Musculoskeletal stress markers (MSM): methodological reflections

Laboratorio di Bioarcheologia e Osteologia Forense
Dipartimento di Biologia Evoluzionistica Sperimentale
Via Selmi, 3 - 40126 Bologna, Italia
Musculoskeletal stress markers (MSM):
methodological reflections
Valentina Mariotti, Marco Milella, Maria Giovanna Belcastro
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. Collegium
Antropologicum, 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.
3. Discuss the interpretative possibilities of MSM: the results of
the study of an identified skeletal sample
1. Terminology
MSM:
Hawkey and Merbs (1995): marks “that occur where a muscle, tendon
or ligament inserts onto the periosteum and into the ubderlying bony cortex.”
Invalidant conditions (fractures,
luxations, amputations, etc.)
age
Some pathologies
(DISH, etc.)
Markers of occupational stress
(MOS)
Type and/or level of
physical activity
Bone architecture
Habitual
postures
Individual factors
(genetics)
very prominent,
but surface
smooth
not prominent,
but surface
rough
evident
enthesophyte
very prominent
medial border
Sardinia,
ossuary
small
enthesophyte
??ENTHESOPATHY??
enthesophytes,
erosions
pitting
MSM
(Hawkey and Merbs, 1995)
Robusticity marker: ”…normal reaction …to habitual muscle usage…seen in its most
extreme expression as sharp ridges, or crests, of bone.”
Stress lesion: “…pitting, or ‘furrow’, into the cortex to the degree it superficially
resembles a lytic lesion.”
Ossification exostosis: “…exostosis, or bony ‘spur’.”
(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
Enthesopathy
“pathological” bone
response to stress.
Pathological
1.
denoting an abnormal finding, particularly a morphological alteration
2.
resulting from disease
(International Dictionary of Medicine and Biology, Whiley and Sons, 1986)
2.
Scoring method
Standardised scoring method
Reproducible observations
Comparable results
MSM
qualitative nature + continuous variation
macroscopic observation
subjectivity
Descriptive standard for evaluation of
type of bone change (ROB, EF, OL)
degree of development
23 entheses of
postcranial skeleton
ROBUSTICITY (standard different for each enthesis) (Mariotti et al., Coll. Antrop., 2007)
1 – low to medium development
Interobserver error: about 20%
2 – high development
3 – very high development
M. SOLEUS
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.
1a
1b
1c
2
3
ENTESOPATHIES (standard applicable to any enthesis)
(Mariotti et al., Coll. Antropol., 28 (1), 2004)
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%
1
2
3
“OSTEOLYTIC” FORMATION (OL)
1: ‘pitting’
0 - absence
2 and 3: ‘erosions’
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)
1
2
a
b
3
nr – more than 50% of the area is
illegible
1
2
Attention !!!
1
Data collecting form
Specimen
N° 33
sex / age
M / F / NI
YA/MA/OA/NI
M / F / NI
YA/MA/OA/NI
left
right
left
right
rob.
EF
OL
rob.
EF
OL
1c
0
0
2
0
1
costoclavicular lig.
2
0
2
2
0
2
conoid lig.
…
scapula
m.triceps brachii
clavicle
trapezoid lig.
m.pectoralis major
m.deltoideus
humerus
m.pectoralis major
m.lat.dorsii/teres m.
m.deltoideus
m.brachioradialis
…
rob.
EF
OL
rob.
EF
OL
3.
Interpretation
Identification of the factors that influence the expression of MSM
1.
multifactorial etiology (genetic and environmental factors)
2. monotone bone response to stress (bone production – bone resorption)
age
genetics
disease
activity
sex factors
……
No biunivocal
correspondence
between
etiological
factors and
bone changes
Difficulty of recognising which factors are responsible for the feature
observed and to which extent, respectively
Possible approaches:
1.
Anthropological: study of identified skeletal collections (known age, sex, etc.)
2.
Medical: clinical cases of occupational and sports medicine
Approach
Anthropological
Medical
Interest
variability
disease
Material
dry bone
living person
Bone observation
direct
(> resolution)
indirect
(x-rays, tomography, etc.)
Soft tissues
observation
not possible
possible
Evolution
static situation
dynamic prcess
Diagnosis
pattern of bony
alterations
symptoms, anamnesis,
medical tests, evolution of
disease
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.
