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Brief communication УPathologicalФ deformation in the skull of LB1 the type specimen of Homo floresiensis.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:177–185 (2009)
Brief Communication: ‘‘Pathological’’ Deformation in the
Skull of LB1, the Type Specimen of Homo floresiensis
Yousuke Kaifu,1,2* Hisao Baba,1 Iwan Kurniawan,3 Thomas Sutikna,4 E. Wahyu Saptomo,4
Jatmiko,4 Rokhus Due Awe,4 Tsuyoshi Kaneko,5 Fachroel Aziz,3 and Tony Djubiantono4
1
Department of Anthropology, National Museum of Nature and Science, Tokyo 169-0073, Japan
Department of Biological Sciences, The University of Tokyo, Tokyo 113-0033, Japan
3
Geological Museum, Geological Survey Institute, Bandung 40122, Indonesia
4
The National Research and Development Centre for Archaeology, Jakarta 12510, Indonesia
5
Department of Plastic and Reconstructive Surgery, National Center for Child Health and Development,
Tokyo 157-8535, Japan
2
KEY WORDS
deformational plagiocephaly; LB1; Liang Bua; Flores
ABSTRACT
If the holotype of Homo floresiensis,
LB1, suffered from a severe developmental pathology,
this could undermine its status as the holotype of a new
species. One of the proposed pathological indicators that
still remains untested is asymmetric distortion in the
skull of LB1 (Jacob et al.: Proc Natl Acad Sci USA 103
(2006) 13421–13426). Here, we present evidence that
LB1 exhibits antemortem craniofacial deformities that
are consistent with posterior deformational (positional)
plagiocephaly. This is a relatively common condition in
modern people with no serious associated health problems and does not represent a severe developmental
abnormality in LB1. Am J Phys Anthropol 140:177–185,
2009. V 2009 Wiley-Liss, Inc.
The excavation of a skeleton (LB1) and other remains
of diminutive hominids at Liang Bua, a limestone cave
on Flores in East Indonesia led to an extended debate
about their taxonomic status; specifically, whether they
represent a new species, Homo floresiensis, as claimed
by the discoverers (Brown et al., 2004; Morwood et al.,
2004, 2005), or whether they are pathological H. sapiens.
Some researchers have suggested that the tiny brain,
short stature, and other skeletal features of LB1 result
from microcephaly and/or a severe genetic growth disturbance such as Laron Syndrome (LS) or cretinism
(Martin et al., 2006; Richards, 2006; Hershkovitz et al.,
2007; Obendorf et al., 2008). However, these claims are
based primarily on the published descriptions and
released images and misrepresent some important characteristics of LB1 (see Larson et al., 2007b; Falk et al.,
2008; Dalton, 2008; Culotta, 2008), nor have such critics
been able to produce a microcephalic, LS, or cretinous
patient who exhibits the same mosaic of morphological
traits evident in LB1 (Brown et al., 2004; Argue et al.,
2006; Falk et al., 2007, 2008; Larson et al., 2007a).
In contrast, Jacob et al. (2006) studied the original
LB1 skeleton and noted unusual morphological asymmetries that they attributed to unspecified, but severe, developmental anomalies. Whereas further studies of the
remains showed that the reported postcranial asymmetries were exaggerated (Jungers et al., in press; Larson
et al., in press), the cranium of LB1 has turned out to be
‘‘fairly asymmetrical’’ from 3D morphometric analyses
(Baab and McNulty, in press). Although Baab and
McNulty (in press) concluded that the degree of cranial
asymmetry in LB1 was moderate and readily explained
by the taphonomic processes that occur after death, our
examination of the original specimen strongly suggests
that the majority of the cranial asymmetries were present before the individual’s death. In this article, we
describe and diagnose the cranial asymmetries observed
in LB1. The asymmetric deformation extends into the
cranium, face, mandible, and even dental occlusion of
LB1, but the condition does not represent a severe developmental abnormality.
C 2009
V
WILEY-LISS, INC.
C
MATERIALS AND METHODS
We examined the original specimen in September 2007
and March 2008 at the National Research and Development Centre of Archaeology in Jakarta. The skull surface was cleaned and the reconstruction of the left mandibular corpus corrected at the crack below P1. The right
mandibular ramus/corpus was also found to be slightly
misaligned—it was dislocated superiorly and laterally
(10 mm and 5 mm at the condyle, respectively)—but
the nature of the adhesive that was used to join the
right corpus below P1 and M3 meant that this problem
could not be remedied. These uncorrected distortions do
not significantly affect the following morphological
description.
