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 attivit. PhD thesis, Universit 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) Enthsopathies et activits des hommes prhistoriques. Recherche mthodologique et
application aux fossiles europens du Palolithique suprieur et du Msolithique. Thse de Doctorat,
Universit 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 usageseen 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

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%

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)

nr more than 50% of the area is

illegible

Attention !!!

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

costoclavicular lig.

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 (2)
- 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.

YA

MA

OA

YA

MA

OA

N=59-75

N=51-63

N=50-61

N=61-75

N=70-82

N=86-96

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

YA
M

upper limb

1,36

shoulder

MA
M

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

OA

0,021

0,031

M>F or F>M

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(2)

Males

P(2)

0,000

0,000

LEFT

P(2)

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(2)

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

10

34

traders/
employees

13

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)