47© 2019 The Anthropological Society of Nippon

IntroductionThe skull is the most studied anatomical element of the

skeleton because of its complexity and relationship with the brain, as well as with the masticatory and sensory organs (Scheuer and Black, 2000; White et al., 2011). In anthropol-ogy and osteoarchaeology, cranial vault thickness (CVT) is a remarkable metric variable, which refers to the distance be-tween the endocranial and ectocranial surfaces of the vault bones (Anzelmo et al., 2015; Eisová et al., 2016), and has been studied by many authors in different species and human groups, and in several biological contexts (e.g. Nawrocki, 1991; Gauld, 1996; Balzeau, 2013; Marsh, 2013). The CVT is thought to be determined by genetic factors and physio-logical responses to the environment, including hormones

and physical activity (Lieberman, 1996), diet, and climate (Endo, 1966; Baab et al., 2010; Menegaz et al., 2010; Gupta, 2016). It has also been related to other biological variables such as sex (Roche, 1953; Ross et al., 1998; Hatipoglu et al., 2008) and age (Roche, 1953; Young, 1957; Koenig et al., 1995; Anzelmo et al., 2015), although ontogenetic studies are still scarce. Finally, other authors have studied CVT in a clinical context in relation to surgical interventions (i.e. cra-nial bone harvesting) (Koenig et al., 1995; Elahi et al., 1997) and pathological conditions such as craniosynostosis and hydrocephalus (Anderson et al., 1970; Branson and Shroff, 2011).

Traditionally, anthropologists have used spreading calli-pers or radiographs to measure cranial thickness at specific anatomical landmarks (Todd, 1924; Roche, 1953; Ivanhoe, 1979; Nawrocki, 1991; Koenig et al., 1995; Lynnerup, 2001). Traditional callipers can be easily employed to meas-ure isolated bones and fragmented skulls, but they cannot be used with complete skulls, where the foramen magnum rep-resents the only access to the endocranial cavity. Some au-thors partially circumvented this problem by modifying cal-lipers or osteometric boards (Munizaga, 1962; Brown, 1987). However, as technologies developed, computed to-

AnthropologicAl Science Vol. 127(1), 47–54, 2019

Cranial vault thickness measurement and distribution: a study with a magnetic calliper

Irene del Olmo LiAneS1*, Emiliano Bruner2, Oscar CAmbrA-Moo1,3, María MolinA Moreno1, Armando González MArtín1,3

1Laboratorio de Poblaciones del Pasado (LAPP), Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, 28049 Madrid, Spain

2Programa de Paleobiología, Centro Nacional de Investigación sobre la Evolución Humana, 09002 Burgos, Spain3Grupo de Investigación en Arqueología Antigua y Medieval, Universidad de Oviedo, 33011 Oviedo, Spain

Received 2 October 2018; accepted 6 March 2019

Abstract Cranial vault thickness is a widely studied variable in physical anthropology. However, di-rect physical measurements are difficult to assess in complete skulls, where the endocranial surface is not easily accessible for standard callipers. Computed tomography represents the best alternative, but is expensive and not always available for many field or museum samples. In this study we present a meth-od for the measurement of cranial vault thickness based on magnetism. We measured bone thickness at 71 points of the vault in 30 human skulls with the use of a portable magnetic calliper, which offers a simple, direct, non-invasive, and cost-effective methodology. Magnetic measures were compared with physical measures sampled with a traditional spreading calliper, and error analysis was assessed. Thick-ness distribution was evaluated and represented in bidimensional maps after spatial interpolation. The two types of callipers provide the same results, suggesting that the magnetic calliper can be used in those situations in which a traditional calliper is not applicable. In accordance with previously published data, the most variable and thickest bones in our sample were the frontal and the occipital bones, and cranial vault thickness distribution follows a pattern of increasing thickness from lateral regions of the vault to the sagittal plane. The magnetic calliper is a reliable and effective tool to measure cranial thickness in those cases in which the endocranial surface is not easily accessible, and where expensive technology cannot be employed for economic or practical reasons.