However, the cranium and mandible of LB1 do not
articulate or occlude perfectly, mainly because of the
aforementioned misalignment in the right mandibular
corpus and the slight dislocation of some teeth. To examine the dental occlusion of LB1, plaster casts of its dentiGrant sponsor: National Museum of Nature and Science, Tokyo.
*Correspondence to: Yousuke Kaifu, Department of Anthropology,
National Museum of Nature and Science, 3-23-1 Hyakunincho,
Shinjuku-ku, Tokyo 169-0073, Japan. E-mail: kaifu@kahaku.go.jp
Received 29 October 2008; accepted 10 February 2009
DOI 10.1002/ajpa.21066
Published online 8 April 2009 in Wiley InterScience
(www.interscience.wiley.com).
178
Y. KAIFU ET AL.
tions were prepared following the methods described in
Kaifu (2007). Silicone molds were made by the authors
separately for the right and left maxillary tooth rows
(C1–M2), the right and left mandibular anterior sections
(I1–P1 and I2–P1), and the right and left mandibular
molar rows of LB1. The accuracy of these casts was less
than 0.1 mm for each group of teeth.
The dislocated teeth (left M2 and each mandibular
molar) were sawn off of the casts and then put back in
their original positions by fitting interproximal and occlusal facets between adjacent and opposing teeth.
Putty-type silicone was used as stabilizer for this castbased reconstruction. The left P1, which protruded
slightly from the occlusal plane, was not corrected but
this did not affect our occlusal reconstruction. After centric occlusion (the occlusal position with the maximal
intercuspation) between opposing maxillary and mandibular elements had been determined, the final alignment
of the dental arches and their occlusal relationships
were reconstructed using the maxillary dentition as a
guide. This was because almost the whole palate had
retained the original maxillary arch, while the mandibular arch was distorted, particularly on its right side as
described earlier. The centric occlusion thus reconstructed was then schematized by modifying the occlusal
photographs of the dentitions using Adobe Photoshop.
To observe sutural and endocranial morphology, we
examined the CT images of LB1 prepared by Brown
et al. (2004). The parameters of the scan included a 512
3 512 matrix, 2-mm collimation, 1-mm reconstruction
interval, and a H70s reconstruction kernel. Several
ectocranial and endocranial measurements were taken
from 3D surface renderings of the CT data produced by
Analyze 6.0 (Mayo Clinic). The endocranial angle measurements were taken directly on a rendering image projected onto the Frankfurt Horizontal. Ectocranial linear
measurements were taken to examine morphological
asymmetries in the form of the ratio between the right
and left sides. These distances were calculated based on
the 3D coordinates of the landmarks, which were
recorded on the 3D rendering images. The measurement
was repeated twice by Y.K., and the means of both trials
were used for the following comparisons. The two trials
of the endocranial angle measurements were identical
and had a maximum discrepancy of 0.58. The discrepancies in the ratios of the linear measurement were also
small enough to not significantly affect the analytical
results (see notes of Table 2).
DESCRIPTION OF CRANIAL ASYMMETRIES
Jacob et al. (2006) argued that asymmetries are evident in the lower orbital border of LB1, and the location
of the nasal spine, the expression of the canine juga,
maxillary body rotation, left occipital flattening, nuchal
torus, and the mastoid regions. Our study confirmed
that such cranial asymmetries are present in LB1 and
that there are also other cranio-mandibular deformations, which are important for our diagnosis.
Skull deformations can be caused by many factors.
Postmortem distortion can be caused by postdepositional
earth pressure or during the postexcavation preparation
or treatment of the specimen, whereas antemortem factors include pathology and artificial deformation (deliberate or accidental). A degree of nonpathological asymmetry in the body is also common in healthy individuals.
American Journal of Physical Anthropology
Our study was able to identify the specific factors responsible for the deformities seen in the LB1 skull.
For instance, LB1 exhibits facial asymmetries that
cannot be explained by postmortem deformation. These
include asymmetric development of the maxillary canine
and P1 juga; a horizontally deviated or flexed palate midline at the interpalatal suture (maxillary body rotation);
shape and positional asymmetries in the mandibular
ramus; and importantly, disharmonic occlusion (E.
Indriati, pers. comm.), as described below.
