speer et al., 2001; Worland et al.,
impingement, the absence of rotator cuff pathology in 2003) or magnetic resonance imaging (MRI) (Epstein et al.,
shoulders with type IV acromions may reflect the absence 1993; Gagey et al., 1993; Farley et al., 1994; Toivonen
et al., 1995; Vanarthos and Monu, 1995; Schippinger et al.,
1997; Wang et al., 2000; Hirano et al., 2002).
TABLE 1. Distribution of the Acromial Types and Another possible explanation as to why the findings of
Correlation With the Existence of Enthesophytes various authors differ is the medical condition of subjects
that were used for the determination of the acromial shape.
With Without According to the literature (Bigliani et al., 1986; Morrison
Total enthesophytes enthesophytes
and Bigliani, 1987; Ogata and Uhthoff, 1990; Epstein et al.,
Type I 51 (12.1%) 1 (2%) 50 (98%) 1993; Chun and Yoo, 1994; Farley et al., 1994; Toivonen
Type II 239 (56.5%) 19 (7.9%) 220 (92.1%) et al., 1995; Shah et al., 2001; Worland et al., 2003), RCTs
Type III 122 (28.8%) 46 (37.7%) 76 (62.3%) are associated with type III acromions; thus, the more
Type IV 11 (2.6%) 0 (0%) 11 (100%) shoulders with a RCT a study includes, the more type III
Total 423 (100%) 66 (15.6%) 357 (84.4%) acromions will be found in the study.
Four Acromial Types and Enthesophytes 271

TABLE 2. Distribution of the Acromial Types in the Literature


Classification method Type I, % Type II, % Type III, % Type IV, %
Bigliani et al. (1986) Radiographsa 18.6 42 38.6 –
Getz et al. (1996) Visual inspectionc 22.8 68.5 8.6 –
Nicholson et al. (1996) Radiographsc 32 42 26 –
Morrison et al. (1987) Radiographs 18 41 41 –
Speer et al. (2001) Radiographs 11.5 84.5 4 –
Epstein et al. (1993) MRIb 29.7 37.8 32.5 –
Gagey et al. (1993) MRI 27.5 58.8 12.1 1.6
Farley et al. (1994) MRI 47 39 11 3
Toivonen et al. (1995) Radiographs 5.4 62.5 32.1 –
MRI 14.3 62.5 23.2 –
Vanarthos et al. (1995) MRI 40 36.7 10 13.3
Yazici et al. (1995) Visual inspectiona 22.5 70 5 2.5
Schippinger et al. (1997) MRI 67.7 32.3 0 –
Wang et al. (1997) Radiographs 40.8 44.9 14.3 –
Wang et al. (2000) Radiographs 6 66 28 –
MRI 6 69 25 –
Shah et al. (2001) Visual inspection 17 83 –
and radiographsa
Hirano et al. (2002) MRI 36.3 24.2 39.6 –
Worland et al. (2003) Radiographs 7.6 50 42.4 –
Current study Visual inspectionc 12.1 56.5 28.8 2.6
a
Of cadaveric scapulas.
b
MRI, magnetic resonance imaging.
c
Of dried scapulas.

One method of classification is unanimously accepted in Despite a plethora of reports about the relationship
all articles, including this study. This is the identification of between rotator cuff symptoms and hooked acromions and
the acromial type by inspection or radiology of the lateral acromial enthesophytes, the study by Getz et al. (1996) is
aspect of the acromion. All authors who used MRI identified the only one that correlated the three types of acromial
the acromial type via sagittal oblique MRI, to also obtain an shape and the existence of enthesophytes. They examined
image of the lateral aspect of the acromion. Two authors 394 dried scapulas and found enthesophytes in 22 (24%)
used coronal MRI in addition to sagittal MRI (Gagey et al., of type I acromions, in 115 (42.6%) of type II acromions,
1993; Vanarthos and Monu, 1995). and in 20 (59%) of type III acromions, while our relative
Gagey et al. (1993) originally described the fourth percentages were 2%, 7.9%, 37.7%, respectively, and 0%
(convex) type of acromion in 3 out of 182 (1.6%) should- in type IV acromions. There are no studies in the literature
ers. Farley et al. (1994) observed this acromial type in 14 correlating the four types and enthesophytes.
out of 420 (3%) shoulders. Yazici et al. (1995) found it in 2 In conclusion, this study on acromial shape examined
out of 80 (2.5%) shoulders, while Vanarthos and Monu more bones than any other on this topic in the literature. In
(1995) found it in 4 out of 30 shoulders (13%). In the cur- addition, this is the first study that correlates the four types
rent study, the incidence of type IV acromions was 2.6%. of acromion and the presence of enthesophytes. In the lit-
Apart from the percentages of acromial types, the preva- erature, the incidence of the acromial types varies to a
lence of enthesophytes reported in the literature varies as great extent. The reason for this difference may be the sub-
well. This is due to differences in the classification method jective nature of the classification method and also the
and in the type of specimens among the various authors; but medical status of the subjects. The frequency of entheso-
it may also reflect the subjects’ medical condition or occupa- phytes varies as well for similar reasons and perhaps also
tion (Ozaki et al., 1988; Farley et al., 1994; Getz et al., the acquired character of enthesophytes. Our findings,
1996; Nicholson et al., 1996). There is also disagreement in however, are similar to those of two other extensive studies
the literature about how the acromial types develop (Yazici (Bigliani et al., 1986; Nicholson et al., 1996), suggesting
et al., 1995; Getz et al., 1996; Nicholson et al., 1996; Wang that the frequency of enthesophytes involves approximately
et al., 1997; Shah et al., 2001; Worland et al. 2003). 14.2%–15.6% of acromions. Enthesophytes are most com-
The findings of Bigliani et al. (1986) and Nicholson et al. mon in type III acromions and this combination is the one
(1996), however, are very similar to ours. Enthesophytes, that mostly relates to subacromial impingement syndrome
as determined by visual inspection of the acromion, were and RCTs. Enthesophytes are rare in type I acromions as
present in 14.5% of all specimens in the study by Nicholson are RCTs. In this study, enthesophytes were absent in type
et al. (1996) and in 14.2% in the study by Bigliani et al. IV acromions in keeping with the negligible rotator cuff pa-
(1986). Our relative percentage was 15.6%, using the thology found with this acromial type.
same method. In contrast, Farley et al. (1994), who identi-
fied the enthesophytes via MRI, reported 19.5%. Getz et al.
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