subacromial impingement syndrome: has evolution failed us?

Physiotherapy April 2001/vol 87/no 4

Professional articles

IntroductionSubacromial impingement syndrome(SIS) refers to the symptoms of pain anddysfunction resulting from pathology ofany of the structures in the subacromialspace. The symptoms and loss of functionassociated with SIS are most severe whenthe arm is used in elevated positions. Neer(1972, 1983) described impingement asoccurring as a result of direct mechanicalcompression on the rotator cuff tendons.Others (Uhthoff and Sarkar, 1991) havesuggested that rotator cuff overload maybe the primary etiologic mechanism.Failure of the passive glenohumeralstabilisers also appears to contribute toSIS (Jobe et al, 1989). Although numerousmechanisms have been proposed, theaetiology of impingement syndrome still remains unclear. Meyer (1931)commented that ‘no one can rightlymaintain that the shoulder is perfectlyadapted for the uses to which it is put’.

The pathogenesis of SIS may, in part,

relate to the evolutionary constraintsplaced upon the modern human shouldergirdle. The purpose of this article is toreview the evolutionary development ofthe shoulder girdle from quadrupedalismto bipedalism, and the possible evol-utionary challenge faced by modernhumans when using the shoulder girdlein elevated positions.

Origins of Bipedal Posture and theNon-weight-bearing Upper ExtremityThe evolutionary development fromquadrupedalism to bipedalism requiredsignificant changes in bone structure andmuscular function. Although thesechanges were more pronounced in thelower limbs, the forelimbs also underwentconsiderable change with the result thatthe upper extremity was freed from aweight-bearing role to one of higherfunction.

Palaeoanthropologists argue that thefossil record suggests that the hominidspecies, Australopithecus (A) afarensis, wascapable of a bipedal posture betweenthree and four million years ago (Wood,1993). One specimen found in the AfarLocality in Ethiopia, known as Lucy (AL 288-1), was certainly capable ofupright posture and locomotion, whichimplies an ability to use the forelimb formore than weight-bearing. There ishowever, considerable debate as to whyLucy stood upright. Although the conceptof direct lineage is questionable(Tattersall, 2000), the evolutionary recordsuggests that modern Homo sapien sapiensis possibly descended from A afarensisthrough a number of intermediate stages.Homo habilis may have succeeded Aafarensis, and in turn was possibly followedby Homo ergaster or Homo erectus, andapproximately 100,000 to 200,000 yearsago Homo sapien sapiens appeared (Aielloand Dean, 1990; Wood, 1992; Hunt,

Subacromial ImpingementSyndrome Has evolution failed us?

Summary Evolution has endowed the human shouldergirdle with a unique range of movement, that whencombined with elbow movement enables the hand toperform a myriad functions. Although the human shouldergirdle is capable of large ranges of movement, commonplacein many sporting and vocational pursuits, there are manyfeatures which suggest that the modern human arm is betteradapted for use in a lowered position and is less well adaptedfor use in an elevated position. The human shoulder hasevolved a relatively small suprascapular fossa, a laterallyfacing glenoid fossa and acromion, and a clavicle without alateral upward flare. The insertional angle of the upwardscapular stabilisers is similar to that of quadrupedal primatesand less like our more immediate ancestors and the greatapes. These changes may place a challenge on the shoulder,which makes it less suited to perform vocational and sportingpursuits in elevation and may be a contributing factor to thepredisposition of subacromial pathology.

Key WordsShoulder, subacromial impingement,evolution, posture.

by Jeremy LewisAnn GreenZiva YizhatDonald Pennington

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Lewis, J, Green, A,Yizhat, Z andPennington, D (2001).‘Subacromialimpingementsyndrome: Hasevolution failed us?’Physiotherapy, 87, 4,191-198.


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1994). Modern human bipedalism andupper limb function may be seen as acontinuum with anatomical adaptationsrelating to the evolutionary needs over aperiod of time.

The recession of the tropical rainforestenvironment in Africa about four millionyears ago, and its replacement by grass-land savannah, have been proposed as a significant evolutionary stimulus forattaining upright stance (Makepeace-Tanner, 1981). Bipedal gait would haveallowed A afarensis to move more easilybetween scattered feeding resources. Anupright posture and a freed upperextremity would also have provided theseearly hominids with a form of defence onthe open grassland savannah. Branchesand leaves could be thrown at potentialpredators and an upright posture mayhave discouraged predation by lions,hyenas, jackals and wild dogs bypresenting a strange and unfamiliarposture that discouraged attack (DeVoreand Washburn, 1963; Makepeace-Tanner,1981).