20-35
(YA)
36-50
(MA)
> 50
(OA)
Tot
Males
84
89
101
274
Females
84
66
62
212
Tot
168
155
163
486
(pathological specimens or specimens with uncertain age excluded)
occupation known: 173 M (39% farmers)
125 F (95% housewives)
METHODS
Males
L
YA
Females
R
MA
L
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)
entheses grouped into six “FUNCTIONAL COMPLEXES”
upper limb: shoulder, elbow -flexion/extension,
forearm-pronation/supination
lower limb: hip, knee, foot
Mean score: mean degree of development of the
entheses of each “functional complex”
YA
R
MA
OA
- differences among age
classes in M and F
respectively: p (χ2)
- differences between
sexes or sides within
each age class: p (Fisher)
-relation age/score:
Spearman R and
relative p value
-side differences:
Wilcoxon matched pairs
test
- sex and activity
differences: MannWhitney U test
ROBUSTICITY – BILATERAL ASYMMETRY
(Wilcoxon matched pairs test)
L / R
1.
F
M
YA
MA
OA
YA
MA
OA
N=59-75
N=51-63
N=50-61
N=61-75
N=70-82
N=86-96
p
p
p
p
p
p
upper limb
0,000
0,069
0,628
0,000
0,000
0,000
shoulder
0,000
0,041
0,895
0,001
0,000
0,000
elbow
0,980
0,504
0,994
0,028
0,019
0,001
forearm
0,038
0,112
0,510
0,114
0,020
0,172
lower limb
0,818
0,164
0,712
0,071
0,058
0,492
hip
0,638
0,826
0,245
0,029
0,265
0,184
knee
0,557
0,513
0,808
0,375
0,172
0,548
foot
0,790
0,014
0,307
0,507
0,327
0,442
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)
mean score
L
R
YA
M
F
upper limb
1,36
shoulder
MA
M
F
M
F
p
1,46
1,77
1,76
2,30
1,98
0,005
1,51
1,57
1,76
1,84
2,22
2,01
elbow
1,44
1,46
1,95
1,73
2,31
2,02
forearm
0,88
1,07
1,50
1,47
2,47
1,85
0,000
lower limb
1,45
1,55
2,01
2,03
2,61
2,37
0,005
hip
1,66
1,73
2,24
2,16
2,88
2,48
knee
1,38
1,47
1,85
1,88
2,33
2,18
foot
1,35
1,54
1,99
2,11
2,81
2,63
0,008
upper limb
1,46
1,55
0,044
1,88
1,77
2,44
1,99
0,032
shoulder
1,61
1,73
0,036
1,90
1,90
2,35
2,02
elbow
1,47
1,49
2,01
1,69
2,43
2,00
forearm
0,93
1,12
1,58
1,56
2,55
1,85
lower limb
1,51
1,52
2,03
2,05
2,58
2,37
hip
1,75
1,73
2,26
2,16
2,91
2,52
knee
1,42
1,46
1,92
1,92
2,36
2,17
foot
1,40
1,49
1,98
2,21
2,59
2,65
F>M
p
OA
0,021
0,031
M>F or F>M
p
0,026
0,040
M>F
CORRELATION ROB - AGE
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)
F
(N: 173-202)
M
(N: 226-268)
shoulder
0,44
0,51
elbow
0,49
0,59
forearm
0,55
0,76
upper limb
0,58
0,69
hip
0,51
0,68
knee
0,52
0,55
• Bilateral asymmetry
foot
0,61
0,58
lower limb
0,66
0,67
• YA: F>M;
shoulder
0,32
0,52
elbow
0,45
0,61
forearm
0,56
0,76
upper limb
0,52
0,69
hip
0,54
0,67
knee
0,50
0,58
foot
0,64
0,53
lower limb
0,66
0,68
Spearman R
LEFT
RIGHT
p<0.00001
M more correlated with age than F
Mechanical stress or sex factors?