We confirmed that the maxillary body rotation relative
to the cranial midline is slightly more pronounced (68)
than was reported by Jacob et al. (2006): 4–58. This is
evident from the horizontally flexed course of the interpalatal suture (Fig. 1C). There were no obvious signs of
postmortem deformations or fractures in the surrounding bony structures including the fragile palatines,
vomer, and pterygoid plates, indicating that the horizontal flexion was present during the individual’s life. Interestingly, the incisive canal is oriented in the same direction as the anteroposterior axis of the cranial vault as
opposed to the interpalatal suture (Fig. 1C). We infer
from this that the asymmetric development of the canine
and P1 juga (Fig. 1D) was produced by the rotation of
the maxillary dental arch, which also drove the rotation
of the maxillary body (see below).
In the lateral view (Fig. 1F), the left mandibular ramus
joins the corpus at a more anterior position (below M2)
than on the right side (M2/M3). The horizontal position of
the lateral prominence also exhibits side difference,
accordingly (Fig 1E). The left ramus is broad in its lower
part, but narrow in the upper part. The posterior borders
of the rami and the shape and height of the coronoid processes are also markedly asymmetric (Fig. 1F).
Figure 2 shows the occlusal relationship between the
maxillary and mandibular dentitions of LB1, which were
reconstructed based on our examination of the casts. In
the molar region, the occlusal relationship was reliably
reconstructed based on the wear caused by opposing
teeth. The entire occlusal surfaces have been worn flat
on the left molars, and each left maxillary and mandibular molar has been directly occluded. In contrast, the lingual and buccal portions of the right mandibular and
maxillary molars, respectively, remain unworn, due to
the alternate occlusal relationship on this side. The occlusal position thus reconstructed from the molar wear
(see Fig. 2) is consistent with the wear pattern exhibited
by the canines and premolars. The anteroposteriorly
undulating wear on these teeth indicates that the left
maxillary canine occluded anteriorly to the opposing left
mandibular canine in contrast to the right side where
both canines occluded almost directly (see Fig. 3).
Despite complications caused by the rotated P2s and
the congenitally absent right P2 that might have invited
right molar mesial drift, aberrance was apparent in the
anteroposterior occlusal relationship: The left molars
show a Class II relationship (the mandibular teeth are
in a distal relationship with their normal maxillary
opponents), whereas the right molars show a Class III
relationship (the mandibular teeth are in a mesial relationship with their normal maxillary opponents). Henneberg noted that the ‘‘teeth (of LB1) on the right side
were more worn than teeth on the left side,’’ and suggested that this asymmetric wear pattern was caused by
asymmetric chewing muscle forces which, according to
him, resulted from asymmetric brain growth in LB1
(Henneberg and Schofield, 2008, p 45). Contrary to this
PLAGIOCEPHALY IN HOMO FLORESIENSIS
179
Fig. 1. The skull of LB1
shows deformation as described
in the text. A: Frontal view.
Note the lateral skewing of the
mandible with its dental arch
and base shifted toward the
specimen’s left relative to the
condyles. B: Superior view vertical to the Frankfurt Horizontal. A line passing through the
deepest points of the right and
left temporal fossae is indicated.
C: Basal view. A line passing
through the right and left postglenoid processes of the mandibular fossae and one running
along the midline of the maxillary body are indicated. D: Diagonal superior view. Note the
strong development of the right
canine and P1 juga and the
anteriorly located left anterior
malar surface. E: Superior view
of the mandible. lp, lateral
prominence. F: Lateral views of
the right (right side) and left
(left side) mandibular rami (vertical to the external ramal surfaces). Scale bar, 2 cm.
interpretation, we can state that the asymmetric wear
seen in LB1 was as a result of the horizontally twisted
occlusion as shown by the aforementioned occlusal reconstruction.
In addition, viewed from above or below, LB1’s cranium shows ‘‘parallelogram’’ skewing with distinct left
occipital flattening and a slight anterior shift of the left
face, as exemplified by the asymmetric dispositions of
the mandibular fossae, external ear canals, temporal fossae, and anterior malar surfaces (Fig. 1B–D). In combination, this skewing and the maxillary body rotation has
caused the leftward shift of the maxillary dentition relaAmerican Journal of Physical Anthropology
180
Y. KAIFU ET AL.
Fig. 2. Photographic reconstruction of the disharmonic occlusal relationship. A horizontally flipped image of the maxillary
dentition (blue) is superimposed onto the mandibular dentition
(white) in the position of centric occlusion. The left maxillary
third molar (M3) and left mandibular second premolar (P2) were
lost after death (~), while the right P2 was congenitally absent
(~).
tive to the center of both mandibular fossae (Fig. 1C).
