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The calcification pattern of deciduous teeth in miniature swine
Archs oral Bid. Vol. 16, pp. 639-648, 1971.Pergamon Press. Printed in Great Britain.
THE CALCIFICATION PATTERN OF DECIDUOUS TEETH IN MINIATURE SWINE CYNTHIAF. MCKEAN, E. B. JUMPand M. E. WEAVER University of Oregan Dental School, Department of Anatomy, 611 S.W. Campus Drive, Portland, Oregon 97201, U.S.A. Summary-Thirty-eight foetuses of Pitman-Moore “miniature swine” were obtained at different ages in utero by caesarean section and stained with alizarin red S to show calcification. The time and sequence of cakihcation was noted for each tooth and the pattern of calcification within each dental arch as well. Initial calcification of teeth occurred in the same pattern reported for eruption of deciduous incisor and molar teeth in “miniature swine”. The number of calcif?cation centres varied with different types of teeth. There were no separate calcification centres for mammelons. The time and sequence of calcitication were noted for cusps of all teeth and differed somewhat from reports for teeth of domestic swine. The sequence of calcification of teeth within each arch was not from anterior to posterior as often generalized for mammals, but was a different, distinct pattern for each arch. The sequence of calcification within certain teeth exhibited similarities to reports for primates and man, indicating a possible basic genetic control of tooth formation for mammals in general.
FOR MANYyears dental scientists stated that the calcification of deciduous teeth in mammals occurred in a rigid pattern beginning mesially with the fist incisor and progressing distally until finally the last deciduous molar was calcified (LEGROSand MAGITOT, 1880; SCHOUR,1953; ORBAN, 1957). Perusal of the literature, however, revealed little evidence to substantiate such an idea and more recent reports deny this is the sequence in the cat (GAUNT, 1959), the rhesus monkey (SWINDLERand MCCOY, 1964), or even in man (KRAUS, 1959). This study was concerned with the chronology and sequence of dental calcification in Pitman-Moore miniature swine and possible relationships between calcification and eruption. MATERIALS
AND
METHODS
Thirty-eight foetuses were obtained by caesarian section at 19 different stages of gestation ranging from 32 days post-insemination to term (112 & 2 days). Upon removal from the uterus the foetuses were placed immediately in 10 per cent formalin. After adequate fixation, the two specimens of each age were decapitated and the heads were bisected in the midsagittal plane. The right halves were roentgenographed, stained with alizarin red S, and stored in glycerin (NOBACK and NOBACK, 1944). The left halves of the heads were retained for histological study, the data from which will be presented later as a separate report. All of the toothbuds from the right halves of the heads were excised under the dissecting microscope at a magnitication of 20 x . Newborn specimens were dissected first to permit better orientation. Subsequently, as the younger specimens were examined, we could still identify specific tooth germs even before dental mineralization began. Working drawings of each toothbud were made as it was removed from the dental crypt. These drawings facilitated reorientation of specific teeth at a later time. 639
640
F.
CYNTHIA
MCKEAN,
E. B. JUMP AND M. E. WEAVER
The time of initial calcification, as indicated by the alixarin stain, was recorded for each tooth. The following procedure was developed in order to record also the pattern of calcification for each tooth type: (1) Compare by inspection the cleared tooth germs of each tooth type in both animals at a particular age. (2) Photograph one of each type specimen at each age in buccolingual or occlusal projection while the specimen was suspended in glycerol, using both transmitted and incident illumination. Occlusal projections best depict the teeth with multiple cusps. (3) Prepare enlarged tracings of negative images of the calcified zone of a given tooth at successive foetal ages. (4) Produce an artist’s composite drawing of each tooth, using the enlarged tracings from the developmental stages with the cusp tip and axial line of cusp as the registration determinants for superposition. OBSERVATIONS
Typically, P&man-Moore miniature swine have the same deciduous dental formula i3, c, m4 as do commercial swine: However, we have reported that one tooth, the i3, c, m4 . lower first deciduous molar, was usually missing in our miniature swine (WEAVER, JUMP and MCKEAN, 1966). The time and sequence of initial calcification in deciduous teeth is presented in TABLE 1.
CALCIFICATION
FORMULA
FOR
OF A TOOTH
BEOAN
PARENTHESES,
IS
INCISOR,
INDICATED
CANINB,
AND
BY MOLAR
SYMBOLS
FROM
TEETH.
WHEN
AT DIFFERENT
AGES, ITS FIRST APPEARANCE
WHEN
CALCIFICATION
BUT
IN BOTH
SOME
SPECIMENS
SHOWED
NO PARBNTHESES
WBRE
THE
IS INDICATED
IN A GNEN USED
N ITIAL CALCIFICATION OF MINIATURE SWINE DENTITION I
DAYS GESTATION 49 51 53 55 58 61 65 70 75 80 85 91 95 100 105 112 (newborn)
MAXILLA
MANDIBLE
-
-
c,
(m3) (i 31,m3 i3 il, m4 m2 (Ml) Mi i2
C -
(m4) (ill,(i3), m4 m3, il, i3 ‘i2 m2, Ml -
DENTAL
CALCIFICATION IN
TOOTH
CALCIFlCATiON
PATTERN
Table 1. Dental calcification began mineralization was noted throughout molars which develop and calcify teeth showing calcification at birth
IN MINIATURE
SWINE
TEETH
641
at 51 days in utero and at birth some degree of the primary dentition except in the first deciduous after birth, when present. The only permanent were the upper and lower first molars. Figure 1
CALCIFICATION AND ERUPTiON OF DECIDUOUS DENTITION
i 1i 2i 3c m2m3m4-
A Calcification a
Eruption
FIG. 1. Initial calcifkation of individual teeth was approximated to weekly intervals from the data and is compared with eruption times reported for these teeth (WEAVER, JUMP and MCKIZAN, 1966).
