musculoskeletal stress markers (msm): methodological
TRANSCRIPT
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