Pathological bone changes in the mandibles of wild red deer ...
Transcript of Pathological bone changes in the mandibles of wild red deer ...
J. Anat. (1998) 193, pp. 431–442, with 16 figures Printed in the United Kingdom 431
Pathological bone changes in the mandibles of wild red deer
(Cervus elaphus L.) exposed to high environmental levels of
fluoride
MICHAEL SCHULTZ1, UWE KIERDORF2, FRANTISEK SEDLACEK3 AND HORST KIERDORF4
"Zentrum Anatomie, UniversitaX t GoX ttingen, GoX ttingen, Germany, # Institut fuX r Allgemeine und Spezielle Zoologie, Justus-
Liebig-UniversitaX t Giessen, Giessen, Germany, $ Institute of Landscape Ecology, Ceske Budejovice, Czech Republic, and
%Zoologisches Institut, UniversitaX t zu KoX ln, KoX ln, Germany
(Accepted 2 June 1998)
A macroscopic, microscopic and scanning electron microscope study was performed on the pathological
bone changes of the mandibles of wild red deer (n¯ 61) exhibiting severe dental fluorosis. The animals
originated from a highly fluoride polluted area in Central Europe (Ore mountains and their southern
foreland, Czech-German border region) and constituted 11±2% of the studied red deer sample (n¯ 545)
from this area. Pathologically increased wear and fracture of fluorosed teeth caused a variety of mandibular
bone alterations, including periodontal breakdown, periostitis, osteitis and chronic osteomyelitis. As a
further consequence of severe dental attrition, opening of the pulp chamber and formation of periapical
abscesses were occasionally observed. In case of severe periodontal breakdown, loss of teeth from the
mandibles was found. In addition to the inflammatory bone changes, the occurrence of osteofluorotic
alterations was also diagnosed in the specimens with the highest bone fluoride concentrations (" 4000 mg
F−}kg dry wt). These changes comprised extended apposition of periosteal bone onto the mandibular cortex
as well as deformation of the mandibular body, which was attributed to a fluoride-induced osteomalacia.
The present study provided circumstantial evidence that, in addition to fluoride induced dental lesions, the
occurrence of marked periodontal disease and tooth loss is an important factor responsible for a reduction
of life expectancy in severely fluorotic wild red deer.
Key words : Dental fluorosis ; skeletal fluorosis ; periodontal disease ; bone pathology; environmental pollution.
Fluorosed dental hard tissues of deer exhibit a variety
of pathological alterations, including enamel sub-
surface hypomineralisation of different depth and
extent, occurrence of enamel hypoplasias, presence of
large amounts of interglobular dentine and accen-
tuation of the incremental lines in enamel and dentine
(Kierdorf et al. 1993, 1996c, 1997; Appleton et al.
1996; Kierdorf & Kierdorf, 1997). As a consequence
of enamel hypomineralisation, severely fluorosed deer
teeth show markedly increased wear, eventually
leading to the loss of a functional tooth shape. In
addition, fracturing of severely fluorosed teeth and
tooth loss were occasionally observed in wild deer
exposed to increased levels of fluoride (Kierdorf et al.
Correspondence to Dr Horst Kierdorf, Zoologisches Institut, Universita$ t zu Ko$ ln, Weyertal 119, D-50923 Ko$ ln, Germany. Tel. : 49-221-
470-2606; fax: 49-221-470-4987.
1996c). Recently, a strong positive correlation be-
tween the degree of dental fluorosis and mandibular
bone fluoride content was found in a sample of red
deer exposed to elevated levels of fluoride, thus
demonstrating the usefulness of dental fluorosis as a
biomarker of increased fluoride exposure for bio-
monitoring studies in deer (Kierdorf & Kierdorf,
1998). During research in the heavily fluoride-polluted
area of the Ore mountains and their southern foreland
(Czech-German border region) (Kierdorf et al.
1996a, b, c), a high prevalence of pathological bone
changes was also found in the mandibles of fluorotic
red deer. So far, these bone alterations have not been
described in great detail, nor has any other work on
wild mammals focused on mandibular bone pathology
related to the occurrence of dental fluorosis.
Fig. 1. Right hemimandible of a 10-y-old red deer stag, bucco-occlusal view. Bone fluoride content 3647 mg F−}kg dry wt. Severe attrition
of P$, P
%and M
#, and fracturing of M
$. Note roughening of the cortex (arrowhead) beneath the P
$due to periosteal bone apposition.
