Musculoskeletal stress markers (MSM):

methodological reflections

Valentina Mariotti, Marco Milella, Maria Giovanna Belcastro

Laboratorio di Bioarcheologia e Osteologia ForenseDipartimento di Biologia Evoluzionistica Sperimentale

Via Selmi, 3 - 40126 Bologna, Italia

3. Discuss the interpretative possibilities of MSM: the results of the study of an identified skeletal sample

AIM

1. Comment on some terminological ambiguity

2. Illustrate our scoring method, justifying the choices we made

Mariotti V. (1998) Ricerche sugli indicatori scheletrici morfologici di attività. PhD thesis, Università di Bologna.

Mariotti V. et al. (2004) Enthesopathies: proposal of a standardised scoring method and applications. CollegiumAntropologicum, 28/1: 145-159.

Mariotti V. et al. (2007) The Study of Entheses: Proposal of a Standardised Scoring Method for Twenty-three Entheses of the Postcranial Skeleton. Collegium Antropologicum, 31/1: 291-313.

Hawkey D.E. (1988) Use of upper extremity enthesopathies to indicate habitual activity patterns. MA Thesis, Arizona State University, Tempe.

Hawkey D.E., Merbs C.F. (1995) Activity-induced musculoskeletal stress markers (MSM) and subsistence strategy changes among ancient Hudson Bay Eskimo. International Journal of Osteoarchaeology, vol. 5: 324-338.

Robb J. (1994) Issues in the skeletal interpretation of muscle attachments (Presented at the Annual Meeting of the Paleoanthropology Society, Anaheim, California, April 19-20 1994).

Villotte S. (2008) Enthésopathies et activités des hommes préhistoriques. Recherche méthodologique et application aux fossiles européens du Paléolithique supérieur et du Mésolithique. Thèse de Doctorat, Université de Bordeaux 1.

1. Terminology

MSM: Hawkey and Merbs (1995): marks “that occur where a muscle, tendonor ligament inserts onto the periosteum and into the ubderlying bony cortex.”

Invalidant conditions (fractures, luxations, amputations, etc.)

Some pathologies(DISH, etc.)

age

Type and/or level of physical activity

Individual factors(genetics)

Bone architecture

Habitualpostures

Markers of occupational stress (MOS)

very prominent, but surfacesmooth

not prominent, but surfacerough

evidententhesophyte

very prominentmedial border

smallenthesophyte

enthesophytes, erosions

pitting

??ENTHESOPATHY??

Sardinia, ossuary

(Mariotti et al., 2004, 2007)

Robusticity: “normal” surface irregularity or rugosity

“osteolytic” lesion (OL): presence of pitting or eroded areas

enthesophitic formation (EF): presence of enthesophytes

MSM(Hawkey and Merbs, 1995)

Robusticity marker: ”…normal reaction …to habitual muscle usage…seen in its mostextreme expression as sharp ridges, or crests, of bone.”

Stress lesion: “…pitting, or ‘furrow’, into the cortex to the degree it superficiallyresembles a lytic lesion.”

Ossification exostosis: “…exostosis, or bony ‘spur’.”

Pathological

1. denoting an abnormal finding, particularly a morphological alteration

2. resulting from disease(International Dictionary of Medicine and Biology, Whiley and Sons, 1986)

“pathological” bone response to stress.

Enthesopathy

2. Scoring method

Descriptive standard for evaluation of

type of bone change (ROB, EF, OL)

degree of development

Standardised scoring methodReproducible observationsComparable results

MSMqualitative nature + continuous variation

macroscopic observationsubjectivity

23 entheses of postcranial skeleton

1a 1b 1c 32

1a - slight impression: the surface is practically smooth, even though an oblique line is perceptible to the touch.

1b – low development: the insertion is marked by a line of rugosity.

1c – medium development: the line of insertion is marked by obvious rugosity, or there is a slight crest with smooth surface.

2 - high development: definite crest, possibly discontinuous, but with obvious rugosity.

3 – very high development: very raised and rugose crest.

