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Dietary fluoride uptake into the enamel of caries-susceptible “yellow” permanent teeth and of caries-resistant permanent and primary teeth of polynesians
Archs oral Bid. Vol. 15,pp.431443,1970. Pergamon Press.Printedin GreatBritain.
DIETARY FLUORIDE UPTAKE INTO THE ENAMEL OF CARIES-SUSCEPTIBLE “YELLOW” PERMANENT TEETH AND OF CARIES-RESISTANT PERMANENT AND PRIMARY TEETH OF POLYNESIANS L. J.
BAUME
and
J.-P. VULLI~MOZ
South Pacific Commission-Noumea, New Caledonia School of Dental Medicine, Medical Faculty, University of Geneva Switzerland Sunnnary-Within the frame of a dental and dietary survey, 95 shed and extracted intact teeth were collected from three groups of Polynesians of a known caries intensity for determination of the fluoride concentration in the enamel. The first group consisted of “yellow” highly caries-susceptible permanent teeth of young Tahitians; the second group comprised slightly fluorosed caries-resistant permanent teeth of schoolchildren and adults of the Austral Islands (French Polynesia) and Savaii (Western Samoa), including some teeth from pre-colonial skulls; the third group was composed of shed second primary molars of Savaiian children. The fluoride concentration was determined for the enamel in toto (Groups 1 and 2) and for successive surface layers (Groups 2 and 3) by tests carried out by well-calibrated laboratories. Enamel of young “yellow” teeth contained only half the concentration (51 ppm) of their caries-resistant counterparts. Older caries-resistant teeth showed a higher average concentration (140 ppm) reflecting a continuous post-eruptive accumulation of fluoride; brown mottled teeth (300 ppm) ranked highest; pre-colonial young ones matched the modem counterparts in fluoride concentration. Analysis of the surface layer of caries-resistant permanent teeth showed increasingly higher concentrations with advancing age, averaging in the outermost surface layer of young permanent teeth 2222 ppm, and 4517 in the older ones. The higher the surface concentration, the steeper was the decrease within the iirst tenth of millimetre depth measured. It was shown that, with no fluoridation measure other than dietary fluorides, concentrations as high as 6960 ppm have been reached in the enamel without untoward aesthetic and systemic effects. Primary second molars drawn from the same population sample, on the other hand, showed strikingly lower surface concentrations-on the average 4-times less than permanent teeth of corresponding age. The values decreased little with progressive depth. The reasons for this phenomenon are discussed. It reflected the relatively greater caries suceptibility of primary teeth of Polynesian populations showing a low caries frequency in the permanent teeth. Hence the remarkable caries resistance through life recorded in some isolated Polynesian collectivities was associated with a continuous topical enrichment of the enamel of their permanent teeth with dietary fluorides in extremely high quantities.
INTRODUCTION
A DENTAL survey of the school population of French Polynesia revealed marked differences in the geographic distribution of caries attack in the permanent teeth (BAUME, 1969). Tahitians, on the one hand, showed a prevalence of 90 per cent and 431
432
L. J. BAUM~ ANDJ.-P. V~JLL&MOZ
an average intensity rate of 12 DMF teeth per person at the age of 15. Pupils of the remote Austral Islands, on the other hand, remained for the most part caries-free, showing an average attack rate of 3 DMF teeth at the age of 14. Among Tahitians a condition called “yellow teeth” proved to be particularly vulnerable to early rampant decay (VULLIEMOZ and BAUME,1966). Dietary surveys pointed to a possible background of malnutrition characterized by an excessive intake of refined (imported) carbohydrates and an insufficient consumption of foods containing calcium and protein (BAUME,1965). Children in the Austral Islands who still adhered to the traditional Polynesian diet absorbed, through the consumption of fish, taro and coconut, sufficiently high quantities of fluorides so that slight to moderate fluorosis of the permanent teeth was a predominant feature. A recent survey carried out among 10,000 inhabitants of Western Samoa showed that an identical condition of a high caries resistance associated with slight enamel fluorosis also prevailed among the inhabitants of the island of Savaii (BAUME,1968). The primary teeth of the French Polynesian children, on the other hand, showed little difference in caries intensity when the results were tabulated by geographic location. The average d.f. rate at the age of 5 was 7.5 in Tahitians and 5 *Oin children in the Austral Islands. Similar lowered caries resistance in the primary teeth has been reported from other isolated Polynesian communities (BARMES,1967). These variations in caries susceptibility of the permanent teeth by geographic location on the one hand, and of primary and permanent teeth on the other, among persons of the same closed populations have been related to host factors including the chemical and physical composition of the teeth as determined by diet and nutrition (DAVIES, 1965). An attempt was made therefore to collect samples of intact teeth which, according to related epidemiological data, were representative of distinct caries-resistant and caries-susceptible