432 M. Schultz and others
In an attempt to further characterise the con-
sequences of increased fluoride exposure on free-living
deer the aims of the present study have been: (1) to
provide a detailed description of the pathological
changes to the mandibular bone of red deer from this
highly fluoride polluted area, (2) to study the aetiology
and pathogenesis of these lesions and (3) to discuss the
consequences of the pathological mandibular bone
alterations for the individual and the population.
Specimens
A total of 61 defleshed, cleaned and dried red deer
mandibles (n¯ 43) or hemimandibles (n¯ 18) ex-
hibiting marked to severe dental fluorosis (for details
of tooth classification see Kierdorf et al. 1996b) were
at our disposal. Except for 1 specimen, all mandibles
originated from male animals. The analysed material
represented 11±2% of the total number of red deer
specimens (n¯ 545, of which 410 showed dental
fluorosis of varying degrees) with a completed per-
manent dentition, that were inspected in the course of
our above-mentioned biomonitoring studies (Kierdorf
et al. 1996a, b). The study area is exposed to severe
fluoride pollution, originating mainly from emissions
of the large brown-coal fired power plants situated in
the north-Bohemian basin (Reuter et al. 1997).
Except for 2 animals, which were found dead, all
red deer had been taken during normal hunting
operations. Their mandibles were collected, cleaned
and provided for study by the local hunters. The age
of the individuals was assessed independently by 3
experienced persons, based on the wear of the first
molats. The ages given in this paper are the means of
these 3 values, rounded to the nearest full year. The
M"
was used for age estimation since in red deer
exposed to high fluoride levels during dental de-
velopment this tooth is the only one exhibiting normal
enamel mineralisation and, thus, also normal, i.e. age
related wear (Kierdorf et al. 1996c). This has
previously been attributed to the fact that crown
formation in the M"takes place prenatally and during
the period of milk feeding and that, contrary to the
Fig. 2. Left hemimandible of an 8-y-old red deer hind, bucco-occlusal view. Bone fluoride content 4167 mg F−}kg dry wt. Formation of deep
alveolar bone pockets with partial or total root exposure between the molars and between P%and M
". Loss of interdental contact between,
and slight mesial inclination of, the molars. Also note roughening and dilatation of the corticalis and deformation of the mandibular body.
Fig. 3. Left hemimandible of an 8-y-old red deer stag, bucco-occlusal view. Bone fluoride content 4680 mg F−}kg dry wt. Pronounced loss
of alveolar bone, especially between M"
and M#, leading to total or partial root exposure. Loss of interdental contact between the molars
and between P%
and M". Also note deformation of the mandibular body.
Fig. 4. Left hemimandible of a 6-y-old red deer stag, lingual view. Bond fluoride content 2262 mg F−}kg dry wt. Normal enamel appearance
of M"
(asterisk), whereas the other teeth exhibit enamel discolouration and moderately (premolars) to severely (M#) increased wear. Note
wedging of forage into interdental gap between P%
and M".
other, later mineralising permanent cheek teeth, it is
therefore not exposed to markedly elevated plasma
fluoride levels during development, even in individuals
from highly fluoride-polluted habitats (Kierdorf et al.
1996 a, c). The estimated ages of the specimens
forming our sample ranged between 5 and 13 y.
Crown formation in the permanent dentition in red
deer is completed at C 26 mo of age (Brown &
Chapman, 1991).
Samples of mandibular bone were obtained and
analysed for fluoride content with a fluoride ion
specific electrode (Orion model 96-09, Cambridge,
MA) as described previously (Kierdorf et al. 1996c).
Compared with age matched controls from an
unpolluted area (highest concentration 1026 mg
F−}kg dry wt in a 14-y-old animal), the bone fluoride
levels recorded in the present sample were increased
by factors of 4±0 to 8±1 (Kierdorf et al. 1995, 1996c).
The highest value (4680 mg F−}kg dry wt) was
measured in an 8-y-old individual.
Examination of bone changes
All mandibles were first inspected for gross mor-
phological bone changes and photographed. After-
wards, buccolingually oriented -rays were taken
from selected specimens. For histopathological analy-
sis, epoxy resin embedded, buccolingual ground
sections of 70 µm thickness were prepared from
segments of some of the mandibles according to the
method described by Schultz & Drommer (1983) and
Schultz (1988). The sections were viewed and photo-
graphed in normal and polarised transmitted light.
For scanning electron microscopy, bone samples were
removed from the mandibles, mounted on aluminium
stubs, sputter-coated with gold-palladium and viewed
in a scanning-electron microscope Zeiss DSM 250,
operated at 15 kV.