The mandibular dentition has also been shifted to the
left relative to the condyles by the lateral skewing of the
entire mandible (Fig. 1A,E).
Such overall skewing of a bone is often produced by
postdepositional earth pressure, but there are some reasons to suspect otherwise in this case. First, as the cranium was unearthed with its vertex up, the presence of
ground pressure exerted diagonally from the left occipital bone is unlikely. Second, the concordant lateral distortion of the cranium and mandible suggests that they
were articulated when the distortion occurred (Fig. 1A).
As these were excavated side by side in a completely disarticulated condition with the mandible upside-down,
the aforementioned deformation probably occurred during the individual’s life. Further support for the lack of
significant postmortem deformation in the LB1 skull is
demonstrated by the completeness of other fragile elements such as the scapula, pelvis, fibula, and the face
and base of the skull itself.
From the aforementioned observations, most or all of
the craniofacial deformities described earlier were present during the life of LB1. As asymmetric craniofacial
deformities are not typically seen in a skull with intentional artificial deformation, the aforementioned asymmetric deformities are likely to have been caused by
some pathological or abnormal condition.
Another marked deformity in the skull of LB1 is the
medially depressed right zygomatic arch (Brown et al.,
2004). Whether this was present during the individual’s
life is unclear.
DIAGNOSIS
Several forms of hemihyperplasia and hemihypoplasia
cause craniofacial asymmetry [e.g., unilateral overgrowth or undergrowth at the mandibular condyle or
American Journal of Physical Anthropology
Fig. 3. The buccal sides of the dentition showing the occlusal relationships of the right (upper) and left (lower) canines
and first premolars (plaster casts).
hemifacial microsomia (Cohen, 1995)], but the major distortion in the LB1 skull is skewing rather than cubical
dilatation/restriction. Also, LB1 does not exhibit signs of
infection, trauma, or ankylosis in its temporomandibular
joints (Bishara et al., 1994; Cohen, 1995).
Two well-known etiologies of an obliquely deformed
head (plagiocephaly) are the abnormal early closure of
sutures (craniosynostosis) and deformational plagiocephaly (DP). Unicoronal synostosis (UCS) and unilamboid
synostosis (ULS) both cause pronounced craniofacial
asymmetry. Although the details of the sutural morphology of LB1 are not visible in the available CT images,
LB1 lacks some of the key diagnostic features of synostosis (Kane et al., 1996; Lo et al., 1996; Huang et al., 1996;
Mulliken et al., 1999; Captier et al., 2003; Ehret et al.,
2004; Netherway et al., 2006). Such features include a
trapezoid head shape and strong horizontal flexion of the
cranial base midline in both UCS and ULS; overt asymmetry in the anterior and a largely unaffected posterior
cranium in UCS; and a compressed occipital with occipitomastoid bossing on the affected side, marked expansion of the unaffected side of the posterior cranium, a
laterally tilted cranial base, a symmetric anterior cranium (variable), and posteriorly displaced external ear
canal on the affected side (variable) in ULS. Some of
these differences are metrically indicated in Table 1. For
example, the crista galli-sella-opisthion (CSO) angle
(Captier et al., 2003) of LB1 was 180.58 on the affected
(occipital flat) side. This is outside of the range of variation for UCS. Furthermore, a thick bony ridge formed
frequently over the fused suture in a synostotic patient
(Wood and Shell, 2005) is absent in LB1.