groups. In an earlier series of studies, the histopathological aspects of specific conditions such as infantile “melanodontia” and “odontoclasia” as well as “yellow permanent teeth” have been reported (BAUMEand MEYER, 1966). In this second series of studies, quantitative analyses of the fluoride and mineral content of three samples of teeth of caries-susceptible and caries-resistant groups were assessed. It is the purpose of the present pilot study to report on data of the fluoride concentration of the enamel, and to discuss its relation to dietary fluorides. MATERIAL AND METHODS The three samples of caries-free teeth were constituted as follows : Group 1 of highly caries-susceptible permanent teeth. This group was composed of 18 yellow teeth from Tahitian schoolchildren between the ages of 10 and 18 years which exhibited the characteristics described by VULLIEMOZand BAUME(1966). The portions not used for median ground sections of 8 caries-free yellow teeth were used for fluoride analyses of the enamel in toto. Group 2 of caries-resistant permanent teeth. This group was composed of 38 incisors and molars showing signs of very slight to slight fluorosis of the enamel l&-2* according to the scale of MILLER (1965), and two with brown discolourations (scale 3). They were divided into two subgroups according to the age of the patients:
PERhfANEW AND PRIMARY TEETH OF POLYNESIANS
433
(a) Fifteen teeth of younger persons between the ages of 10 and 20 yr: 6 teeth from Savaii were analyzed for the fluoride content of the entire enamel and 5 teeth from Savaii and the Austral Islands respectively for analysis of fluoride uptake by successive layers. Four molars removed from skulls found on Makatea (Tuamotu) were analyzed by Dr. MCCLURE. (b) Twenty-three teeth of persons over the age of 30 yr who were suffering from advanced periodontal diseases: 8 from Savaii were used for total fluoride determination and 15 (9 from Savaii, 6 from the Austral Islands) for fluoride assay of successive layers of the enamel surface. Group 3 of caries-resistant primary teeth. This group included 39 shed primary second molars from children of Savaii. These teeth were used exclusively for analysis of the fluoride content of successive layers. Records of the teeth selected at random in each group included both macrophotographs in black and white as well as in colour made with a Nikon equipment and 2 radiographs of both the mesiodistal and buccolingual aspects made with a dental X-ray machine. For the determination in toto, the F separation method by diffusion of BWMLER and GLINZ (1964), modified according to NEWESELY(personal communication), was applied. The final calorimetric F determination using alizarin complexan was carried out according to the method of QUENTIN(1965). These analyses were supervised by H. NEWESELY. For the analysis of fluoride in successive layers of external enamel, the crowns were first cleaned with pumice applied by an electrical toothbrush for 1 min. Then the roots and the marginal third of the crowns were covered with wax. Afterwards, in order to remove successive enamel layers the crowns were exposed separately and successively to 5 ml 2%perchloric acid. Exposure times were 5, 10 and 15 set, and two sequences of 3 x 15 sec. After each demineralization, the crowns were washed with 5 ml of distilled water which were added to the perchloric acid solution. Each demineralizing solution was analyzed for phosphorus and fluoride according to methods described by M~~HLEMANN, SCHAITand KOENIG (1964) who performed the analyses. Since the roots of the primary molars were absent owing to resorption some difficulties arose in the performance of micromeasurements of layer thickness. The ratio of “dissolved microlayer” and “total of phosphorus” in the diffusate varied between 4.9 and 29 *3. The average ratio gained from 40 measurements was 11.4. This value was used for the calculations of the layer thickness according to the phosphorus content of the diffusate. For these reasons, a relatively larger sample of primary molars was assayed. RESULTS Data of fluoride concentration of the total enamel are shown in Table average of Group 1 “yellow teeth” was 51 f 14 ppm, the lowest figure being the highest 65 ppm. Caries-resistant enamel of the younger Group 2a contained twice as much fluoride, namely 97 f 30 ppm, the lowest figure being 55 and the
1. The 35 and almost highest
434
L. J. BAUMEAND J.-P. VULL&MOZ
125 ppm. This difference between the means of two groups proved to be statistically significant (t = 3 ~66). The average of the Group 2 b caries-resistant enamel of older persons was 140 f 72 ppm, the lowest figure being 60 and the highest 300 ppm. It suggests an increase in fluoride concentration with increasing age. The difference between older and young resistant teeth was not statistically significant, possibly because the range of 20 and 50 yr in this older age group was too wide. The enamel of the 2permanent molars taken from skulls of young adults of the caries-free pre-colonial times contained an average of 99 ppm (90-l 10). TABLE 1. MEAN FLUORIDECONCENTRATION (PPM) OF ENAMELin foto OF POLYNESIAN NA'IWES
Group
Tooth sample
n
R
S. D.
1
“Yellow” teeth
8
51
xtl4
2a
Young caries-resistant
6
96
*29
2b
Old, caries-resistant
8
140
*71
2c
Young prccolonial
4
99
t test
=3.662 =1*109
f8
Analyses supervised by H. Newesely (Berlin).