compares initial calcification of the deciduous teeth with the eruption time reported for those same teeth (WEAVER et al., 1966). The left end of each bar, marked with the
triangle, represents the mean age at which corresponding teeth in both specimens showed evidence of calcification. Conversely, the right end of each bar, marked with the dark circle, represents the mean age reported for the clinical eruption of that tooth. A vertical line placed along the abscissa at any desired age between 7 weeks in uiero and 11 weeks post partum will intersect bars of those teeth undergoing calcification at that age. The length of the bar representing a particular tooth indicates the number of weeks elapsed between the beginning of calcification and the eruption of that tooth into the mouth and allows an easy comparison of the developmental history of different teeth. With respect to calcification of teeth, several different basic patterns became apparent, ranging from a single centre of calcification to as many as six major calcification centres. All of the anterior teeth had single centres of calcification. The third incisors and canines developed smooth conical teeth without any evidence of cingula or accessory cusps. The G.rst deciduous incisors in both arches and the mandibular second incisors did exhibit mammelons. However, in each case calcification began at the tip of the central mammelon and gradually enveloped the rest of the tooth (Fig. 2). There were no mammelons associated with the second maxillary incisors. A.O.B. S/~--P
CYNTHIAF. MCKEAN,E. B. JUMPANDM. E. WEAVER
642
r
Mesial
)--c
Distal
Days
gestation 61
mm 70 91 (
1 Newborn
FIG. 2. The right mandibular fkst incisor exhibits three mammelons, the central one being the site of initial calci6caCon for the tooth. Other single cusp teeth ditkr slightly in shape but exhibit the same developmental pattern, without mammelons.
Another type of tooth showing a single centre of calcification was trilobate in form and included both maxillary and mandibular second deciduous molars (Fig. 3). Each of these tooth germs developed two or more cusps in a linear arrangement in the mesio-distal axis of the tooth. In each instance calcification began with the central Mesial Days
-
Distal
gestation
mm
right maxillary second molar has a single calcification centre but develops multiple cusps. Buccal or lateral view, with occlusal surface upward.
FIG. 3. The
CALCIFICATION
PATI-ERN
IN MINIATURE
SWINE
TEETH
643
cusp and progressed both anteriorly and posteriorly until the other cingulate cusps were completed. We therefore grouped these particular deciduous molars with the mammelon-forming incisors on the basis of similar development. The rest of the deciduous teeth had multiple calcification centres. The simplest arrangement of these was in the mandibular third molar which seemed to represent a transition from single to multiple centres of calcification. It had a linear arrangement of its cusps as did the second molars. Calcification in this tooth was first noted for the major cusp at 61 days followed by minor cusp formation. A second more distal centre developed at 65 days and fused with the first cusp at 70 days. At this age, calcification had also progressed mesially toward a third cusp. Finally, calcification appeared in yet a fourth cusp of the tooth at 80 days and was fused with the rest of the calcified crown of the tooth 5 days later. The maxillary third molar had three separate calcification centres, which developed at different times as indicated in Fig. 4. Instead of the linear cuspal arrangement, which was noted in the mandibular third molar, its occlusal outline roughly formed an isosceles triangle, the apex of which was anterior or mesial. The mesial cusp was the most prominant and the Grst to calcify. Figure 5 shows the quadrangular form of the maxillary fourth deciduous molar. Its calcification progressed from four centres beginning with the mesio-buccal cusp at 61 days. The mandibular fourth molar presented the most complex form of the deciduous dentition. This crown consisted of six major cusps and at least two minor ones, all of which appeared as separate calcification centres. The details of its formation have been summarized in a diagram (Fig. 6). The figures within the circles represent the order of Mesial
Days gestation 55
Buccal
q Newborn Fro. 4. The right maxillary third molar developsfrom three separate cenkzs of calcification, beginning at different ages. Occlusal view.
-
F. MCKEAN,E. B. JUMPAND M. E. WEAVER
r
Mesial
Days
gestation 61 65
70-75 lllllllllll
mm
a
s
=I= __
85
95
cl Newborn FIG. 5. The right fourth maxillary molar develops from four centres of calcification which begin at diierent ages and fuse buccal-lingually before calcikation mediodistally is completed. Occlusal view.
MESIAL
CALCIFICATION
LINGUAL
FUSION
FIG. 6. Diagram of the calcification pattern of the right fourth mandibular molar. This shows the greatest complexity of form in swine teeth, with multiple centres of calcification, fusion of cusps buccal-lingually, and later fusion mek-distally.