ROBUSTICITY (standard different for each enthesis) (Mariotti et al., Coll. Antrop., 2007)1 – low to medium development

2 – high development

3 – very high development M. SOLEUS

Interobserver error: about 20%

ENTESOPATHIES (standard applicable to any enthesis)(Mariotti et al., Coll. Antropol., 28 (1), 2004)

1 2 3

ENTESOPHYTIC FORMATION (EF)

0 – absence

1 - minimal exostosis (<1 mm)

2 - clear exostosis (1-4 mm)

3 - substantial exostosis (>4 mm)

nr – more than 50% of the area is illegible

Interobserver error : about 5%

“OSTEOLYTIC” FORMATION (OL)0 - absence

1 - fine porosity (holes <1mm)

2 - gross porosity, (holes ∼ 1 mm) or small area of erosion (∼ 4 mm)

3 - a: several small areas of erosion (∼ 4 mm); b: extensive and deep osteolytic area (> 4 mm)

nr – more than 50% of the area is illegible

1 2 3ba

1 2

1: ‘pitting’ 2 and 3: ‘erosions’

Attention !!!

1

…

m.brachioradialis

m.deltoideus

m.lat.dorsii/teres m.

m.pectoralis major

humerus

m.deltoideus

m.pectoralis major

trapezoid lig.

…conoid lig.

202202costoclavicular lig.

clavicle

102001cm.triceps brachii

scapula

OLEFrob.OLEFrob.OLEFrob.OLEFrob.

rightleftrightleft

YA/MA/OA/NIM / F / NIYA/MA/OA/NIM / F / NIsex / age

N° 33Specimen

Data collecting form

Identification of the factors that influence the expression of MSM3. Interpretation

Difficulty of recognising which factors are responsible for the featureobserved and to which extent, respectively

1. multifactorial etiology (genetic and environmental factors)

age

genetics

disease

activity

sex factors

… …

2. monotone bone response to stress (bone production – bone resorption)

No biunivocalcorrespondencebetweenetiologicalfactors and bone changes

living persondry boneMaterial

symptoms, anamnesis, medical tests, evolution of

disease

pattern of bonyalterations

Diagnosis

dynamic prcessstatic situationEvolution

possiblenot possibleSoft tissuesobservation

indirect(x-rays, tomography, etc.)

direct(> resolution)

Bone observation

diseasevariabilityInterest

MedicalAnthropologicalApproach

1. Anthropological: study of identified skeletal collections (known age, sex, etc.)

2. Medical: clinical cases of occupational and sports medicine

Possible approaches:

The “Frassetto” identified skeletal collections (known age, sex, occupation)(Museum of Anthropology, University of Bologna, Italy)

Sassari (SS – Sardinia, Italy), end of 19th-beginning of 20th c.

(pathological specimens or specimens with uncertain age excluded)

486

212

274

Tot

Tot

Females

Males

163155168

626684

1018984

> 50(OA)

36-50(MA)

20-35(YA)

occupation known: 173 M (39% farmers)

125 F (95% housewives)

entheses grouped into six “FUNCTIONAL COMPLEXES”upper limb: shoulder, elbow -flexion/extension, forearm-pronation/supinationlower limb: hip, knee, foot

Mean score: mean degree of development of the entheses of each “functional complex”

METHODSMales

L R

YA MA OA

Females

L R

YA MA OA

frequencies (%) for each ENTHESIS:

ROB: grades 1, 2+3 (low-medium / high development)

EF: grades 0+1, 2+3 (absence / presence)

OL: grades 0, 1, 2+3 (absence / pitting / erosions)

- differences among age classes in M and F respectively: p (χ2)

- differences betweensexes or sides withineach age class: p (Fisher)

-relation age/score: Spearman R and relative p value

-side differences: Wilcoxon matched pairs test

- sex and activity differences: Mann-Whitney U test

0,4420,3270,5070,3070,0140,790foot0,5480,1720,3750,8080,5130,557knee0,1840,2650,0290,2450,8260,638hip0,4920,0580,0710,7120,1640,818lower limb