Many of the theories as to the evol-utionary development of modern human bipedalism and posture fromquadrupedalism support this concept.Standing upright would reduce the needfor water. Wheeler investigated the originsof human bipedalism and concluded thatthe upright posture adopted by A afarensiswould have significantly reduced thermalstress and assisted in thermoregulation(Wheeler, 1991) and would have reduceddrinking water requirements from 2.5 to1.5 litres a day (Wheeler, 1993). Othertheories to support the evolutionarysuccession to bipedalism includeincreased range for food gathering(Rodman and McHenry, 1980; Wheeler,1993; Hunt, 1994), tool use and carryingbehaviour (Hewes, 1961; Washburn,1963), enhancing tool use, by being able to use an upright trunk for lever-age in applying force (Marzke et al, 1988), demographic and reproductiveconstraints (Lovejoy, 1981), energyefficiency (especially when walking ascompared with quadrupedalism orrunning) (Rodman and McHenry, 1980;Leonard and Robertson, 1995) andcarrying (Hewes, 1961; Lovejoy, 1981).

Lovejoy (1981) argued that the origin ofbipedality was a necessary evolutionarydevelopment to free forelimbs to allowfood to be carried ‘by hand’. Lovejoy

(1981, 1988) suggested that positiveevolutionary selection, in order to de-crease infant mortality, maximise famil-iarity with a geographic core locality,reduce exposure to predators, and allowintensification of parenting behaviour,would favour a less mobile female and amore mobile male. The male would beable to range for food and carry it back tothe core locality for his mate and theiroffspring. This would only be possible ifthe forelimbs were freed from weight-bearing in order to carry food.

To a large extent the success of thegenus Homo has depended upon thedevelopment of technology such as tooluse. The evolutionary development of thenon-weight-bearing upper limb, with astable scapula acting as a base of supportfor a hand that has become capable ofadvanced manipulative skills, was criticalfor this success. The first recognisabletools appeared two million years ago andthe development of more advancedhafted tools appeared only 50,000 to100,000 years ago (Isaac and Leakey,1979). This questions the primaryevolutionary stimulus for bipedalism to be based around advanced upper limbfunction. Lovejoy (1988) argued that theearly hominids made no special use oftools or only to the extent that wascomparable to the hominoids beforethem. As tool use was not a feature ofevolutionary development for at least amillion years, it is unlikely that thedevelopment of bipedalism occurred tofree forelimbs for this purpose. As there isno evidence for using tools, this supportsthe argument that bipedal posturedeveloped for physiological and defensivepurposes on the grassland savannah.

Evolutionary Development of theShoulder Girdle Human evolution has involved aunivertebral articulation between the firstrib and first thoracic vertebra. The uni-vertebral pattern was established in thehominid lineage by the appearance of A afarensis (Ohman, 1986). Before this thehominoids displayed a bivertebral pattern,with the seventh cervical and first thoracicvertebrae. Ohman (1986) suggested anumber of possible reasons for thisevolutionary development. First, as a con-sequence of the more barrel-shapedthorax in hominids, secondly as a result ofdifferent thoracic motion while breathing


193Professional articles

in upright posture, and thirdly to allowfor functional modifications in thehominid shoulder girdle, allowing the upper limb to be freed from theconstraints of quadrupedal locomotoractivity.

Evolutionary adaptations of the scapulahave included a relative increase in itsbreadth (measured from the superior toinferior angles) while its length(measured along the base of the spine)has remained fairly static (Schultz, 1968;Roberts, 1974). This implies that theinfraspinous fossa has increased in sizecompared with the supraspinous fossa,whose size has remained fairly static.Enlargement of the infrascapular fossa is associated with an increase in the infraspinatus and teres minor musculature, allowing these muscles to be more effective in their roles asexternal rotators and depressors of thehumerus.

Orthograde posture, which is defined as walking with the body upright, isassociated with a significant enlargementof the coracoid and acromion processes,together with elongation of the clavicle(Gregory, 1928; Schultz, 1968). Althoughthe supraspinatus muscle has remainedrelatively static morphologically, theenlarged acromion has allowed for arelative increase in the size of the deltoidmuscle. Further, the large lateral proj-ection of the acromion increases themechanical advantage of the deltoid byprojecting the origin of the muscle overthe glenohumeral joint (Aiello and Dean,1990). The insertion site of the deltoidhas also migrated more distally. Duringabduction the arm acts as a third-classlever and the larger deltoid and the lowerinsertion point have improved the leverarm of the muscle (Miller, 1932; Evansand Krahl, 1945; Ashton and Oxnard,1964).