CALCIFICATION
PAlTERN
IN MINIATURE
SWINE
TEETH
645
initial cusp calcification. The letters correspond to the order of successive fusions between the areas of calcification in the direction indicated by the arrows. As with the maxillary fourth molar, there was calcification or bridging between adjacent buccal and lingual cusps prior to fusion of calcified areas in a mesio-distal axis. As in man, the first permanent molars began mineralization with the deciduous dentition, much earlier than the other permanent teeth and therefore, are being described in this report. The maxillary tist molar was quadrangular. The order of cuspal calcification was mesio-buccal (91 days), mesio-lingual (95 days), disto-buccal MESIAL
DISTALm3
weeks 3
m4
m4
m3
m4
m3 m’3
m4
m2
7 m3
m4
m2
8 m4
m3 m3
m4
m2
m2
IO m4
FIG.7.The eruption and occlusal
m3
m2
pattern of the deciduous teeth, which in fact mirrors
the calcification sequence. The shaded teeth or parts thereof appear in the mouth for the tirst time at the specified ages.
(105 days), and disto-lingual (newborn). At birth none of the cusps had fused with each other. The mandibular permanent fkst molar also had four major calcification centres but had several minor ones as well. Since the tooth was only partially formed at birth, mention will be limited to the quadrangle of the four major centres. The mesial cusps were present fist (91 days), followed by both distal cusps (100 days). At birth only the anterior pair of cusps had fused.
646
Cnmm
F. MCKEAN,E. B. JUMP AND M. E.
WEAVER
DISCUSSION
The data demonstrated that the pig does not have a progressive antero-posterior sequence of calcification. For example, Table 1 indicates that in our material the deciduous canines began to calcify prior to any incisors and the more posterior deciduous molars were initiated earlier than the more anterior molars. This observation concurs with BUTLER’Sgeneralization (1963) that a common belief that tooth buds develop in serial order antero-posteriorly is nearly true in man but does not apply to mammals generally. Comparison of the sequence of calcification with the sequence of eruption (Fig. 1) shows that within the incisor and molar groups of teeth the sequences are the same. However, the eruption sequence does not parallel the calcification sequence when considering all the teeth together. This demonstrates that the rate of growth is not the same for all teeth, one of the features associated with “tooth districts” (DAHLBERG, 1945) or the “field theory of development” (BUTLER,1939) along with differences in size and morphology. The rate of growth within groups of teeth may indicate the difference in “tooth districts” but a more basic explanation may be the time of initial development. Figure 1 shows that the lapsed time from initial calcification to eruption is much less for teeth which develop early, e.g. I,, than for teeth of the same “tooth district” which start calcifying later, as I, or 12. Other teeth which have an early origin but which are larger in size, e.g. m3 or m4, have a long period of development because of size, but require less time than similar or smaller teeth that begin development later, as m2. This may reflect the declining rate of growth with increasing foetal or post-natal age that is typical of organ systems and body growth in general. Concerning the relationship of calcification time and the size of teeth, our data present some exceptions to the statement that from the initial cheek teeth forward the most precocious tooth germs develop into the largest teeth (BUTLER, 1963). The earliest tooth germs produce the canine and the third incisor in the pig, which are much smaller than the first incisor which appears subsequently. However, there is some agreement of our data to the specific examples used when this rule was tist stated by LECHEin 1895 (from BUTLER,1963). This consideration was a comparison between the S.rst and second incisor, which in the pig, as in man and many other mammals, the more precocious first incisor becomes a much larger tooth. The rule as stated applies best to animals with a dental formula reduced in number from the “original mammalian number” which included a third incisor as present in the pig. Just as the morphology of the tooth is associated with its location in the arch rather than its position in the sequence of eruption, (the field concept of development of BUTLER,1939), so also must the size of the tooth be associated with the location in the arch rather than the time of initial calcification. With regard to the calcification within teeth, this report also concurs with the findings in human teeth of KRAUS (1959), that calcification of deciduous anterior teeth always starts from a single centre regardless of whether or not the crown possesses mammelons or cingula. In this study the dental calcification was first
CALCIFICATIONPATI'ERNINMNIATURESWINETEETH
647
observed at an age corresponding to 46 per cent of the gestation period compared with the corresponding time in man of 32 per cent normal term gestation (-us, 1959). The shape of the uncalcsed tooth in primates (BUTLER, 1963) as well as the number of cusps and sequence of fusion of the calcified centres within the tooth of rhesus (SWINDLER and MCCOY, 1964), and man (TURNER,1963), (Klaus and JORDAN, 1965), has been reported to reflect the genetic control of tooth formation. This would account also for the close similarity within our small sample. The similarity of cusp formation and coalescence in the maxillary fourth molar of the pig and the first molar of rhesus (SWINDLERand MCCOY, 1964) or man (Klaus and JORDAN,1965) may indicate a basic genetic pattern for all mammalian teeth of a certain type and cusp number. Functional occlusion was established initially between the maxillary third molar and the mandibular fourth molar, shown diagrammatically in Fig. 7. As the jaws elongate with growth, additional deciduous teeth erupt or additional cusps erupt into function both anterior and posterior to the first occlusal contact. Thus the masticatory area increases in both directions, while simultaneously additional teeth are erupting in the anterior part of the arch to produce a balanced, functional dental apparatus. Comparison of our data with the dental calcification chronology of domestic swine is based on a preliminary report by MCCLURE (1966). His sample included several domestic breeds from an abattoir source and only the earliest calcification times were reported. He indicated no difference between the calcification sequence of the deciduous teeth in the maxillary and mandibular arches. Our corresponding data shows a definite variation in pattern. In our study the maxillary third incisor, canine and third molar all began to calcify between 51 and 55 days, well ahead of the fourth molar whereas the mandibular canine, fourth molar, and first and third incisor develop in the interval between 55 and 61 days (Table 1). There are several possible explanations for the differences: genetic variation, method of age determination, criteria for determining initial calcification, etc. This report has presented normal data from a series of precisely aged foetuses of miniature pigs to indicate their calcification chronology. Comparisons were presented between eruption sequences previously published, and the present data on the initiation and progress by cusps of mineralization of the primary dentition of this promising laboratory animal. Acknowledgement-This study was supported in part by U.S.P.H.S. research grant DE 01514-05 from the National Institutes of Dental Research, National Institutes of Health. R&urn&-Trentehuit foetus de “port miniature” Pitman-Moore,
obtenus par cksariene, a divers stades in ufero, sont color& au rouge d’alizarine S pour etudier la calcikation, dont le debut et le developpcment sont not& pour chaque dent et pour l’enscmble de I’arcade dentaire. Lc debut de calciikation dentaire se developpe de la meme facon que l’tkuption des incisives et molaires temporaires chez le “port miniature”. Le nombre des centres de calcification varie avcc les divers types de dents. 11 n’y a pas de centres de calcification differems pour les cuspides. Le debut et l’ordre de calcification des cuspides semblent differents de ceux des dents du port domestique.