0,1720,0200,1140,5100,1120,038forearm0,0010,0190,0280,9940,5040,980elbow0,0000,0000,0010,8950,0410,000shoulder0,0000,0000,0000,6280,0690,000upper limb

ppppppN=86-96N=70-82N=61-75N=50-61N=51-63N=59-75

OAMAYAOAMAYA

MFL / R

ROBUSTICITY – BILATERAL ASYMMETRY(Wilcoxon matched pairs test)

1. bilateral asymmetry in both sexes upper limb

2. bilateral asymmetry decreases with age in F, remains stable in M

ROBUSTICITY – SEX DIFFERENCES(Mann-Whitney U test)

2,652,590,0402,211,981,491,40foot2,172,361,921,921,461,42knee2,522,912,162,261,731,75hip2,372,582,052,031,521,51lower limb

1,852,551,561,580,0311,120,93forearmR2,002,430,0261,692,011,491,47elbow2,022,351,901,900,0361,731,61shoulder

0,0321,992,441,771,880,0441,551,46upper limb0,0082,632,812,111,991,541,35foot

2,182,331,881,851,471,38knee2,482,882,162,241,731,66hip

0,0052,372,612,032,011,551,45lower limb

0,0001,852,471,471,500,0211,070,88forearmL2,022,311,731,951,461,44elbow2,012,221,841,761,571,51shoulder

0,0051,982,301,761,771,461,36upper limbpFM pFM pFM

OAMAYAmean score

F>M M>F or F>M M>F

CORRELATION ROB - AGE

p<0.000010,680,66lower limb

0,530,64foot

0,580,50knee

0,670,54hip

0,690,52upper limb

0,760,56forearm

0,610,45elbow

0,520,32shoulder

RIGHT

0,670,66lower limb

0,580,61foot

0,550,52knee

0,680,51hip

0,690,58upper limb

0,760,55forearm

0,590,49elbow

0,510,44shoulder

LEFT

M(N: 226-268)

F(N: 173-202)Spearman R

age effect: microtrauma from normal body movements accumulating on entheses over time

expected pattern: higher age correlation for the lower limb (locomotion)

lower age correlation for upper limb (more movements possible)

M more correlated with age than F

• Bilateral asymmetry

• YA: F>M; OA: M>F

Hp:• young F worked hard• developed entheses in spite of the young age

lower correlation coefficient with age

Mechanical stress or sex factors?

0,00038,719,04,30,00032,316,94,3Achilles tendon CA

0,8444,03,42,50,1767,12,32,5m.soleus TI

0,04613,19,42,60,06212,18,02,5qudriceps tendon TI

0,00119,511,51,30,00020,910,30,0quadriceps tendon PA

0,07912,04,54,80,00315,06,81,2m.iliopsoas FE

0,01010,93,90,00,0806,53,60,0m.triceps brachii UL

0,2074,13,50,00,0757,22,31,2m.biceps brachii RA

0,3305,02,31,30,0065,90,00,0m.deltoideus CL

N=92-101N=76-89N=67-84N=91-101N=78-88N=70-83P(χ2)OAMAYAP(χ2)OAMAYA

RIGHTLEFTMales

0,00062,515,04,00,00056,114,87,4Achilles tendon CA

0,2931,60,00,01,60,00,0m.soleus TI

0,7131,73,11,20,2763,33,00,0qudriceps tendon TI

0,00036,813,61,40,00032,115,03,9quadriceps tendon PA

0,0568,11,61,30,00013,10,00,0m.iliopsoas FE

0,0467,50,01,61,91,71,4m.triceps brachii UL

0,1064,91,60,05,00,00,0m.biceps brachii RA

0,00012,90,00,00,00011,50,00,0m.deltoideus CL

N=53-62N=57-66N=63-83N=57-61N=60-66N=74-82

P(χ2)OAMAYAP(χ2)OAMAYA

RIGHTLEFTFemalesFrequency of EF (2+3%)