Key words: skull, morphometrics, bone thickness, magnetic measurement

* Correspondence to: Irene del Olmo Lianes, Laboratorio de Pobla-ciones del Pasado, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, C/Darwin 2 (B-118), 28049 Ma-drid, Spain. E-mail: irene.delolmo@inv.uam.esPublished online 11 April 2019 in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.190306

I. DEL OLMO LIANES ET AL.48 AnthropologicAl Science

mography (CT) emerged, and nowadays is one of the most commonly used methodologies when investigating skull thickness. However, CT has a number of disadvantages, namely the high costs and the logistic difficulties, due to the limited possibility of moving samples and specimens to hos-pitals or radiographic centres. Other techniques use ultra-sound, and rely on equipment that is portable and relatively inexpensive (Elahi et al., 1997; Hakim et al., 1997). Howev-er, ultrasound devices require much work for sample prepa-ration, and require immersion of the bone in water. Moreo-ver, it has been much more often utilized to measure bone density rather than thickness (Wünsche et al., 2000; Gluër et al., 2004). Here we propose an alternative method based on magnetism that is simpler and quicker to apply than the aforementioned techniques. This methodology is derived from a magnetized instrument called the Hacklinger calliper, which was conceived with the aim of measuring wood thick-ness in the resonance box of string instruments such as vio-lins, as this is a factor that strongly influences sound quality (Bieber, 2008). Apart from the standard original version, this device can be easily handmade (Bieber, 2008), and digital versions are also available (Figure 1a). The main advantages of this instrument are its low cost compared with other tech-niques such as CT, its easy transport and use in situ, and the provision of direct and instantaneous measurement in a non-invasive way.

Although this methodology had previously only been ap-plied in a musical context by luthiers when making instru-ments, it can be easily employed in craniometrics, represent-ing a practical, specific solution to the methodological problem of CVT measurement of complete skulls. Here, we present a control study of the application of this magnetic calliper to bone thickness, and visualization maps of the distribution of cranial thickness in a modern human popula-tion.

Materials and MethodsA MAG-ic Probe V5.0 (MAG-ic Probe, Dallas) digital

magnetic calliper was used in this study. Its functioning is based on the force needed to separate two magnets, which is inversely proportional to the distance between them. The

equipment consists of a small and portable device that con-tains a measurement display screen and a sensor probe topped with a strong neodymium magnet (see Figure 1a). This magnet interacts with the accessory mobile magnet. In this case we made use of the spherical neodymium magnet accessory (measuring range/precision: 0–15.24 mm, instru-mental error: 0.1 mm) instead of the smaller cylindrical magnet because of its higher precision and easier mobility across the endocranial surface (see Figure 1b and c). This magnet is positioned on the endocranial surface, and the other on the corresponding ectocranial side, measuring the distance (thickness) between them. The instrument can be connected to a computer with a dedicated software, specifi-cally MAG-ic Probe PRO, which allows the compilation of data directly on an image that can later be used to create contour maps. Here we used the free version of the software, MAG-ic Probe Lite, to record measurements on a sampling points diagram (see Figure 2).

The study sample consisted of 30 normal adult human skulls, with no taphonomical or pathological alterations. These skeletal remains were selected from an osteological collection referred to as a medieval ossuary excavated in the Santa María de la Soledad church in Almansa (Castilla-La Mancha, Spain). This site was utilized as a cemetery from the 12th to 18th centuries and has been used for several in-vestigations, the results of which have been published else-where (Cambra-Moo et al., 2012, 2014; García Gil et al., 2016). Sex and age were not considered in this methodolog-ical survey.