In the fluorotic red deer mandibles only the 1st molar
exhibited normal wear, whereas the other permanent
cheek teeth showed pathologically increased attrition
Pathological bone changes in fluorotic deer mandibles 433
Fig. 5. Lingual mandibular surface of the specimen shown in Fig. 3. Note pitting of the cortex and numerous impressions of small blood
vessels.
Fig. 6. Scanning electron micrograph of the bone surface shown in Fig. 5. Impressions of small blood vessels (asterisk), blood vessel openings
(arrowhead) and numerous microfistulae are discernible. ¬22.
Fig. 8. Apposition of periosteal bone onto the original cortical surface of the mandible shown in Fig. 3. Scanning electron micrograph. ¬50.
(Figs 1–4). In consequence, a marked and often
irregular reduction of crown height and crown length
was observed in the fluorosed teeth, leading to the
formation of dysfunctional, sometimes sharp-edged
tooth crowns. Fracturing of M#or M
$was seen in 15
of the 61 (¯ 24±6%) specimens (Figs 1, 12, 13). In the
434 M. Schultz and others
complete mandibles, tooth fractures mostly occurred
in a bilaterally symmetric fashion.
As a sequel of severe dental attrition and tooth
fracturing, advanced periodontal lesions and signs of
dentoalveolar abscess formation were found in 32 of
the 61 (¯ 52±5%) specimens forming our sample. In
the (macerated) specimens an initial sign of perio-
dontal disease was a slight bone loss at the alveolar
crest, leading to exposure of cancellous bone and of
the proximal parts of the tooth roots (Figs 2, 3). A
more pronounced reduction in height of the alveolar
process was typically associated with loss of contact
and the occurrence of gaps between adjacent teeth
(Figs 2, 3). Such diastema formation was most
frequently found between the 1st molar, possessing
enamel of normal hardness, and its neighbouring
teeth (P%and M
#), whose hypomineralised enamel had
been rapidly eroded due to interdental and occlusal
wear. Gap formation between P%and M
"was further
promoted by the fact that the contact face between the
crowns of these 2 teeth is rather small and confined to
their more occlusal portions. In 1st and 2nd molars,
the loss of contact with their neighbouring teeth often
led to a mesial drift and sometimes also to a slight
mesial inclination, leading to additional gap form-
ation within the tooth row (Figs 2, 3). Wedging of
forage into the interdental gaps (Fig. 4) was associated
with further resorption of alveolar bone, thereby
creating more space for additional food impaction.
In specimens exhibiting severe periodontitis and
alveolar bone loss, the basal portions of the tooth
sockets were also affected, and advanced bone
resorption concomitant with complete exposure of
individual tooth roots as well as formation of deep
and distended bone pockets were observed (Figs 2, 3).
Gross morphological bone changes related to the
suppurative inflammatory processes included
roughening and pitting of the buccal and lingual bone
cortex due to penetration by small blood vessels and
presence of numerous microfistulae (Figs 2, 5, 6).
Inspection of ground sections taken from the
affected regions revealed pathological changes of the
mandibular cortex resulting from the inflammatory
processes. Thus in the specimen shown in Figure 3
apposition of layers of woven bone onto the original
lingual surface of the mandibula was observed
(Fig. 7a). As a consequence, a highly porous outer
bone layer had been formed. This finding marks a
chronic inflammation which seemingly acted with
recidivation.
In some specimens, new cortical bone formation
was confined to areas affected by the inflammation
and the bone apposition was thus regarded as resulting
from a periosteal reaction triggered by the inflam-
matory processes. However, in 2 specimens with very
high bone fluoride levels (4680 and 4167 mg F−}kg
dry wt, respectively) a more generalised apposition of
a layer of periosteal bone onto the original mandibular
surface occurred (Figs 7b, 8). Also, in 3 of the 4
specimens with bone fluoride levels exceeding 4000 mg
F−}kg dry wt present in our sample, an abnormal
curvature of the mandibular body was observed (Figs
2, 3). This deformation indicated a weakening of the
mandibular bone in the affected individuals.
In cases of excessive dental attrition, the occurrence
of pulpits and periapical inflammation, causing the
formation of chronic periapical abscesses, was also
occasionally observed. Thus in the specimen shown in
Figures 9–11, opening of the pulp chamber of the
severely worn P%
had caused the formation of a
periapical abscess associated with the distal root of
this tooth (Figs 9, 11). Deep-seated suppuration at
this location then produced an opening fistula in the
buccal cortex of the mandibular body, the relatively
large sinus opening being surrounded by a rim of
newly formed woven bone (Fig. 10), indicative of a
reactive periostitis. Microscopic examination revealed
that the abscess had penetrated through the bottom of
the tooth socket into the mandibular canal (Fig. 7c).