0,0

5,0

10,0

15,0

20,0

25,0

30,0

cost

ocla

v. C

L

delto

ideu

s C

L

pect

oral

is m

. HU

lat.d

./ter

es m

a. H

U

bice

ps b

r. R

A

sole

us T

I

cost

ocla

v. C

L

delto

ideu

s C

L

pect

oral

is m

. HU

lat.d

./ter

es m

a. H

U

bice

ps b

r. R

A

sole

us T

I

Females - LEFT

YAMAOA

0,0

10,0

20,0

30,0

40,0

50,0

60,0

70,0

cost

ocla

v. C

L

delto

ideu

s C

L

pect

oral

is m

. HU

lat.d

./ter

es m

a. H

U

bice

ps b

r. R

A

sole

us T

I

cost

ocla

v. C

L

delto

ideu

s C

L

pect

oral

is m

. HU

lat.d

./ter

es m

a. H

U

bice

ps b

r. R

A

sole

us T

I

Males - LEFT

YAMAOA

PITTING (grade 1) EROSIONS (grade 2+3)

Frequency of OL (1% - 2+3%)

Males

significant differences among age classes

pitting (OL 1) increases with age

erosions (OL 2+3) decreases with age (except m. biceps brachii)

Females

no significant differences among age classes (except m. biceps brachii)

no age pattern

erosions more frequent in Mpitting more frequent in F

PITTING (grade 1) EROSIONS (grade 2+3)

EROSIONS PITTING

Maleserosions juvenile featurepitting elderly feature

R HumerusSardinia, ossuary

R TibiaVCN t. 155 (Y)

m. soleus

R HumerusTf XXVII-2 (M?, Y)

L HumerusSS 296 M, 62 y.

m. pectoralis major

m. pectoralis major

m. latissimus dorsii/ teres major

bone metabolism changes through time, bone response thus different?

OCCUPATION

Males with known occupation

173 males with known occupation, performing 47 different jobs!

39% farmers, 5% masons …

237313traders/employees

173565958MALES

49231511other

craftsmen

farmers

3410915

67163219

TotOAMAYA

Few significant differences between jobs

Entheses and enthesopathies as activity markers

age markers influenced by activity

instead of

activity markers influenced by age!

Increasing development of ROB and EF with age adaptive response of the bone to microtraumas from normal body movements accumulating over time.EF, OL more frequent at some entheses: maybe in relation to the anatomical structure of the enthesis

Concluding remarks 1

“The increased surface area created at the tendon-bone junction may be an adaptivemechanism to ensure the integrity of the interface in response to increased mechanicalloads. … … …Bony spur formation in the rat Achilles tendon … is essentially an extension of normal bonedevelopment and is endochondral ossification through fibrocartilage rather than hyalinecartilage.” (Benjamin et al., 2000)

But a hope remains …1. The study of homogeneous samples with respect

to the occupation gave interesting results (seeMilella et al. on porters and shoemakers -TOMORROW!!!)

2. The study of MSM and joint features in individuals with altered patterns of locomotionhighlighted the influence of mechanical stress, in agreement with medical data (Belcastro and Mariotti, 2000; Mariotti and Belcastro 2001)

Two Roman skeletons fromCasalecchio (Bologna, II-III AD)

Concluding remarks 2

3. Our results are referred to only 23 entheses, and maybe other entheses are more sensible tomechanical stress

4. We analised only the Sassari sample, but thereare many other known collections that can bestudied and that may give different results

To obtain reliable results about past activities:

1. Exclude individuals affected with diseases influencing the featuresconsidered (e.g. DISH)

2. Exclude individuals with generalised high or low development of enthesesConsider only individuals presenting - clear bilateral asymmetry

- only some entheses developed

3. Compare groups of the same sex and age class (or at least with the same age distribution), better if MA (or YA)

4. Consider all the possible activity markers (not only MSM)

5. Be very careful in the interpretation (taking into account possible sampling problems, the age, and, obviously, the archaeological or historical record)

Concluding remarks 3

Scoring method:

Record ROB, EF and OL separately: they do not behave in the same way in relation to age