648
CYNTHIAF. MCKEAN, E. B. JUMP AND M. E. WEAVER Le developpement de la calcification des dents dune arcade ne s’effectue pas de l’avant vets l’arri&e, comme chez la plupart des mammiferes, mais est dierent pour chaque arcade. Le mode de developpement de la calcitication, dans certaines dents, parait similaire 21celui des primates et des humaines, pouvant indiquer un controle genetique possible de la formation des dents chez les mammifi%es. Zusammenfassang-38 Feten des Pitman-Moore-“Miniaturschweins” wurden in verschiedenen Altersstufen in utero operativ gewonnen und mit Alizarinrot angefarbt, um die Mineralisation zu demonstrieren. Zeitpunkt und Aufeinanderfolge der Verkalktmgsvorgange wurden fi.ir jeden Zahn festgestellt, ebenso der Verkalkungsablauf innerhalb jeden Zahnbogens. Die erste Verkalkung von Zahnen trat in der gleichen Reihenfolge auf, wie sie fur den Durchbruch der Milchschneidezahne und Molaren beim “Miniaturschwein” beschrieben worden war. Die Anzahl der Mineralisationskeme schwa&e bei den verschiedenen Zahntypen. Fiir die Hiicker gab es keine getrennten Kalzifikationszentren. Zeitpunkt und Aufeinanderfolge der Mmeralisation wurden ftir die H&cker aller Z&ne bestimmt; sie unterschieden sich etwas von den Berichten iiber die Zi%hne des Hausschweins. Die Verkalkungsfolge der Z&ne innerhalb des Zahnbogens verlief nicht, wie friiher ftir ssiugetiere verallgemeinert, von anterior nach posterior, sondem sie ergab ein unterschiedliches, ftir jeden Zahnbogen typisches Bild. Der Mineralisationsablauf innerhalb bestimmter ziihne ergab Ahnlichkeiten zu Berichten tiber Primaten und Menschen, was auf die Moglichkeit eines allgemeinen Prinzips einer genetischen Kontrolle der Zahnentwickhmg bei SSiugetieren hinweist.
REFERENCES BUTLER, P. M. 1963. Tooth morphology and primate BROTHWELLD. R.) Pergamon Press, Oxford.
evolution.
Dental Anthropology (edited by
DAHLBERG,A. A. 1945. The changing dentition of man. J. Am. dent. Ass. 32, 676-690 GAUNT, W. A. 1959. The development of the deciduous cheek teeth of the cat. Acta Anat. 38,187-212. LEGROS,C. and MAGITOT,E. 1880. Origin and Formation of the Dental Follicle. (Translation by M. S. Dean) Jansen, McClurg 8c Co., Chicago. KRAUS, B. S. 1959. Calcification of the human deciduous tee0 /. Am. dent. &. 59(6), 1128-1136. KRAUS, B. S. and JORDAN,R. E. 1965.7% Human Dentition Bejiire Birth. Lea & Febiger, Philadelphia. MCCLURE, R. C. 1966. Preliminary studies of the development, calcitlcation and eruption of the deciduous teeth in domestic swine. Anat. Rec. 154(2), 385. NOBACK, C. R., and NOBACK,E. 1944. Demonstrating the osseous skeleton of human embryos and fetuses. Stain Technol. 19, 51-53. ORBAN, B. J. 1957. Oral Histology and Embryology (4th edn). C. V. Mosby Co., St. Louis. SCHOUR,I. 1953. Noyes’ Oral Histology and Embryology (7th edn). Lea & Febiger, Philadelphia. SWLNDLER,D. R. and McCoy, H. A. 1964. Calcification of deciduous teeth in rhesus monkeys. Science 144,1243-M. TURNER, E. P. 1963. Crown development in human deciduous molar teeth. Archs oral Biol. 8, 523-540. WEAVER, M. E., JUMP E. B. and MCKEAN, C. F. 1966. The eruption pattern of deciduous teeth in miniature swine. Anat. Rec. 154(l), 81-86.