However, the ‘‘parallelogram’’ skewing seen in LB1 is
a typical symptom of posterior deformational plagiocephaly (PDP) (Lo et al., 1996; Huang et al., 1996; Mulliken et al., 1999; Persing et al., 2003). Figure 4 shows a
typical case of PDP in a modern infant. PDP is a frequently encountered form of deformational plagiocephaly
181
PLAGIOCEPHALY IN HOMO FLORESIENSIS
TABLE 1. Comparisons of the cranial fossa angles among LB1 and children with UCS, ULS, and PDP
b
Measurement
CSO angle
Occipital flat sidec
Occipital bossing side
CSX angle
Occipital flat side
Occipital bossing side
XSM angle
Occipital flat side
Occipital bossing side
MSO angle
Occipital flat side
Occipital bossing side
UCS
ULSb
PDP
N 5 18 Mean (range)
N 5 2 Mean
N 5 22 Mean (range)
167 (158–175)
194 (185–202)
54 (45–64)
71 (61–82)
69 (59–79)
79 (70–89)
43 (38–48)
43 (36–50)
(Strongly flexed)
172
189
(Essentially symmetrical)
–
–
(Minor asymmetry)
–
–
(Expansion of bossing side)
–
–
181 (174–187)
179 (173–186)
a
LB1
180.5
179.5
65 (56–75)
64 (55–72)
51–58d
58–65d
70 (59–81)
69 (58–81)
80–85d
74–82d
46 (39–53)
46 (40–53)
44.5
40
C, anterior crista galli; M, internal acoustic metus; O, opisthion; S, sella; X, xiphoid of the lesser wing of the sphenoid.
a
Comparative metric data from Captier et al. (2003). The ranges in parentheses were calculated as mean 6 2SD.
b
Data not presented in Captier et al. (2003) except for the means of the CSO angle. Descriptions by Lo et al. (1996) are within
parentheses.
c
‘‘Occipital flat side’’ in UCS and ULS refer to the synostotic side.
d
A possible range is presented due to an unclear X point on the available CT images of LB1.
Fig. 4. A deformed head of a present-day, 8.5-month-old
infant with PDP.
(DP), which refers to an asymmetrical cranium caused
by repeated pressure to the same area of the head. Overt
cranial asymmetry caused by PDP often develops secondarily after birth by forces exerted on the posterior cranium. Minor unilateral occipital flattening from compressive forces in utero and/or at birth can be accentuated by
postnatal sleeping posture if an infant is habitually
placed supinely on a flat surface and rests his/her head
on the flattened area of the skull (Mulliken et al., 1999;
St. John et al., 2002; Peitsch et al., 2002; Hutchison et
al., 2003, 2004). This explains the recent dramatic
increase in the incidence of PDP in America, which
occurred after the 1992 recommendation by the American Academy of Pediatrics that an infant should sleep on
its back to reduce the risk of sudden infant death syndrome (Argenta et al., 1996; Turk et al., 1996; Lo et al.,
1996; Huang et al., 1996; see also Boere-Boonekamp and
van der Linden-Kuiper, 2001 for a case in the Netherlands; Persing et al., 2003).
The cranial shape in PDP varies to some extent
according to position, period, strength of the pressure,
etc., but there are some common morphological features
associated with this condition (Lo et al., 1996; Captier
et al., 2003; Netherway et al., 2006). PDP shows minimal or no horizontal flexion in the cranial base midline
and the posterior, middle, and sometimes anterior cranial fossae are shifted anteriorly on the affected side,
but their volumes do not change significantly between
the affected and unaffected sides. These are reflected in
the measurements in Table 1. LB1 is well within the
variation range of PDP in these respects.
Almost all the aforementioned cited modern plagiocephaly reference data are from infants, but we assume
that they can be reasonably compared with the adult
cranium of LB1. There seems to be no significant ‘‘selfcorrection’’ of PDP during childhood, and cranial deformities present at the late infant stage seem to be
maintained throughout adulthood (Argenta et al., 1996;
Mulliken et al., 1999; Persing et al., 2003). Simple repositioning of a sleeping child’s head (either by him/herself
or by a caretaker) or molding helmet therapy are often
effective when the child is 8 months or younger. In most
cases, correcting head shape in PDP children older than
1–2 years requires surgery (Wood and Shell, 2005). Longitudinal follow-up studies are rare, but one such
attempt based on a small sample led Danby (1962) to
conclude that plagiocephaly persists from infancy into
adolescence. This author reported the presence of plagiocephaly in 19 of 21 children (8–11.5-years old) in whom