As is shown in Figures 1 and 7d, a chronic
inflammatory process, established as a consequence of
severe dental attrition, could also induce a periosteal
reaction, leading to the apposition of woven bone
onto the buccal cortex.
Tooth fractures constituted another pathological
condition causing periodontal disease in the fluorotic
mandibles. In the specimen depicted in Figure 1,
molar fracturing must have occurred shortly before
death, since the associated periodontal lesion is still
rudimentary. A much more advanced stage of perio-
dontal disease resulting from tooth fracture is shown
in Figures 12 and 13. In these cases, inflammation
following tooth fracture had led to deep-seated
suppuration and partial destruction of the tooth
sockets of both M$. In the left hemimandible, opening
of the mandibular canal had occurred (Fig. 12).
Beneath the fractured teeth, the lingual face of the
mandible’s outer cortex exhibited an irregular pitting
and impressions caused by small blood vessels.
Inspection of ground sections revealed signs of severe
bone inflammation in the tooth socket of the 3rd
molar. On the lingual face of the mandibular body a
thin external basic lamella covering the original cortex
was observed. In the pitted area, the bone surface was
structured by partly very flat, partly deeper foveolar,
this being indicative of healed inflammation. On the
Pathological bone changes in fluorotic deer mandibles 435
Fig. 7. Thin ground sections (70 µm) viewed in polarised light using a hilfsobjekt-I (quartz) (a, b, d–h) or in normal transmitted light (c).
(a) Apposition of layers of woven bone onto the original lingual alveolar cortex, marking a chronic inflammation; arrows: original bone
surface ; specimen shown in Fig. 3 ; ¬57. (b) Periosteal bone deposited onto the original cortical surface of the mandibular body, interpreted
as a fluoride-induced osteoblastic reaction; asterisk: blood vessel canal ; specimen shown in Fig. 3 ; ¬228. (c) Destruction of the bony plate
436 M. Schultz and others
buccal side, the original bone surface was covered by
a layer of woven bone (Fig. 7e). The external basic
lamella and a narrow area of the external osteonal
bone (Fig. 7e) as well as the roof of the mandibular
canal (Fig. 7 f ) were destroyed by osteoclastic activity.
These findings demonstrate the presence of severe
chronic inflammatory processes, including early
chronic osteomyelitis, that were still active when the
animal died.
A very severe case of chronic osteomyelitis and
concomitant osteitis, periostitis and periodontitis was
observed in the mandible of a 9-y-old stag found dead
(Figs 14–16). In this specimen, both M$were missing.
Since the remnants of their former alveoli were almost
completely filled with cancellous bone, loss of these
teeth, probably as a consequence of tooth fracture,
must have occurred long before death. In addition,
the P$, P
%and M
#were worn down to their roots. In
the left hemimandible, opening of the mandibular
canal had occurred in the region of the 3rd molar. On
the right side, destruction of the 3rd premolar tooth
socket and opening of the mandibular canal at this
location were noted (Fig. 14). In the affected area, the
mandibular body formed a large, bulging capsule with
a highly porous surface structure (Fig. 15). At the
level of the M", a wide fistula opening was present in
the lingual cortex. Within the distended mandibular
canal, a large bony sequestrum was found, which
extended from the level of the 2nd premolar to that of
the 1st molar (Fig. 16). This sequestrum represented
part of the original lingual alveolar cortex, which had
become displaced and partly destroyed due to a severe
inflammatory process associated with dentoalveolar
abscess formation. Histological study further pro-
vided evidence of (1) apposition of woven bone onto
the surface of the sequestrum (Fig. 7g), (2) advanced
osteoclastic bone resorption that had caused de-
struction of the former lingual alveolar corticalis, and
(3) formation of new periosteal bone constituting the
highly porous bulging capsule (involucrum) now
forming the lingual cortical surface of the mandible
(Fig. 7h). As a consequence of intense suppuration,
the premolar and molar roots of the specimen
exhibited a very marked hypercementosis (Fig. 16).
separating the tooth sockets from the mandibular canal due to a chronic periapical abscess ; asterisk: root cement ; specimen shown in Fig.