Cranial vault thickness was measured at a total of 71 sam-pling points over the frontal, parietal, temporal, and occipital bones, and the cranial sutures, forming a deformable grid (Figure 2). These points were determined by taking traditional osteometric landmarks (i.e. nasion, bregma, pterion, lambda, asterion, inion, and ophistion) as reference, and their corre-sponding arcs: nasion–bregma, bregma–lambda, lambda– inion, lambda ophistion, bregma–left pterion, bregma–right pterion, lambda–left asterion, and lambda–right asterion (Buikstra and Ubelaker, 1994; White et al., 2011). In the case of the temporoparietal sutures, we chose to measure the pterion–asterion chords instead. All these cranial lengths were divided into halves, thirds, or quarters (depending on

Figure 1. Magnetic thickness calliper: (a) MAG-ic probe V5.0 (scale: 3 cm); (b) MAG-ic probe V5.0 calliper in use (scale: 3 cm); (c) detailed picture of MAG-ic probe V5.0 (scale: 3 cm).

SKULL THICKNESS AND MAGNETIC CALLIPER 49

the anatomy and size of each bone), in order to define inter-mediate equally spaced landmarks able to represent the cra-nial contours (see Figure 2 and Table 1) (Moreira-Gonzalez et al., 2006).

Each sampling point was measured three times and the mean value was used as the final figure. Statistics were com-puted with SPSS Statistics version 24.0 (IBM Corporation, Armonk). Error analysis was divided in two parts. On one hand, a cluster analysis based on Euclidean distances and paired average (UPGMA) was performed to evaluate the replicability of the method. For the UPGMA analysis, each thickness variable and individual were included and, addi-tionally, four individuals were randomly selected to replicate their measurements. Among these, individuals AL-CR8, AL-CR10, and AL-14307 were measured twice, while the individual AL-CR14191 was measured twice a day for three days, i.e. a total of six measurements. UPGMA was comput-ed with PAST 2.17c (Hammer et al., 2001). On the other hand, uncertainty was evaluated with a single thickness mean value for all the points and all the replicas in the UPGMA analysis and its standard deviation.

Ten fragmented adult skulls were selected from the same collection and five landmarks were chosen to compare the measurements taken with the magnetic calliper with meas-urements acquired with a traditional calliper: bregma, Pl3, Pl6, Pl9, and lambda. Bone thickness was measured twice on each point using the MAG-ic probe V5.0 and a standardized spreading calliper, respectively. Values were compared us-ing an intraclass correlation test (two-way mixed, absolute agreement), a paired-samples t-test, and Wilcoxon’s test (P = 0.01). The intraclass correlation test was used in order to see the concordance between measurements of both meth-ods, whereas the paired-samples t-test and the Wilcoxon test

Figure 2. Bidimensional skull diagram in superior view. Sampling points are represented in red and indicated by a number in purple which denotes the order of their measurement as shown in Table 1. Cranio-metric reference points are represented in red and surrounded by a red circle. Cranial sutures are represented by discontinuous blue lines and green lines reflect the lines traced to get sampling points, apart from those of the sutures. Color figure can be viewed in electronic form.

Table 1. Sampling points

1. N Nasion2. N-B1, 3. N-B2 Nasion–bregma arc sampling points4. B Bregma5. B-L1, 6. B-L2, 7. B-L3 Bregma–lambda arc sampling points8. L Lambda9. L-I Lambda–inion arc sampling point

10. L-OP Lambda–ophistion arc sampling point11. I Inion12. LPT Left pterion13. PT-ASl1, 14. PT-ASl2, 15. PT-ASl3 Pterion–asterion left chord sampling points16. LAS Left asterion17. B-PTl1, 18. B-PTl2, 19. B-PTl3 Bregma–pterion left arc sampling points20. F1, 21. F2, 22. F3, 23. F4, 24. F5, 25. F6 Left side frontal sampling points26. LP1, 27. LP2, 28. LP3, 29. LP4, 30. LP5, 31. LP6, 32. LP7, 33. LP8, 34. LP9 Left parietal sampling points35. L-ASl1, 36. L-ASl2, 37. L-ASl3 Lambda–asterion left arc sampling points38. O1, 39. O2, 40. O3, 41. O4 Left side occipital sampling points42. RPT Right pterion43. PT-ASr1, 44. PT-ASr2, 45. PT-ASr3 Pterion–asterion right chord sampling points46. RAS Right asterion47. B-PTr1, 48. B-PTr2, 49. B-PTr3 Bregma–pterion right arc sampling points50. F7, 51. F8, 52. F9, 53. F10, 54. F11, 55. F12 Right side frontal sampling points56. RP1, 57. RP2, 58. RP3, 59. RP4, 60. RP5, 61. RP6, 62. RP7, 63. RP8, 64. RP9 Right parietal sampling points65. L-ASr1, 66. L-ASr2, 67. L-ASr3 Lambda–asterion right arc sampling points68. O5, 69. O6, 70. O7, 71. O8 Right side occipital sampling points