THE CALCIFICATION PATTERN OF DECIDUOUS TEETH IN MINIATURE SWINE CYNTHIAF. MCKEAN, E. B. JUMPand M. E. WEAVER University of Oregan Dental School, Department of Anatomy, 611 S.W. Campus Drive, Portland, Oregon 97201, U.S.A. Summary-Thirty-eight foetuses of Pitman-Moore “miniature swine” were obtained at different ages in utero by caesarean section and stained with alizarin red S to show calcification. The time and sequence of cakihcation was noted for each tooth and the pattern of calcification within each dental arch as well. Initial calcification of teeth occurred in the same pattern reported for eruption of deciduous incisor and molar teeth in “miniature swine”. The number of calcif?cation centres varied with different types of teeth. There were no separate calcification centres for mammelons. The time and sequence of calcitication were noted for cusps of all teeth and differed somewhat from reports for teeth of domestic swine. The sequence of calcification of teeth within each arch was not from anterior to posterior as often generalized for mammals, but was a different, distinct pattern for each arch. The sequence of calcification within certain teeth exhibited similarities to reports for primates and man, indicating a possible basic genetic control of tooth formation for mammals in general.
FOR MANYyears dental scientists stated that the calcification of deciduous teeth in mammals occurred in a rigid pattern beginning mesially with the fist incisor and progressing distally until finally the last deciduous molar was calcified (LEGROSand MAGITOT, 1880; SCHOUR,1953; ORBAN, 1957). Perusal of the literature, however, revealed little evidence to substantiate such an idea and more recent reports deny this is the sequence in the cat (GAUNT, 1959), the rhesus monkey (SWINDLERand MCCOY, 1964), or even in man (KRAUS, 1959). This study was concerned with the chronology and sequence of dental calcification in Pitman-Moore miniature swine and possible relationships between calcification and eruption. MATERIALS
AND
METHODS
Thirty-eight foetuses were obtained by caesarian section at 19 different stages of gestation ranging from 32 days post-insemination to term (112 & 2 days). Upon removal from the uterus the foetuses were placed immediately in 10 per cent formalin. After adequate fixation, the two specimens of each age were decapitated and the heads were bisected in the midsagittal plane. The right halves were roentgenographed, stained with alizarin red S, and stored in glycerin (NOBACK and NOBACK, 1944). The left halves of the heads were retained for histological study, the data from which will be presented later as a separate report. All of the toothbuds from the right halves of the heads were excised under the dissecting microscope at a magnitication of 20 x . Newborn specimens were dissected first to permit better orientation. Subsequently, as the younger specimens were examined, we could still identify specific tooth germs even before dental mineralization began. Working drawings of each toothbud were made as it was removed from the dental crypt. These drawings facilitated reorientation of specific teeth at a later time. 639
640
F.
CYNTHIA
MCKEAN,
E. B. JUMP AND M. E. WEAVER
The time of initial calcification, as indicated by the alixarin stain, was recorded for each tooth. The following procedure was developed in order to record also the pattern of calcification for each tooth type: (1) Compare by inspection the cleared tooth germs of each tooth type in both animals at a particular age. (2) Photograph one of each type specimen at each age in buccolingual or occlusal projection while the specimen was suspended in glycerol, using both transmitted and incident illumination. Occlusal projections best depict the teeth with multiple cusps. (3) Prepare enlarged tracings of negative images of the calcified zone of a given tooth at successive foetal ages. (4) Produce an artist’s composite drawing of each tooth, using the enlarged tracings from the developmental stages with the cusp tip and axial line of cusp as the registration determinants for superposition. OBSERVATIONS
Typically, P&man-Moore miniature swine have the same deciduous dental formula i3, c, m4 as do commercial swine: However, we have reported that one tooth, the i3, c, m4 . lower first deciduous molar, was usually missing in our miniature swine (WEAVER, JUMP and MCKEAN, 1966). The time and sequence of initial calcification in deciduous teeth is presented in TABLE 1.
CALCIFICATION
FORMULA
FOR
OF A TOOTH
BEOAN
PARENTHESES,
IS
INCISOR,
INDICATED
CANINB,
AND
BY MOLAR
SYMBOLS
FROM
TEETH.
WHEN
AT DIFFERENT
AGES, ITS FIRST APPEARANCE
WHEN
CALCIFICATION
BUT
IN BOTH
SOME
SPECIMENS
SHOWED
NO PARBNTHESES
WBRE
THE
IS INDICATED
IN A GNEN USED
N ITIAL CALCIFICATION OF MINIATURE SWINE DENTITION I
DAYS GESTATION 49 51 53 55 58 61 65 70 75 80 85 91 95 100 105 112 (newborn)
MAXILLA
MANDIBLE
-
-
c,
(m3) (i 31,m3 i3 il, m4 m2 (Ml) Mi i2
C -
(m4) (ill,(i3), m4 m3, il, i3 ‘i2 m2, Ml -
DENTAL
CALCIFICATION IN
TOOTH
CALCIFlCATiON
PATTERN
Table 1. Dental calcification began mineralization was noted throughout molars which develop and calcify teeth showing calcification at birth
IN MINIATURE
SWINE
TEETH
641
at 51 days in utero and at birth some degree of the primary dentition except in the first deciduous after birth, when present. The only permanent were the upper and lower first molars. Figure 1
CALCIFICATION AND ERUPTiON OF DECIDUOUS DENTITION
i 1i 2i 3c m2m3m4-
A Calcification a
Eruption
FIG. 1. Initial calcifkation of individual teeth was approximated to weekly intervals from the data and is compared with eruption times reported for these teeth (WEAVER, JUMP and MCKIZAN, 1966).