9 ; ¬57. (d ) Newly formed bone spicules covering the original buccal cortical surface, the bone formation representing a periostitis caused
by a chronic inflammatory process ; specimen shown in Fig. 1 ; ¬57. (e) Original mandibular buccal surface covered by a secondary layer
of woven bone. The external basic lamella and a thin layer of the external haversian systems have been destroyed by osteoclastic resorption;
specimen shown in Fig. 12; ¬57. ( f ) Howship’s lacunae (arrows) in the roof of the mandibular canal denoting osteoclastic bone resorption;
specimen shown in Fig. 12; ¬228. (g) Bone apposition (asterisk) onto the surface of the bony sequestrum representing part of the original
lingual alveolar cortex; specimen shown in Fig. 14; ¬57. (h) Newly formed porous bone, representing an involucrum, covering the remnants
of the original outer cortical plate ; asterisk: resorption cavity within the original cortex; specimen shown in Fig. 14; ¬57.
The present study revealed that reduced enamel
hardness and the resulting increased wear of fluorosed
deer teeth caused a variety of pathological mandibular
bone changes in the affected animals. Rapid occlusal
and interdental attrition led to diastema formation,
the resulting increase in tooth mobility causing an
imbalance in periodontal tension and in consequence
a drift of individual teeth away from their normal
positions, leading to an enlargement of interdental
gaps. Mechanical trauma to the gingiva, due to
wedging of forage into these gaps and}or occurrence
of injury caused by the sharp-edged tooth crowns,
promoted the establisment of periodontal inflam-
mation. Periodontal breakdown with damage to and
recession of the alveolar bone occurred as a sequel to
this process.
Severe periodontal lesions were also frequently
observed as a consequence of tooth fracture. Fur-
thermore, the occurrence of periapical abscesses,
caused by exaggerated attrition of the fluorosed teeth
and, in consequence, an opening and infection of the
pulp cavity, was occasionally observed in our material.
Similar lesions have previously been described on a
macroscopic scale in deer (Karstad, 1967; Kay et al.
1975), sheep (Roholm, 1937; Milhaud & Gras, 1978),
horses (Shupe & Olson, 1971) and cattle (Gru$ nder,
1972; Lasarov et al. 1972; Shupe & Olson, 1983) with
severe dental fluorosis. As already stated by Shupe &
Olson (1971), in contrast to the typical tooth changes,
the periodontal lesions present in fluorotic animals are
not pathognomonic of a chronic fluoride intoxication.
Prevalence and severity of periodontal lesions
present in our sample of red deer exhibiting marked
dental fluorosis substantially differed from the situ-
ation in a population not exposed to increased levels
of fluoride. Thus Geiger et al. (1992), who studied 431
red deer mandibles from the Harz mountains
(Germany) found only 3 cases (¯ 0±7%) of perio-
dontal disease, all affected individuals being 13 or
more years of age. In 267 complete red deer skulls
from the same area, the lower jaw was significantly
less affected by periodontal lesions than the upper
Pathological bone changes in fluorotic deer mandibles 437
Fig. 9. Right hemimandible of a 13-y-old red deer stag, bucco-occlusal view. Bone fluoride content 4223 mg F−}kg dry wt. Severe dental
disfigurement. Note formation of a periapical abscess associated with the distal root of the P%
as a consequence of opening of the tooth’s
pulp cavity (arrow). A large sinus opening penetrates the buccal cortex.
Fig. 10. Newly formed woven bone caused by reactive periostitis surrounding the large sinus opening shown in Fig. 9. Asterisk, distal root
of P%.
Fig. 11. Radiograph of the hemimandible shown in Fig. 9. Note radiolucent space around the tip of the distal root of the P%
(arrowhead)
and marked hypercementosis on the roots of this tooth.
438 M. Schultz and others
Figs 12, 13. Left (12) and right (13) hemimandibles of a 6-y-old red deer stag, bucco-occlusal views. Bone fluoride content 2670 mg F−}kg
dry wt. Fracturing of both M$
in a symmetric fashion and opening of the mandibular canal in the left hemimandible (arrow). In the right
hemimandible, the distal column of the 3rd molar has not been shed. Note marked loss of alveolar bone at the fracture site (arrowhead).
jaw. In the complete skulls, periodintal changes
affecting only the lower jaw were not observed.
Furthermore, occurrence of tooth fractures was not
reported in the 698 specimens studied by Geiger et al.
(1992).