Vol. 127, 2019

I. DEL OLMO LIANES ET AL.50 AnthropologicAl Science

were used to check if measurements were equal or not. The values of the cranial vault thickness obtained by using the magnetic calliper were compared with those in previous studies focused on the normal and non-deformed/non- pathological cranium in order to show the normality of measurements.

CVT distribution maps for thickness mean and standard deviation were computed on the skull bidimensional dia-gram through Kriging interpolation (Olea, 1974). Maps were created with Surfer®13 (Golden Software LLC, Gold-en, CO).

ResultsTable 2 shows the comparison between traditional and

magnetic callipers. The paired-samples t-test and the Wil-coxon test results show no significant differences between the magnetic and the standard calliper mean values, and the correlation between the two values is very high (ICC ≥ 0.97). UPGMA after repeated measures shows that replicated indi-viduals cluster together, suggesting sufficient reliability on the replicability of the method (Figure 3). As for the uncer-tainty measure, we obtained a thickness mean value of 6.51

Table 2. Comparison of physical calliper and magnetic calliper measurements

Statistics Method Bregma LP3 LP6 LP9 LambdaMean Physical 7.0 6.5 7.7 7.6 7.2

Magnetic 7.0 6.5 7.6 7.5 7.3Standard deviation Physical 1.2 0.9 1.2 1.2 1.9

Magnetic 1.1 0.9 1.2 1.1 1.7Median Physical 7.3 6.5 7.5 7.5 7.3

Magnetic 7.2 6.3 7.5 7.5 7.4Minimum Physical 4.5 5.5 6.0 5.5 4.5

Magnetic 4.6 5.2 5.5 5.8 4.6Maximum Physical 8.5 8.0 10.0 9.5 10.2

Magnetic 8.2 8.0 9.8 9.6 10.2Intraclass correlation test ICC = 0.98 ICC = 0.97 ICC = 0.99 ICC = 0.98 ICC = 0.99

95% CI: 0.926–0.995

95% CI: 0.885–0.993

95% CI: 0.951–0.997

95% CI: 0.925–0.995

95% CI: 0.960–0.997

F = 49.32 F = 31.87 F = 76.01 F = 48.38 F = 90.66p = 0.0001 p = 0.0001 p = 0.0001 p = 0.0001 p = 0.0001

Student’s t-test t = –0.325 t = 0.020 t = 0.903 t = 0.313 t = –0.646df = 9 df = 9 df = 9 df = 9 df = 9

p = 0.753 p = 0.984 p = 0.390 p = 0.761 p = 0.534Wilcoxon test z = –0.306 z = –0.357 z = –0.918 z = –0.255 z = –0.770

p = 0.760 p = 0.721 p = 0.359 p = 0.799 p = 0.441

Figure 3. UPGMA cluster analysis. Resulting replicas are grouped in boxes.

SKULL THICKNESS AND MAGNETIC CALLIPER 51

Tabl

e 3.

D

escr

iptiv

e re

sults

NN

-B1

N-B

2B

B-L

1B

-L2

B-L

3L

L-I

L-O

PI

LPT

PT-

ASl

1PT

-A

Sl2

PT-

ASl

3LA

SB

-PTl

1B

-PTl

2B

-PTl

3F1

F2F3

F4F5

N30

3030

3030

3030

3030

3030

2930

3030

3030

3030

3030

2930

30M

in.

8.5

5.4

3.3

5.2

4.6

4.1

4.0

4.5

4.9

3.9

6.7

2.5

1.3

1.1

4.0

2.9

3.3

4.5

5.3

4.8

2.2

3.3

3.2

3.9

Max

.15

.212

.510

.79.