plagiocephaly had been observed in early infancy (among
the two ‘‘nonplagiocephalic’’ cases, one showed unilateral
frontal asymmetry and the other was not asymmetric in
the vertex view radiograph). There is no information
about the correlation of the type of plagiocephaly (e.g.,
left posterior, right frontal, etc.) between the infancy and
childhood, but the author found some association
between the fetal head position before and at birth and
the type of plagiocephaly at 10-years old. Furthermore,
examples of permanent retention of the infant’s altered
American Journal of Physical Anthropology
182
Y. KAIFU ET AL.
TABLE 2. Relative percentage differences between the ipsilateral
and contralateral measurementsa
Modern
infants
with PDPc
Cranium
Anterior nasal spine—porion
Orbitale-porion
Frontomalare orbitale—porion
Jugale (zygotemporale)—porion
Mandible
Condylion lateral—gonion
Coronoid tip—condylion laterale
Coronoid tip—gonion
LB1b mean
SD
LB1d
23.6
24.7
24.0
20.3
27.4
25.5
21.9
23.3
3.94
4.40
3.57
4.77
25.5
28.6
2.3
0.7
25.9
1.0
6.05 \2 SD
5.09 \1 SD*
3.62 \1 SD
\1
\1
\1
\1
SD*
SD
SD
SD
a
Relative difference calculated as 100 3 (ipsi-contra)/[(ipsi 1
contra)/2]. The number of measurements included was restricted by the preservation of LB1.
b
The means of two measurement trials are presented. Each of
the two trials was identical in terms of the direction of asymmetry (positive or negative).
c
Data cited from Netherway et al. (2006). N 5 21, mean age 5
6.75 months.
d
Position of LB1 in terms of the modern infant sample. An asterisk indicates that one of the two measurement trials
exceeded 1 SD but was still within the 2 SD range of variation.
cranial form are amply documented in ethnographic
studies of artificial cranial deformation. In this cultural
practice, force is applied to the infant’s head until the
desired shape is reached or the child rejects the deforming apparatus (Dingwall, 1931; Gerszten and Gerszten,
1995).
PDP often accompanies facial and mandibular asymmetries (Argenta et al., 1996; Kane et al., 1996; St. John
et al., 2002; Lee et al., 2008). Extensive unilateral occipital compression may anteriorly dislocate the ipsilateral
hemiface. However, this facial protrusion is often less
extensive than the occipital flattening, so that the horizontal distances between the midface (e.g., nasion or anterior nasal spine) and temporal region (e.g., porion)
tend to be shortened on the affected side (Netherway
et al., 2006). The cranial vault of LB1 exhibits near complete parallelogram skewing, but the zygomatic arch on
the occipital flattening side is shorter than that on the
opposite side (see Fig. 1). This observation is metrically
confirmed in Table 2, which examines differences in craniofacial measurements between the ipsilateral (occipital
flattening) and contralateral sides.
Table 2 also suggests that, at least in the mandibular
ramus, the asymmetric pattern of LB1 is consistent with
that observed in modern infants with PDP. However, a
detailed comparison of the faces of LB1 and present-day
children with PDP is difficult. This is because of the lack
of sufficient published data for the latter, the incompleteness of the LB1 skull (missing landmarks and distortion
in the mandible as stated earlier), differences in developmental age (the face experiences more significant growth
after birth compared to the neurocranium), and the variability of facial deformation in PDP (cf. Kane et al.,
1996; St John et al., 2002; Netherway et al., 2006). The
last observation is not unexpected because deformities in
the face are influenced primarily by the form of the posterior cranial deformation in PDP.
Nevertheless, LB1’s major facial asymmetries can be
explained as correlates of PDP, as described below. First,
the asymmetric positioning of the mandibular fossae of
American Journal of Physical Anthropology
LB1 probably affected the marked asymmetries in its
mandible. St John et al. (2002) suggested that the principal causative factor of mandibular asymmetry lies in the
positional distortion of the right and left mandibular fossae. When the mandibular fossa on the affected side is
dislocated anteriorly, the mandible inevitably rotates toward the unaffected side. Second, one interesting observation in LB1 is that the maxillary body rotation toward
the unaffected side (toward right) is slightly more extensive than those observed in the malar region (Fig. 1C)
and mandibular arch (see Fig. 2). As there are no
obvious signs of facial flattening on the left hemiface of
LB1, frontal or facial DP is excluded as a potential causative factor of the maxillary body rotation. We infer that
the comparatively extensive rotation of the maxillary
body was formed through occlusal guidance from the
mandibular dentition during the primary dentition period. Interestingly, the palatal midline runs nearly perpendicular to the line connecting the right and left mandibular fossae (Fig. 1C), whereas the incisive canal is
oriented in the same direction as the anteroposterior
axis of the cranial vault as described earlier (Fig. 1C).