As was previously shown (Kierdorf et al. 1996c),
severely fluorosed premolars and molars of red deer
are characterised by the loss of a functional crown
shape. In analogy to the situation reported for severely
fluorotic cattle (Shupe & Olson, 1983), an impairment
of body condition can be expected in this situation.
Severe periodontal disease and its sequels (tooth loss,
pain, abscess formation, etc.) will exacerbate this
fitness reduction due to further limitations in food
intake and processing as well as a general deterioration
of the animal’s health, especially in case of acute or
chronic abscess formation. A corresponding loss of
body condition resulting from dental and periodontal
disease was previously described in chamois
(Rupricapra rupricapra) (Pekelharing, 1974) and rein-
deer (Rangifer tarandus) (Leader-Williams, 1980), the
latter animals probably suffering from lumpy jaw
disease. It is reasonable to assume that in severely
fluorotic red deer emaciation resulting from the
pathological conditions described above will eventu-
ally lead to premature death, especially of older
individuals. This situation is thus an example of an
initially sublethal effect (fluoride induced dental
changes) becoming lethal under certain conditions
(Heinz, 1989), in this case as a consequence of
Pathological bone changes in fluorotic deer mandibles 439
Fig. 14. Right hemimandible of a 9-y-old red deer stag, bucco-occlusal view. Bone fluoride content 3555 mg F−}kg dry wt. Loss of M$and
very severe attrition of the other cheek teeth, except M". Remnants of the former alveolar cavity of the M
$almost completely filled by woven
bone (asterisk). Opening of the mandibular canal at the bottom of the alveolar cavity of the P$
(arrowhead).
Fig. 15. Lingual view of hemimandible shown in Fig. 14. The cortical bone forms a large bulging capsule with a porous surface structure.
A large sinus opening is present and a sequestrum lying in the mandibular canal is discernible.
Fig. 16. Radiograph of the hemimandible shown in Fig. 14. The sequestrum extends from the level of the P#to that of the M
"(arrowheads).
Also note very pronounced hypercementosis on the tooth roots.
440 M. Schultz and others
established severe pathological bone changes and
tooth loss with advanced age.
Premature death can also occur as a direct result of
dentoalveolar abscess formation. According to Miles
& Grigson (1990), opening of an abscess into the oral
cavity commonly leads to a septic pneumonia due to
inhalation of septic discharges. Also a generalized
septicaemia due to spreading of the infection via the
blood stream could lead to the animal’s death.
Some of the pathological bone alterations observed
in the animals with the highest skeletal fluoride levels
are regarded as resulting from of a systemic effect of
the ingested fluoride on bone formation and turnover.
Thus the generalised apposition of periosteal new
bone, which was observed in some of the fluorotic red
deer, is a well-known consequence of chronic fluoride
intoxication (Roholm, 1937; Shupe & Olson, 1983;
Shupe et al. 1992; Vikøren & Stuve, 1996), due to a
fluoride induced stimulation of osteoblastic activity.
The abnormal curvature of the mandibular body seen
in 3 red deer specimens with bone fluoride contents
exceeding 4000 mg F−}kg dry wt denotes a weakening
of the bone, leading to its deformation upon mech-
anical loading. As was shown in clinical and ex-
perimental animal studies, prolonged uptake of
increased amounts of fluoride leads to osteomalacia
and decreased biomechanical competence of bone
(Boivin et al. 1989; Chavassieux et al. 1991; Søgaard
et al. 1994, 1995; Lundy et al. 1995; Turner et al.
1995). On the basis of these findings, the mandibular
deformation observed in the highly fluoride exposed
red deer is supposed to be the result of a fluoride
induced osteomalacia. However, in addition the severe
inflammatory changes present in these mandibles may
have contributed to the weakening of the mandibular
bone.
The present study provides circumstantial evidence
that in addition to the fluoride induced dental lesions
the occurrence of severe periodontal disease (including
tooth loss) is also a potential factor limiting the life-
span of severely fluorotic red deer. In populations
from highly fluoride polluted habitats a shift in age
structure compared to populations from uncontam-
inated areas is therefore likely to occur. This view is in
principal accordance with the findings of Kay et al.
(1975), who reported a shift to younger age classes in
mule deer (Odocoileus heminonus) and white-tailed
deer (Odocoileus virginianus) inhabiting a severely
fluoride polluted area. Since the red deer inhabiting
our study area are under considerable hunting
pressure, effects of regional fluoride pollution on
population structure are however difficult to assess.
The expert technical assistance of M. Brandt, A. Heise
and I. Hettwer-Steeger is gratefully acknowledged.
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