compares initial calcification of the deciduous teeth with the eruption time reported for those same teeth (WEAVER et al., 1966). The left end of each bar, marked with the
triangle, represents the mean age at which corresponding teeth in both specimens showed evidence of calcification. Conversely, the right end of each bar, marked with the dark circle, represents the mean age reported for the clinical eruption of that tooth. A vertical line placed along the abscissa at any desired age between 7 weeks in uiero and 11 weeks post partum will intersect bars of those teeth undergoing calcification at that age. The length of the bar representing a particular tooth indicates the number of weeks elapsed between the beginning of calcification and the eruption of that tooth into the mouth and allows an easy comparison of the developmental history of different teeth. With respect to calcification of teeth, several different basic patterns became apparent, ranging from a single centre of calcification to as many as six major calcification centres. All of the anterior teeth had single centres of calcification. The third incisors and canines developed smooth conical teeth without any evidence of cingula or accessory cusps. The G.rst deciduous incisors in both arches and the mandibular second incisors did exhibit mammelons. However, in each case calcification began at the tip of the central mammelon and gradually enveloped the rest of the tooth (Fig. 2). There were no mammelons associated with the second maxillary incisors. A.O.B. S/~--P
CYNTHIAF. MCKEAN,E. B. JUMPANDM. E. WEAVER
642
r
Mesial
)--c
Distal
Days
gestation 61
mm 70 91 (
1 Newborn
FIG. 2. The right mandibular fkst incisor exhibits three mammelons, the central one being the site of initial calci6caCon for the tooth. Other single cusp teeth ditkr slightly in shape but exhibit the same developmental pattern, without mammelons.
Another type of tooth showing a single centre of calcification was trilobate in form and included both maxillary and mandibular second deciduous molars (Fig. 3). Each of these tooth germs developed two or more cusps in a linear arrangement in the mesio-distal axis of the tooth. In each instance calcification began with the central Mesial Days
-
Distal
gestation
mm
right maxillary second molar has a single calcification centre but develops multiple cusps. Buccal or lateral view, with occlusal surface upward.
FIG. 3. The
CALCIFICATION
PATI-ERN
IN MINIATURE
SWINE
TEETH
643
cusp and progressed both anteriorly and posteriorly until the other cingulate cusps were completed. We therefore grouped these particular deciduous molars with the mammelon-forming incisors on the basis of similar development. The rest of the deciduous teeth had multiple calcification centres. The simplest arrangement of these was in the mandibular third molar which seemed to represent a transition from single to multiple centres of calcification. It had a linear arrangement of its cusps as did the second molars. Calcification in this tooth was first noted for the major cusp at 61 days followed by minor cusp formation. A second more distal centre developed at 65 days and fused with the first cusp at 70 days. At this age, calcification had also progressed mesially toward a third cusp. Finally, calcification appeared in yet a fourth cusp of the tooth at 80 days and was fused with the rest of the calcified crown of the tooth 5 days later. The maxillary third molar had three separate calcification centres, which developed at different times as indicated in Fig. 4. Instead of the linear cuspal arrangement, which was noted in the mandibular third molar, its occlusal outline roughly formed an isosceles triangle, the apex of which was anterior or mesial. The mesial cusp was the most prominant and the Grst to calcify. Figure 5 shows the quadrangular form of the maxillary fourth deciduous molar. Its calcification progressed from four centres beginning with the mesio-buccal cusp at 61 days. The mandibular fourth molar presented the most complex form of the deciduous dentition. This crown consisted of six major cusps and at least two minor ones, all of which appeared as separate calcification centres. The details of its formation have been summarized in a diagram (Fig. 6). The figures within the circles represent the order of Mesial
Days gestation 55
Buccal
q Newborn Fro. 4. The right maxillary third molar developsfrom three separate cenkzs of calcification, beginning at different ages. Occlusal view.
-
F. MCKEAN,E. B. JUMPAND M. E. WEAVER
r
Mesial
Days
gestation 61 65
70-75 lllllllllll
mm
a
s
=I= __
85
95
cl Newborn FIG. 5. The right fourth maxillary molar develops from four centres of calcification which begin at diierent ages and fuse buccal-lingually before calcikation mediodistally is completed. Occlusal view.
MESIAL
CALCIFICATION
LINGUAL
FUSION
FIG. 6. Diagram of the calcification pattern of the right fourth mandibular molar. This shows the greatest complexity of form in swine teeth, with multiple centres of calcification, fusion of cusps buccal-lingually, and later fusion mek-distally.