During or after cusp removal by occlusal tooth wear,
such occlusal interference would have been relaxed, and
the mandibular arch may have been forced to re-orient
(rotation toward the affected side) due to the actions of
the chewing muscles. The zygomatic arches and temporal fossae that support these chewing muscles are not
symmetrically arranged relative to the palatal midline in
LB1, but are oriented more or less along the cranial midline (Fig. 1C). The twisted occlusion between the maxillary and mandibular arches (see Fig. 2) must have been
present at the beginning of the mixed dentition period,
but at this stage, the occlusal guidance probably could
no longer influence the occlusal relationship because of
the advanced growth in the facial skeleton. Although the
aforementioned explanation about the maxillary and
mandibular deformation is hypothetical, PDP may well
produce such facial deformation. Figure 5 shows an
example of a prehistoric adult skull that exhibits a pattern of PDP-related craniofacial deformation similar to
the case of LB1.
On the other hand, the causative background of the
medially depressed right zygomatic arch in LB1 (Fig.
1C,D; Brown et al., 2004) is unclear. This may have
occurred before or after death, and the former possibility
includes PDP and fracturing. If the right zygomatic arch
fractured soon after birth in LB1, the resultant unilateral disturbance of the jaw function may have influenced
the asymmetric facial development, but the documented
patterns of facial asymmetry in rats, monkeys, and
humans with unilateral masseter muscle dysfunction
(Rogers, 1947, 1955; Horowitz and Shapiro, 1955) are
different from the pattern observed in LB1. Overall, the
facial distortions in LB1 are in the horizontal rather
than the vertical direction, which is more reasonably
explained by PDP. Thus, even if the fracture in the right
zygomatic arch was present during the life of LB1, it
had little or no lasting impact.
DISCUSSION
We conclude that LB1 suffered from PDP and that
this was the dominant, if not the sole, cause of the specimen’s cranio-mandibular deformation. Although postdepositional earth pressure may have had some effect,
PDP offers an explanation that is consistent with the
PLAGIOCEPHALY IN HOMO FLORESIENSIS
183
Fig. 5. The skull of a mid-Holocene Jomon hunter-gather from Hokkaido, Japan. The individual exhibits a mild case of right
PDP as is recognized from the right occipital flattening and asymmetric nuchal muscle attachment area. As is the case with LB1,
the mandibular fossa is shifted anteriorly on the affected side, and the maxillary and mandibular dentitions are shifted toward the
affected side with the mandible showing overt lateral skewing. The maxilla exhibits a slight rotation, but the incisive canal is
directed anteriorly. The left maxillary molars were lost during the individual’s life, and the left maxillary lateral incisor was probably ritually ablated (Dodo, 1973).
whole range of observed asymmetries. The lack of significant postmortem distortion in the LB1 skull is also supported by the situation of its discovery and the completeness of the fragile skeletal elements. Intentional artificial deformation of the skull cannot be completely
rejected, but such practices by modern human groups
usually produce symmetrically deformed cranial vaults
(Dingwall, 1931), not the asymmetric cranio-facial deformation evident in LB1.
So, what are the implications of the presence of PDP
in LB1? To discuss this issue, we shall summarize below
the causative background, incidence, consequences, and
other features of PDP (or more generally DP because
much of the literature does not distinguish between the
two conditions) in modern children.
Hutchison et al. (2004) observed that some congenital
cranial deformities disappeared after birth while some
infants with no signs of cranial flattening at birth
acquired deformities postnatally. They concluded that
limiting head rotation and resting position are the most
important risk factors, and the first 4 months after birth
seemed to be an important time for the initiation of DP.
In other words, DP is multifactorial but severe cases are
often produced after birth by the infant’s preferential
head position (Boere-Boonekamp and van der LindenKuiper, 2001; Peitsch et al., 2002). As stated in the diagnosis section, there seems to be no significant ‘‘self-correction’’ of DP during childhood, and correcting head
shape in children older than 1–2 years requires surgery
in most cases (Wood and Shell, 2005).
Localized cranial flattening resulting from in utero or
intrapartum molding is now the most frequently cited
pre-natal factor, whereas birth injury associated with
forceps or vacuum-assisted delivery can be another risk
factor (Peitsch et al., 2002). Premature births are at particular risk here because of the need to spend a long
time in an incubator under helpless conditions. Congenital muscular torticollis and other conditions (scoliosis,
cephalohematoma, etc.) may also lead to a preferential
head position in an infant, but torticollis can also be
acquired after birth by preferential head position. Extensive use of car seats, cradleboards, and other devices that
fix the infant’s head to a flat surface may also produce
unintentional artificial cranial deformation (e.g., Kohn
et al., 1995; Persing et al., 2003), but the condition is
actually a more general phenomenon that occurs under
ordinary conditions without any special apparatus.