69.

311

.110

.110

.412

.015

.215

.25.

96.

94.

78.

08.

18.

711

.39.

815

.28.

47.

811

.711

.0M

ean

13.5

8.3

7.2

7.1

6.7

7.4

6.8

6.7

8.1

8.4

12.0

4.0

4.2

2.4

6.1

5.9

5.5

6.8

6.9

9.5

4.8

5.7

6.8

6.2

SD2.

01.

71.

51.

11.

31.

61.

61.

51.

92.

82.

70.

81.

40.

81.

01.

21.

41.

61.

02.

51.

41.

42.

11.

7

F6LP

1LP

2LP

3LP

4LP

5LP

6LP

7LP

8LP

9L-

ASl

1L-

ASl

2L-

ASl

3O

1O

2O

3O

4R

PTPT

-A

Sr1

PT-

ASr

2PT

-A

Sr3

RA

SB

-PTr

1B

-PTr

2

N30

2930

3029

2930

3030

3030

3030

3030

3030

3030

3030

3030

30M

in.

4.3

2.8

3.8

4.5

3.2

3.6

4.8

3.0

4.4

4.7

3.4

4.6

4.5

3.1

3.3

3.9

2.7

2.3

1.9

1.5

4.5

3.8

3.6

4.8

Max

.9.

97.

88.

310

.16.

19.

612

.07.

89.

911

.38.

89.

210

.07.

811

.48.

310

.15.

95.

24.

39.

39.

17.

810

.0M

ean

7.0

4.6

6.2

6.5

4.6

6.4

7.8

4.6

6.5

7.2

5.1

6.4

6.7

5.5

7.2

5.6

6.5

4.1

3.2

2.5

6.7

5.8

5.2

6.7

SD1.

61.

11.

21.

40.

91.

41.

71.

11.

41.

51.

31.

11.

51.

01.

81.

21.

70.

80.

90.

71.

21.

31.

21.

4

B-P

Tr3

F7F8

F9F1

0F1

1F1

2R

P1R

P2R

P3R

P4R

P5R

P6R

P7R

P8R

P9L-

ASr

1L-

ASr

2L-

ASr

3O

5O

6O

7O

8

N30

2930

3030

3030

2930

3029

2930

2930

3030

3030

3030

3030

Min

.4.

74.

91.

33.

53.

63.

74.

03.

34.

35.

02.

73.

85.

23.

24.

54.

43.

24.

54.

23.

94.

34.

03.

8M

ax.

10.0

13.4

6.9

8.9

11.3

9.5

9.9

6.9

8.5

9.9

7.4

9.5

10.4

5.8

9.6

10.7

8.3

8.7

9.0

9.3

10.8

8.1

10.0

Mea

n7.

19.

54.

45.

66.

65.

97.

14.

56.

46.

74.

26.

17.

64.

46.

17.

15.

16.

56.

56.

08.

05.

57.

3SD

1.2

2.0

1.4

1.3

1.8

1.6

1.6

1.0

1.2

1.3

1.0

1.4

1.5

0.7

1.2

1.6

1.2

1.1

1.4

1.3

1.8

1.1

1.7

Vol. 127, 2019

I. DEL OLMO LIANES ET AL.52 AnthropologicAl Science

(SD = 0.85). Descriptive results of all variables are included in Table 3. Table 4 shows descriptive results per bone; vari-ation is represented by the standard deviation (SD), median and P25 and P75 quartiles, and the coefficient of variation (SD/mean). The occipital bone has the highest mean thick-ness value, followed by the frontal, parietal, and temporal bones, respectively. The occipital and frontal bones also display a larger degree of variation, while the temporal bones are the least variable.

The spatial distribution of the bone thickness is represent-ed as interpolated contour maps in Figure 4. The areas with the highest mean thickness values (colored in red) are the nasion and inion and adjacent areas in the frontal and occip-ital bones, respectively. The lower values (colored in violet) are located within the squama of the temporal bones. Thick-ness of the lateral regions of the vault is generally lower than the thickness of the sagittal plane, displaying an organiza-tional pattern. The distribution of the SD values shows re-gions of high and low variation, with the occipital and fron-tal bones again being the most variable regions, along with

the region surrounding the centre of the sagittal suture; and the temporal bones the least variable ones, as reflected in Table 4.