The humeral head has enlarged andbecome globular. This would haveoccurred to allow for greater shouldermobility (Larson, 1988). The humeralhead has rotated medially (medialtorsion). Torsion of the humeral head isdefined as the axis of the head of thehumerus with the mediolateral axis of theelbow (Aiello and Dean, 1990). Thisenables the humeral head to maintaincontact with the dorsally positionedscapulae and the laterally facing glenoidfossa. Torsion allows the elbow to flex and

extend in the sagittal plane and not in thecoronal (Larson, 1988). Larson (1988)argued that the lateral orientation of theglenohumeral joint and the medialtorsion of the humerus has allowed theforearm and hand to be used in front ofthe body for the purposes of manip-ulation.

Factors Suggesting the HumanShoulder Girdle Is Not Well Adapted toOverhead ActivityThe evolution of the human shouldergirdle suggests that it is not well adaptedfor overhead activity. Over the past 3.6million years arboreal locomotion(brachiation) and climbing behaviour,activities requiring prolonged andpowerful overhead elevation, have beenreplaced with manipulative skillsperformed within the visual field as themain activity of modern human forelimbs.This change in function has necessitatedvarious evolutionary adaptations. Theforelimbs have become shorter, the chestless cone shaped, together with changesin scapula, glenoid and acromial shapeand changes in shoulder girdle muscles.Many of these changes make the modernhuman shoulder girdle less able to sustainpowerful, prolonged elevation, which mayin turn contribute to the pathogenesis ofSIS when the arm used in this manner.

A afarensis had a chest as large antero-posteriorly as it was transversely but ofgreatest significance is the cone shapedthorax (Schmid, 1983) (fig 1). The cone

Fig 1: Thoracic differences between Homo sapien sapiens (man, left), a reconstruction of A afarensis and Pan troglodytes (chimpanzee, right). The cone shaped ribcage of A afarensis implies an upwardly rotated scapulaplacement on the thorax (Hunt, 1994, page 194)


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shape would imply that the scapula restedon the thorax in significantly moreupward rotation than in later hominidspecies, especially Homo sapien sapiens.The functional implication of the greaterupward rotation would be to allowactivities performed in elevation, suchas brachiating and climbing, to beaccomplished with a reduced risk ofimpinging the subacromial structureswhile performing these activities.

A afarensis, like modern apes, demon-strated forelimb and hindlimb musclemass and bone lengths in reverseproportions to modern humans. Thisreflects a shortening of the forearm andnot the humerus (Aiello and Dean, 1990)(fig 2). Like apes, the longer forelimbssuggest that A afarensis was involved inbrachiation and climbing activities as wellas quadrupedal postures, and possiblyquadrupedal locomotion. The evolut-ionary adaptation of a shorter forearm inHomo sapien sapiens has allowed for betterhand manipulation within the visual field,a task which is generally performed withthe arms in a lowered position. Bybringing the hands into a better visualfield the shorter upper limb wouldimprove the dexterity of tool making andother manipulative skills. However, toachieve this, arms designed for powerfuloverhead activities (brachiating orclimbing) that require a long reach forefficiency, would be sacrificed.

Another important feature which sugg-ests that the modern human shoulder isless well adapted for activities in elevationis the angle of the glenoid fossa. Sternand Susman (1983) reported that theglenoid fossa of A afarensis was directedfar more cranially than is typical ofmodern humans. They reported that theangle made by the ‘ventral bar’ along thelateral border of the scapula and theglenoid fossa was found to be 145° inhumans and 130° in specimen AL 288-1(fig 3). The smaller angle reflects aglenoid fossa directed far more superiorlyand this is also evident in other primates,such as chimpanzees (Oxnard, 1984;Larson, 1988) (fig 4). The scapula of A afarensis appears to be more like that ofmodern apes than that of modernhumans. This may indicate that the armwas habitually used in an elevated positionas would be common during climbingbehaviour. It seems that the modernglenoid fossa is less well adapted for

Fig 3: Comparison of scapula of A afarensis (left) and Homo sapien sapiens.Anterior views show ‘ventral bar’and the ‘bar-glenoid’ angle. The angle of A afarensis is 130° in comparison to the angle in a typical human scapula(145°). It can be clearly seen that the glenoid is directly significantly morecranially in A afarensis (Stern and Susman, 1983, page 285)

Fig 2: Comparison of primate (left) and Homo sapien sapiens skeletaldifferences, showing postural differences between quadrupedalism andbipedalism. Gorilla pelvis is longer and angled and forelimbs are longer thanhindlimbs; thorax is wide anteroposteriorly. In comparison, modern Homosapien sapiens has a short, vertically orientated pelvis and upper limbsshorter than lower limbs (Isaac and Leakey, 1979, page 57)

Vertebralborder

130˚145˚

Vertebralborder



activities involving elevation than it was inthe early hominids and the present-dayapes.