CALCIFICATION
PAlTERN
IN MINIATURE
SWINE
TEETH
645
initial cusp calcification. The letters correspond to the order of successive fusions between the areas of calcification in the direction indicated by the arrows. As with the maxillary fourth molar, there was calcification or bridging between adjacent buccal and lingual cusps prior to fusion of calcified areas in a mesio-distal axis. As in man, the first permanent molars began mineralization with the deciduous dentition, much earlier than the other permanent teeth and therefore, are being described in this report. The maxillary tist molar was quadrangular. The order of cuspal calcification was mesio-buccal (91 days), mesio-lingual (95 days), disto-buccal MESIAL
DISTALm3
weeks 3
m4
m4
m3
m4
m3 m’3
m4
m2
7 m3
m4
m2
8 m4
m3 m3
m4
m2
m2
IO m4
FIG.7.The eruption and occlusal
m3
m2
pattern of the deciduous teeth, which in fact mirrors
the calcification sequence. The shaded teeth or parts thereof appear in the mouth for the tirst time at the specified ages.
(105 days), and disto-lingual (newborn). At birth none of the cusps had fused with each other. The mandibular permanent fkst molar also had four major calcification centres but had several minor ones as well. Since the tooth was only partially formed at birth, mention will be limited to the quadrangle of the four major centres. The mesial cusps were present fist (91 days), followed by both distal cusps (100 days). At birth only the anterior pair of cusps had fused.
646
Cnmm
F. MCKEAN,E. B. JUMP AND M. E.
WEAVER
DISCUSSION
The data demonstrated that the pig does not have a progressive antero-posterior sequence of calcification. For example, Table 1 indicates that in our material the deciduous canines began to calcify prior to any incisors and the more posterior deciduous molars were initiated earlier than the more anterior molars. This observation concurs with BUTLER’Sgeneralization (1963) that a common belief that tooth buds develop in serial order antero-posteriorly is nearly true in man but does not apply to mammals generally. Comparison of the sequence of calcification with the sequence of eruption (Fig. 1) shows that within the incisor and molar groups of teeth the sequences are the same. However, the eruption sequence does not parallel the calcification sequence when considering all the teeth together. This demonstrates that the rate of growth is not the same for all teeth, one of the features associated with “tooth districts” (DAHLBERG, 1945) or the “field theory of development” (BUTLER,1939) along with differences in size and morphology. The rate of growth within groups of teeth may indicate the difference in “tooth districts” but a more basic explanation may be the time of initial development. Figure 1 shows that the lapsed time from initial calcification to eruption is much less for teeth which develop early, e.g. I,, than for teeth of the same “tooth district” which start calcifying later, as I, or 12. Other teeth which have an early origin but which are larger in size, e.g. m3 or m4, have a long period of development because of size, but require less time than similar or smaller teeth that begin development later, as m2. This may reflect the declining rate of growth with increasing foetal or post-natal age that is typical of organ systems and body growth in general. Concerning the relationship of calcification time and the size of teeth, our data present some exceptions to the statement that from the initial cheek teeth forward the most precocious tooth germs develop into the largest teeth (BUTLER, 1963). The earliest tooth germs produce the canine and the third incisor in the pig, which are much smaller than the first incisor which appears subsequently. However, there is some agreement of our data to the specific examples used when this rule was tist stated by LECHEin 1895 (from BUTLER,1963). This consideration was a comparison between the S.rst and second incisor, which in the pig, as in man and many other mammals, the more precocious first incisor becomes a much larger tooth. The rule as stated applies best to animals with a dental formula reduced in number from the “original mammalian number” which included a third incisor as present in the pig. Just as the morphology of the tooth is associated with its location in the arch rather than its position in the sequence of eruption, (the field concept of development of BUTLER,1939), so also must the size of the tooth be associated with the location in the arch rather than the time of initial calcification. With regard to the calcification within teeth, this report also concurs with the findings in human teeth of KRAUS (1959), that calcification of deciduous anterior teeth always starts from a single centre regardless of whether or not the crown possesses mammelons or cingula. In this study the dental calcification was first
CALCIFICATIONPATI'ERNINMNIATURESWINETEETH
647
observed at an age corresponding to 46 per cent of the gestation period compared with the corresponding time in man of 32 per cent normal term gestation (-us, 1959). The shape of the uncalcsed tooth in primates (BUTLER, 1963) as well as the number of cusps and sequence of fusion of the calcified centres within the tooth of rhesus (SWINDLER and MCCOY, 1964), and man (TURNER,1963), (Klaus and JORDAN, 1965), has been reported to reflect the genetic control of tooth formation. This would account also for the close similarity within our small sample. The similarity of cusp formation and coalescence in the maxillary fourth molar of the pig and the first molar of rhesus (SWINDLERand MCCOY, 1964) or man (Klaus and JORDAN,1965) may indicate a basic genetic pattern for all mammalian teeth of a certain type and cusp number. Functional occlusion was established initially between the maxillary third molar and the mandibular fourth molar, shown diagrammatically in Fig. 7. As the jaws elongate with growth, additional deciduous teeth erupt or additional cusps erupt into function both anterior and posterior to the first occlusal contact. Thus the masticatory area increases in both directions, while simultaneously additional teeth are erupting in the anterior part of the arch to produce a balanced, functional dental apparatus. Comparison of our data with the dental calcification chronology of domestic swine is based on a preliminary report by MCCLURE (1966). His sample included several domestic breeds from an abattoir source and only the earliest calcification times were reported. He indicated no difference between the calcification sequence of the deciduous teeth in the maxillary and mandibular arches. Our corresponding data shows a definite variation in pattern. In our study the maxillary third incisor, canine and third molar all began to calcify between 51 and 55 days, well ahead of the fourth molar whereas the mandibular canine, fourth molar, and first and third incisor develop in the interval between 55 and 61 days (Table 1). There are several possible explanations for the differences: genetic variation, method of age determination, criteria for determining initial calcification, etc. This report has presented normal data from a series of precisely aged foetuses of miniature pigs to indicate their calcification chronology. Comparisons were presented between eruption sequences previously published, and the present data on the initiation and progress by cusps of mineralization of the primary dentition of this promising laboratory animal. Acknowledgement-This study was supported in part by U.S.P.H.S. research grant DE 01514-05 from the National Institutes of Dental Research, National Institutes of Health. R&urn&-Trentehuit foetus de “port miniature” Pitman-Moore,
obtenus par cksariene, a divers stades in ufero, sont color& au rouge d’alizarine S pour etudier la calcikation, dont le debut et le developpcment sont not& pour chaque dent et pour l’enscmble de I’arcade dentaire. Lc debut de calciikation dentaire se developpe de la meme facon que l’tkuption des incisives et molaires temporaires chez le “port miniature”. Le nombre des centres de calcification varie avcc les divers types de dents. 11 n’y a pas de centres de calcification differems pour les cuspides. Le debut et l’ordre de calcification des cuspides semblent differents de ceux des dents du port domestique.
