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    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

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    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 ofphysical activity

    Individual factors(genetics)

    Bone architecture

    Habitualpostures

    Markers of occupational stress(MOS)

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    very prominent,but surfacesmooth

    not prominent,but surfacerough

    evidententhesophyte

    very prominentmedial border

    smallenthesophyte

    enthesophytes,erosions

    pitting

    ??ENTHESOPATHY??

    Sardinia,ossuary

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    (Mariotti et al., 2004, 2007)

    Robusticity : normal surface irregularity or rugosityosteolytic 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 usageseen 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 boneresponse to stress.

    Enthesopathy

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    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 ofpostcranial skeleton

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    1a 1b 1c 32

    1a - slight impression : the surface is practically smooth, even though an oblique line is perceptibleto 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 slightcrest 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%

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    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 (4 mm)nr more than 50% of the area isillegible

    Interobserver error : about 5%

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    OSTEOLYTIC FORMATION (OL)0 - absence

    1 - fine porosity (holes 4 mm)nr more than 50% of the area isillegible

    1 2 3ba

    1 2

    1: pitting 2 and 3: erosions

    Attention !!!

    1

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    m.brachioradialis

    m.deltoideus

    m.lat.dorsii/teres m.

    m.pectoralis major

    humerus

    m.deltoideus

    m.pectoralis major trapezoid lig.

    conoid lig.

    202202costoclavicular lig.

    clavicle102001cm.triceps brachii

    scapula

    OLEFrob.OLEFrob.OLEFrob.OLEFrob.

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

    N 33Specimen

    Data collecting form

    3 I i

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    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

    diseaseactivity

    sex factors

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

    No biunivocal

    correspondencebetweenetiologicalfactors andbone changes

    bl h

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    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

    diseasevariabilityInterestMedicalAnthropologicalApproach

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

    2. Medical: clinical cases of occupational and sports medicine

    Possible approaches:

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

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

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

    Mean score : mean degree of development of theentheses of each functional complex

    METHODSMales

    L RYA MA OA

    Females

    L RYA 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 Frespectively: p ( 2)

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

    -relation age/score:Spearman R and

    relative p value-side differences:Wilcoxon matched pairstest

    - sex and activitydifferences: Mann-Whitney U test

    ROBUSTICITY BILATERAL ASYMMETRY

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    0,4420,3270,5070,3070,0140,790foot

    0,5480,1720,3750,8080,5130,557knee

    0,1840,2650,0290,2450,8260,638hip0,4920,0580,0710,7120,1640,818lower limb0,1720,0200,1140,5100,1120,038forearm

    0,0010,0190,0280,9940,5040,980elbow0,0000,0000,0010,8950,0410,000shoulder

    0,0000,0000,0000,6280,0690,000upper limbpppppp

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

    OAMA YAOAMA YA

    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

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    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 limbpFMpFMpFM

    OAMA YAmean score

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

    CORRELATION ROB AGE

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    CORRELATION ROB - AGE

    pM; 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?

    Frequency of EF (2+3%)

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

    0,8444,03,42,50,1767,12,32,5m.soleus TI0,04613,19,42,60,06212,18,02,5qudriceps 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=92-101 N=76-89 N=67-84 N=91-101 N=78-88 N=70-83

    P( 2)OAMA YAP( 2)OAMA YA

    RIGHT LEFT Males

    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 TI0,00036,813,61,40,00032,115,03,9quadriceps 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=53-62 N=57-66 N=63-83 N=57-61 N=60-66 N=74-82

    P( 2)OAMA YAP( 2)OAMA YA

    RIGHT LEFT FemalesFrequency of EF (2+3%)

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

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

    Frequency of OL (1% 2 3%)

    Males

    significant differences amongage classes

    pitting (OL 1) increases withage

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

    Females

    no significant differencesamong 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)

    R Humerusd

    R Tibia( )

    R Humerusf ( )

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    EROSIONS PITTING

    Males

    erosions juvenile featurepitting elderly feature

    Sardinia, ossuaryVCN t. 155 (Y)

    m. soleus

    Tf XXVII-2 (M?, Y)

    L HumerusSS 296 M, 62 y.

    m. pectoralis major

    m. pectoralis major

    m. latissimus dorsii / teres major

    bone metabolism changes throughtime, bone response thus different?

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    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 significantdifferences

    between jobs

    Concluding remarks 1

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    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 ofthe 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

    g

    The increased surface area created at the tendon-bone junction may be an adaptive mechanism to ensure the integrity of the interface in response to increased mechanical loads.

    Bony spur formation in the rat Achilles tendon is essentially an extension of normal bone development and is endochondral ossification through fibrocartilage rather than hyaline cartilage . (Benjamin et al., 2000 )

    Concluding remarks 2

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    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 inindividuals with altered patterns of locomotionhighlighted the influence of mechanical stress, inagreement with medical data (Belcastro and Mariotti,2000; Mariotti and Belcastro 2001)

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

    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

    Concluding remarks 3

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    To obtain reliable results about past activities:1. Exclude individuals affected with diseases influencing the features

    considered (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 sameage 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)

    g

    Scoring method:

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