Another feature facilitating function inelevation is the superiorly directed flare ofthe lateral end of the clavicle evident inapes (Oxnard, 1984) (fig 5). The claviclefunctions as a weight-bearing strut(Abbott and Lucas, 1954; Moseley, 1968)between the upper limb and axialskeleton. The cranial flare of the outerend of the clavicle may facilitate elevationby providing more bony support to theacromion during overhead activities andmay allow for a greater range of elevation(Aiello and Dean, 1990). In comparisonmodern humans have a flattened lateralend of the clavicle (Ashton and Oxnard,1964). A cranial flare may also lessen thechance of acromioclavicular degenerationimpinging within the subacromial spaceas described by Neer (1983).

There are also a number of muscularfactors which suggest that the adaptationof the modern human shoulder girdle is compromised for use in elevatedpositions. The orientation of the mainupward rotators of the scapula, theserratus anterior and upper trapezius,resemble those of quadrupeds and notapes (Oxnard, 1967). This may imply thatthe muscles controlling the scapula inelevation are not well adapted to hold thescapula in an upwardly rotated position,especially for prolonged periods. Theevolutionary process has involved a sign-ificant increase in size of the infrascapularfossa, and the infraspinatus and teresminor have evolved as large and powerfulmuscles (Roberts, 1974; Larson and Stern,1989). However, in contrast to thesuprascapular fossa, the origin of thesupraspinatus has become relativelysmaller. As the supraspinatus works withdeltoid to elevate the arm (Otis, et al1994) it may be required to workrelatively harder in the modern shouldergirdle. This may predispose it to overuseand breakdown and degeneration of itscollagenous tissue structures, factorswhich have been associated with SIS(Nirschl, 1979). Atlanto-cervicalis(omocervicalis) arises from the spinousprocess of the atlas and inserts into thelateral margin of the clavicle. This musclewhose action is to assist shoulder girdleelevation, is present in apes, but has beenlost in humans (Miller, 1932). Further, thescapular rotator muscles of humans and

apes differ morphologically. Gorillas andchimpanzees have a more extensive,shorter and thicker upper trapezius thanhumans and the rhomboid of these greatapes originates from the occiput. Thesefactors would provide a better mechanicaladvantage for scapular rotation in theapes than they would for humans.

Modern humans have evolved a largeand relatively flat acromion (Gregory,1928). Oxnard (1984) clearly demon-strated that the human acromion faceslaterally and is placed over the glenoidfossa, whereas the acromia of the threegreat apes (gorilla, chimpanzee andorang-utan) are directed superiorly away

Fig 4: Comparison of scapulae of Homo sapien sapiens (left) and modernprimate. Direction of human glenoid fossa and acromion is clearly differentfrom that of a great ape (adapted from Oxnard, 1984, page 324)

Figure 5: Certain primates such as the chimpanzee (Pan troglodytes, top)exhibit a flare at the lateral end of the clavicle. This may assist shoulderelevation. The human clavicle has no such flare (Oxnard, 1984, page 326)

Medial Lateral


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from and above the fossa. In studies ofSIS, acromia with a small slope, or with ananterior aspect in close proximity to thesubacromial space, have been found tohave the highest correlation withsubacromial pathology (Bigliani et al,1986; Aoki et al, 1986; Morrison andBigliani 1987; Flatow et al, 1994).

Further, suspensory behaviour or usingthe upper limb in elevated position forarboreal locomotion has shown to be afunction of body size and scapular shape.The bonobos (Pan paniscus) was found touse suspensory activity more and to bemore arboreal than the chimpanzee (Pantroglodytes). As well as having a smallerbody than the chimpanzee, the bonoboshas a longer and narrower scapula thanthe chimpanzee (Doran, 1993). In turnthe gorilla is heavier and has a muchbroader scapula than the chimpanzee anddemonstrates significantly less overheadsuspensory behaviour (Doran, 1997).These morphological differences in bodysize and scapula shape suggest largerbodies with broader scapulae are less well adapted to participate in over-head activity. Modern humans have thebroadest scapulae and are among thetallest and heaviest of the primates.

Numerous sporting and vocationalactivities demand repeated use of the armin elevation, which may subject theshoulder to a variety of pathologies. Therange of elevation has been quoted as180˚ (Kent, 1971; Calliet, 1991). However,Boone and Azen (1979) reported that themean range for 109 male subjects agedbetween 1 and 19 years was 168.4˚, and165˚ for those aged between 20 and 54years. Therefore the modern human armmight not achieve the apparently verticalposition of the upper limb as demon-strated by other primates when brach-iating.