The true prevalence of DP is unclear, mainly because
of a disparity in diagnostic criteria (Hutchison et al.,
2004), but there is a consensus that it is a quite common
condition in the present day. From one of the few population-based studies (the Netherlands, N 5 7,609), the
prevalence of DP at the age of 2–3 years is estimated to
be 1.8% (calculated by the present authors using data
from Boere-Boonekamp and van der Linden-Kuiper,
2001). This is close to 1.7%, the value derived from the
study by Hutchison et al. (2004) based on 181 infants at
2-years old (the authors classified another 1.7% into the
extreme brachycephaly category). It is possible that
these figures slightly underestimate the real situation
because the parents involved had the opportunity to
learn about the potential risks.
The incidence of localized cranial flattening is higher
in twins than in single-born neonates. Firstborns and
American Journal of Physical Anthropology
184
Y. KAIFU ET AL.
boys also tend to show a higher prevalence (Peitsch
et al., 2002; Hutchison et al., 2003). In the aforementioned
large-scale study, Boere-Boonekamp and van der LindenKuiper (2001) reported that the male:female ratio of DP
children was 3:2. The affected side is somewhat biased to
the right side, a phenomenon which might be related to
the newborn’s posture at birth (Peitsch et al., 2002).
DP may cause neck muscle asymmetry; but otherwise,
its influence on other parts of the body seems to be
limited. DP is generally viewed as conferring little or
no risk aside from possible cosmetic problems and the
associated social-psychological risks. Although some
researchers suspect a tendency toward slight neurodevelopmental delay in DP children, such associations
still remain controversial (Collett et al., 2005). Collett
et al. (2005) inferred that if such an association exists,
DP and the accompanying brain deformation probably
does not act as a causative factor of neurodevelopmental
delay/deficit, which more likely develops independently
or acts as a primary causative factor that invites limited
mobility of the head during infancy. Moreover, artificial
cranial deformation in recent societies does not appear
to have significantly influenced mental development.
The aforementioned review suggests that DP is a secondary deformation, which has no pernicious effects on
cranial morphology except for overall skewing and other
localized effects. Given the present-day frequency of
DP—and the lack of serious associated health problems—the symptoms of this condition in LB1 do not support the claim that the individual suffered from severe
developmental abnormalities, nor do they undermine the
holotype status of LB1 (c.f. Jacob et al., 2006). Although
the present study does not reject the view that some
severe growth disturbance in LB1 invited limited mobility and PDP during infancy, the evidence of cranial deformation itself should not be cited as an independent
indicator of severe pathology.
The discovery of a DP case from a latest Pleistocene
archaeological site arouses interest as to whether this
accidental cranial deformation is unique to humans and
when and how it appeared in the history of humanity.
One possible scenario is that DP became evident only after the development of secondary altriciality, which
forced modern humans to deliver a helpless newborn
with soft and malleable cranial bones. If this is correct,
studies of DP in paleoanthropological context have the
potential to inform us about some important aspects of
the evolution of life history in hominids.
Although the previous systematic studies of DP in
past populations are few in number (Pospı́šilová and
Procházková, 2006), it is possible that prehistoric human
skulls with DP are not uncommon among archeological
or museum collections but that they have so far
remained relatively unnoticed or ignored. In fact, we
found in our preliminary survey that DP was not a rare
phenomenon among the Holocene hunter-gather population of the Jomon period in Japan (see Fig. 5). This condition may also be evident in a Neanderthal skull from
Le Moustier (Ponce de Léon and Zollikofer, 1999; Ponce
de Léon, 2002). We hope that the present report opens
up studies of the prevalence and origin of DP in prehistoric humans.
ACKNOWLEDGMENTS
The authors thank Mike Morwood, Nobuhito Morota,
Tsutomu Ogata, Etty Indriati, Yuji Mizoguchi, Kenichi
American Journal of Physical Anthropology
Shinoda, Reiko T. Kono, and Kazuhiro Sakaue for advice
and discussion. They also appreciate the two anonymous
reviewers and the editors for their helpful comments.
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