DiscussionCVT has been approached in many different ways be-

cause it has always posed a challenge in anthropological re-search. Hence, the principal aim of this paper was to intro-duce a new thickness measuring methodology that allows researchers to study dry complete skulls without the necessi-ty of imaging methods. The electronic version of the Hack-linger magnetic calliper, originally created for string instru-ments, represents a very useful tool specifically when applied to craniology. The equipment is portable and the method is non-invasive and cheap, and applicable in many different circumstances. The results of the magnetic calliper are similar to the results obtained with the traditional device, and the error analysis proves the replicability of the method and an acceptable uncertainty value when using the MAG-ic probe V5.0; however, it should be emphasized that measure-ment errors are based on mean data of three times repeated measuring. Anatomical expertise and experience is, anyway, necessary to properly handle the position of the magnets through the corresponding ectocranial and endocranial sur-faces.

In general, studies on cranial thickness report similar re-sults, including when using different methodologies (Marsh, 2013; Anzelmo et al., 2015) or working on different geo-graphic populations (e.g. Smith et al., 1985). The occipital bone is the thickest and most variable bone followed by the frontal, as demonstrated by previous analyses (Marsh,

Table 4. Mean, standard deviation (SD), coefficient of variation (CV) and quartiles per bone (mm)

Mean SD CV (%) P25 quartile MedianP75

quartileFrontal 7.2 2.7 37.7 5.4 6.7 8.4Left parietal 6.0 1.7 28.3 4.8 5.9 7.0Right parietal 5.9 1.7 28.6 4.7 5.7 6.8Left temporal 3.3 1.4 43.3 2.3 2.8 4.6Right temporal 2.8 0.9 29.8 2.2 2.8 3.4Occipital 7.3 2.6 35.2 5.4 6.7 8.4

Figure 4. Mean and standard deviation (SD) thickness distributions represented on contour maps. The color scale represents thickness values in mm. Color figure can be viewed in electronic form.

SKULL THICKNESS AND MAGNETIC CALLIPER 53

2013). Moreira-Gonzalez et al. (2006) found an average thickness for the frontal bone of 6.65–7.24 mm and about 5.5 mm for the occipital bone (measured at two locations). These results are similar to those presented in this study, al-though in our case ranges were wider and values were con-siderably higher for the occipital bone. The large variation in frontal and occipital bones is due to the heterogeneous anat-omy of these regions, which include flat squamas, sinuses, and muscular insertions (White et al., 2011). Parietal bones, as reflected in other studies, are more uniform (Anzelmo et al., 2015). Moreira-Gonzalez et al. (2006) report the mean thickness values of the parietals as between 5.3 and 7.0 mm, which is a very similar range to the one found in the present study, though ours is wider and considers both parietals. Temporal bones turned out to be the least variable bones, although only two points were measured on each temporal, and these bones are not usually considered in CVT studies. The analysis of CVT distribution shows an organizational pattern in which thickness increases from the lateral regions of the vault to the sagittal plane. This tendency has also been found in other modern studies (Marsh, 2013; Anzelmo et al., 2015). In light of these results, more exhaustive studies on the organization and distribution of CVT, taking into ac-count factors such as asymmetry, should be included in our future work.

In conclusion, the methodology based on magnetism pre-sented in this study has proven to be accurate and appropri-ate for measuring the CVT of skeletal remains. The Hack-linger calliper is an appropriate and useful device to measure cranial thickness in complete dry skulls, and should be con-sidered for use in future anthropometrical studies.

AcknowledgmentsThis research was supported by the Spanish Govern-

ment (CGL2015-65387-C3-3-P, MAT2013-48426-C2-1-R, CGL2015-68363-P, HAR2016-78036-P, HAR2016-74846- P, HAR2017-82755-P, HAR2017-83004-P).

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