648
CYNTHIAF. MCKEAN, E. B. JUMP AND M. E. WEAVER Le developpement de la calcification des dents dune arcade ne s’effectue pas de l’avant vets l’arri&e, comme chez la plupart des mammiferes, mais est dierent pour chaque arcade. Le mode de developpement de la calcitication, dans certaines dents, parait similaire 21celui des primates et des humaines, pouvant indiquer un controle genetique possible de la formation des dents chez les mammifi%es. Zusammenfassang-38 Feten des Pitman-Moore-“Miniaturschweins” wurden in verschiedenen Altersstufen in utero operativ gewonnen und mit Alizarinrot angefarbt, um die Mineralisation zu demonstrieren. Zeitpunkt und Aufeinanderfolge der Verkalktmgsvorgange wurden fi.ir jeden Zahn festgestellt, ebenso der Verkalkungsablauf innerhalb jeden Zahnbogens. Die erste Verkalkung von Zahnen trat in der gleichen Reihenfolge auf, wie sie fur den Durchbruch der Milchschneidezahne und Molaren beim “Miniaturschwein” beschrieben worden war. Die Anzahl der Mineralisationskeme schwa&e bei den verschiedenen Zahntypen. Fiir die Hiicker gab es keine getrennten Kalzifikationszentren. Zeitpunkt und Aufeinanderfolge der Mmeralisation wurden ftir die H&cker aller Z&ne bestimmt; sie unterschieden sich etwas von den Berichten iiber die Zi%hne des Hausschweins. Die Verkalkungsfolge der Z&ne innerhalb des Zahnbogens verlief nicht, wie friiher ftir ssiugetiere verallgemeinert, von anterior nach posterior, sondem sie ergab ein unterschiedliches, ftir jeden Zahnbogen typisches Bild. Der Mineralisationsablauf innerhalb bestimmter ziihne ergab Ahnlichkeiten zu Berichten tiber Primaten und Menschen, was auf die Moglichkeit eines allgemeinen Prinzips einer genetischen Kontrolle der Zahnentwickhmg bei SSiugetieren hinweist.
REFERENCES BUTLER, P. M. 1963. Tooth morphology and primate BROTHWELLD. R.) Pergamon Press, Oxford.
evolution.
Dental Anthropology (edited by
DAHLBERG,A. A. 1945. The changing dentition of man. J. Am. dent. Ass. 32, 676-690 GAUNT, W. A. 1959. The development of the deciduous cheek teeth of the cat. Acta Anat. 38,187-212. LEGROS,C. and MAGITOT,E. 1880. Origin and Formation of the Dental Follicle. (Translation by M. S. Dean) Jansen, McClurg 8c Co., Chicago. KRAUS, B. S. 1959. Calcification of the human deciduous tee0 /. Am. dent. &. 59(6), 1128-1136. KRAUS, B. S. and JORDAN,R. E. 1965.7% Human Dentition Bejiire Birth. Lea & Febiger, Philadelphia. MCCLURE, R. C. 1966. Preliminary studies of the development, calcitlcation and eruption of the deciduous teeth in domestic swine. Anat. Rec. 154(2), 385. NOBACK, C. R., and NOBACK,E. 1944. Demonstrating the osseous skeleton of human embryos and fetuses. Stain Technol. 19, 51-53. ORBAN, B. J. 1957. Oral Histology and Embryology (4th edn). C. V. Mosby Co., St. Louis. SCHOUR,I. 1953. Noyes’ Oral Histology and Embryology (7th edn). Lea & Febiger, Philadelphia. SWLNDLER,D. R. and McCoy, H. A. 1964. Calcification of deciduous teeth in rhesus monkeys. Science 144,1243-M. TURNER, E. P. 1963. Crown development in human deciduous molar teeth. Archs oral Biol. 8, 523-540. WEAVER, M. E., JUMP E. B. and MCKEAN, C. F. 1966. The eruption pattern of deciduous teeth in miniature swine. Anat. Rec. 154(l), 81-86.