OA: M>F
Hp:
• young F worked hard
• developed entheses in spite of the
young age
lower correlation coefficient with age
Frequency of EF (2+3%)
Females
LEFT
RIGHT
YA
MA
OA
N=74-82
N=60-66
N=57-61
m.deltoideus CL
0,0
0,0
11,5
m.biceps brachii RA
0,0
0,0
m.triceps brachii UL
1,4
m.iliopsoas FE
YA
MA
OA
N=63-83
N=57-66
N=53-62
0,0
0,0
12,9
0,000
5,0
0,0
1,6
4,9
0,106
1,7
1,9
1,6
0,0
7,5
0,046
0,0
0,0
13,1
0,000
1,3
1,6
8,1
0,056
quadriceps tendon PA
3,9
15,0
32,1
0,000
1,4
13,6
36,8
0,000
qudriceps tendon TI
0,0
3,0
3,3
0,276
1,2
3,1
1,7
0,713
m.soleus TI
0,0
0,0
1,6
0,0
0,0
1,6
0,293
Achilles tendon CA
7,4
14,8
56,1
4,0
15,0
62,5
0,000
P(χ2)
Males
P(χ2)
0,000
0,000
LEFT
P(χ2)
RIGHT
YA
MA
OA
N=70-83
N=78-88
N=91-101
m.deltoideus CL
0,0
0,0
5,9
m.biceps brachii RA
1,2
2,3
m.triceps brachii UL
0,0
m.iliopsoas FE
P(χ2)
YA
MA
OA
N=67-84
N=76-89
N=92-101
0,006
1,3
2,3
5,0
0,330
7,2
0,075
0,0
3,5
4,1
0,207
3,6
6,5
0,080
0,0
3,9
10,9
0,010
1,2
6,8
15,0
0,003
4,8
4,5
12,0
0,079
quadriceps tendon PA
0,0
10,3
20,9
0,000
1,3
11,5
19,5
0,001
qudriceps tendon TI
2,5
8,0
12,1
0,062
2,6
9,4
13,1
0,046
m.soleus TI
2,5
2,3
7,1
0,176
2,5
3,4
4,0
0,844
Achilles tendon CA
4,3
16,9
32,3
0,000
4,3
19,0
38,7
0,000
Frequency of OL (1% - 2+3%)
Males - LEFT
70,0
PITTING (grade 1)
Males
EROSIONS (grade 2+3)
60,0
50,0
40,0
30,0
YA
20,0
MA
OA
pitting (OL 1) increases with
age
erosions (OL 2+3) decreases
with age (except m. biceps brachii)
soleus TI
biceps br. RA
lat.d./teres ma. HU
pectoralis m. HU
deltoideus CL
costoclav. CL
soleus TI
biceps br. RA
lat.d./teres ma. HU
pectoralis m. HU
deltoideus CL
0,0
costoclav. CL
10,0
significant differences among
age classes
Females - LEFT
30,0
PITTING (grade 1)
Females
EROSIONS (grade 2+3)
no significant differences
among age classes (except m.
25,0
20,0
biceps brachii)
15,0
YA
soleus TI
biceps br. RA
lat.d./teres ma. HU
pectoralis m. HU
deltoideus CL
costoclav. CL
soleus TI
biceps br. RA
0,0
lat.d./teres ma. HU
OA
pectoralis m. HU
5,0
deltoideus CL
MA
costoclav. CL
10,0
no age pattern
erosions more frequent in M
pitting more frequent in F
R Tibia
VCN t. 155 (Y)
R Humerus
Tf XXVII-2 (M?, Y)
R Humerus
Sardinia, ossuary
m. latissimus dorsii
/ teres major
m. soleus
EROSIONS
m. pectoralis major
Males
erosions
juvenile feature
pitting
elderly feature
bone metabolism changes through
time, bone response thus different?
PITTING
m. pectoralis major
L Humerus
SS 296 M, 62 y.
OCCUPATION
173 males with known occupation, performing 47 different jobs!
39% farmers, 5% masons …
Males with known occupation
YA
MA
OA
Tot
MALES
58
59
56
173
farmers
19
32
16
67
craftsmen
15
9
10
34
traders/
employees
13
3
7
23
other
11
15
23
49
Few significant
differences
between jobs
Concluding remarks 1
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
“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
But a hope remains …
1.
The study of homogeneous samples with respect
to the occupation gave interesting results (see
Milella et al. on porters and shoemakers TOMORROW!!!)
2.
The study of MSM and joint features in
individuals with altered patterns of locomotion
highlighted the influence of mechanical stress, in
agreement with medical data (Belcastro and Mariotti,
2000; Mariotti and Belcastro 2001)
Two Roman skeletons from
Casalecchio (Bologna, II-III AD)
3.
Our results are referred to only 23 entheses,
and maybe other entheses are more sensible to
mechanical stress
4.
We analised only the Sassari sample, but there
are many other known collections that can be
studied and that may give different results
Concluding remarks 3
Scoring method:
Record ROB, EF and OL separately: they do not behave in the same way
in relation to age
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 entheses
Consider 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)