Subacromial impingement has beendescribed as the most common form ofshoulder pathology and is associated withpain and loss of function, primarily whenthe arm is used in elevated positions.Rehabilitation programmes for impinge-ment vary and protocols depend onclinical findings. When designing atreatment plan the initial aim is usually to reduce pain and then gradually toincrease painfree range, while addressingany deficiencies in muscle function,posture, scapula and glenohumeralstability and proprioception.

Physiotherapists generally provideergonomic advice to their clients, basedon physiological and biomechanicalinformation, on how the body is capableof functioning within various parameters,and how best to function within theirenvironments.

Although many occupations, sports andhobbies involve repeated and extendeduse of the arm in elevation some evidencesuggests that various anatomical con-straints may predispose pathology duringthis type of activity. Although it is notnecessary or useful to advise patients tostop these activities or postures, therelevance of these constraints needs to beconsidered. Before discharging a patient,physiotherapists generally ensure thatglenohumeral joint range, scapularmovement and function, local andgeneral muscle function, and the spinalcontribution to arm elevation have beenassessed and treated. Ergonomic advice is based upon the relationship betweenthe person and the environment. Theseclinical, functional and ergonomic issuesare addressed to treat the presentingpathology and minimise the risk ofrecurrence. Evolutionary constraints areone of many possible factors deservingconsideration.

ConclusionThe modern human shoulder girdle isstructurally and subtly different from ourevolutionary ancestors as well as frommodern apes. There is some evidence tosuggest that the modern human shouldergirdle is less well adapted for overheadactivities, especially those involving poweror prolonged effort.

Osteological differences betweenhumans and other primate shoulderjoints are found primarily in the scapulaand the clavicle. These differencesinclude a relatively small suprascapularfossa (Roberts, 1974; Larson and Stern,1989), and an orientation of the upwardscapular rotators that resembles those ofprimate quadrupeds and not apes(Oxnard, 1967). Other features whichsuggest that the modern human arm hasnot evolved for powerful or prolongedactivities in elevation include a glenoidfossa which faces laterally and notcranially as in apes and our evolutionaryancestors (Stern and Susman, 1983). Thelateral end of the modern human claviclefaces laterally and does not exhibit an



upward flare as in primates such as thechimpanzee (Schultz, 1930). The humanacromion is flat and faces laterally overthe glenoid fossa and is not directedsuperiorly above the fossa as in the greatapes (Oxnard, 1984). The smaller supra-scapular fossa implies a relatively smallersupraspinatus. Overhead activity maytherefore predispose this muscle tofatigue and the consequences of fatigue atan earlier point than in primates and ourevolutionary ancestors.

Although the timeframe, progressionand reasons for adopting a bipedalposture are not known, the non-weight-bearing upper limb and theuniquely mobile shoulder girdle haveunquestionably allowed modern Homosapien sapiens to participate in anunparalleled array of sporting, vocationaland cultural activities. However, theshoulder is susceptible to injury inelevation, with subacromial impingementsyndrome being part of the spectrum ofpathology.

Authors

Jeremy Lewis MScMAPA MCSP MMPAAMMACP is a PhDcandidate at CoventryUniversity andresearch co-ordinatorin the department ofphysiotherapy,Chelsea andWestminster Hospital.

Ann Green MScMCSP is principallecturer, School ofHealth and SocialSciences, CoventryUniversity.

Ziva Yizhat PhD BPTis a lecturer in theSchool ofPhysiotherapy, Tel Aviv University.

Donald PenningtonPhD is professor andpro vice-chancellor,Coventry University.

This article wasreceived on February4, 2000, and acceptedon October 5, 2000.

Address forCorrespondence

Jeremy Lewis,Research Co-ordinator,Department ofPhysiotherapy,Chelsea andWestminster Hospital,369 Fulham Road,London SW10 9NH.

[email protected]

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Key Messages

� Subacromialimpingement hasbeen described asthe most commonof shoulderpathologies.

� Evolutionarytheory suggests aprogression fromquadrupedal tobipedal posture andgait, with resultantmusculoskeletaladaptations.

� The evolutionaryadaptations of themodern humanshoulder girdle aredifferent from thoseof early hominidsand the great apes.

� Biomechanically,the humanshoulder girdle maybe less well suited toperform activitieswith the arm in theoverhead position,which maypredispose it tosubacromialimpingement whenelevated.

subacromial impingement syndrome: has evolution failed us?

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