Data of the assay of the layers reflect a consistent pattern of fluoride distribution within the enamel of caries-resistant teeth. The concentration was greatest in the outermost surface layer and reduced in a curvilinear fashion within the first tenth of mm depth. The gradient of decrease was proportionate to the end value at the outermost layer; in other words the higher this value, the steeper was the gradient. As can be seen from Table 2, the fluoride concentrations found in the outermost surface of permanent teeth were 20 times higher than the total average. TABLE 2. AVERAGECONCENTRATION OFF (ppm) FOUNDIN THEOUTER-
MOSTSURFACELAYER(O-4/&) Group 2a
2b
3
Tooth sample Young permanent Savaii and Australes Savaii Australes Adult permanent Savaii and Australes Savaii Australes Primary 2nd molars Savaii
Analyses made by Miihlcmann,
1930-2660 (2)
(2460)
15 (9) (6)
4517 (4402) (4690)
303@6960
39
555
270-1180
Schait and K&rig (Ziirich).
435
PERMANENT AND PRJMARX TEETH OF POLYNESIANS
In the young permanent teeth of Group 2a, the outermost surface uptake amounted to 2222 ppm on the average, the lowest figure being 1930 and the highest 2660 ppm. In Fig. 1 for each individual young tooth assayed, values of each layer are plotted against the corresponding depth in microns from the surface. There is a slightly increasing gradient toward the outermost surface, indicating a slowed penetration into the depth of the enamel.
0
I
I
I
IO
20
Permanent teeth of caries resistant
Savoi i
OXA
Polynesians IO-20
Austmles
n l
years
I
I
I
I
I
30
40
50
60
70
Depth,
I 80
I 90
p
1. Fluoride concentration (ppm) of enamel of young permanent teeth of 5 cariesresistant Polynesians (Group 2a) at advancing enamel depth &) from the surface (0). Interrupted lines indicate incisors, plain lines molars.
FIG.
Permonent teeth of tories msistent Polynesians older than 20 years
Sovoi i X 0 * v * Austmles++*nao
00
X +
---__
4
IZOO-
6000
I IO
I 20
I 30
I 40
I 50 Depth,
I
I
I
I
I
60
70
80
so
100
p
Fluoride concentration (ppm) of enamel of old permanent teeth of 15 cariesresistant Polynesians (Group 2b) at advancing enamel depth Q from the surface (0). Interrupted lines indicate incisors, plain lines molars.
FIG.
436
L. J. BAUMEANDJ.-P. VULL&MOZ
In the older permanent teeth of the Group 2b, the outermost surface absorption ranged from 3030 to 6960 ppm with an average of 4517 ppm (Table 2) suggesting a continuing accumulation of dietary fluorides into the surface layers with age. There was no obvious variation by geographic distribution as the samples from the Austral Islands and Samoa both fitted into the general pattern characterized by an agespecific gradient. The innermost layer measured at 70-100 p depth yielded no values lower than 600 ppm; this may be indicative of a further decrease in fluoride concentration in the enamel at greater depth. In Fig. 2, the concentration of fluoride at successive layers for each tooth of Group 2b were connected by interpolating curves. E 8
1200 900
Primary
second
molars from Savaii
Depth,
/J
,z. 600 Lt. 300 0
0
FIG. 3. Fluoride concentration of enamel (ppm) of shed primary second molars of children from Savaii at advancing enamel depth from the surface (0). The 8 cases are representative for the range of variation of the sample of 39, the average concentration being 554-S ppm at the outermost surface layer.
It will be noted that the gradient toward the outermost surface is definitely steeper than in Fig. 1 relating to the group of young teeth. The fluoride concentrations of the temporary molars of Group 3 averaged on the outermost surface 555 ppm, the minimum being 270 and the maximum 1180 ppm (Table 2). The lowest concentrations in the innermost layer measured amounted to 50 ppm. Figure 3 presents the plotted data for r-individual teeth representative of the range of variation. Most of the teeth (27 out of 39) come within the range of 280-680 ppm in the outermost surface concentration. The curves are very flat for the samples with low concentration and only in those with high concentration does the curvilinear recession become obvious. DISCUSSION (1) The role of dietary fluorides in producing dentaljuorosis
and resistance to caries
The epidemiological evidence of a resistance of primitive populations to caries was, to a great extent, contained in studies made among early Polynesians (MUMMERY, 1869; PICKERILL, 1912; PRICE, 1938). The increasing caries susceptibility of some of these islanders in recent times was related to changes in dietary habits, in particular to increasing consumption of imported refined carbohydrates (DAVIES, 1965; BARMES, 1967). Not until recently were any field and laboratory studies carried out in the territories in question to determine the relationship between caries resistance and a possible high fluoride consumption. The observation of mottled enamel among French Polynesians whose drinking water contained practically no fluorides pointed to the possible sources of dietary fluorides in the sea food and staple food (BAUME,
437
PERMANENT ANDPRIMARYTEETHOPPOLYNESIANS
1965). From Table 3 it will be noted that the fluoride content of the sea and lagoon water is unusually high, a factor influencing the vegetation and fauna that draws its water supply from these sources. The high fluoride concentration in taro and sago roots has since been confirmed by BARQUES (1969) who found in New Guinea up to 14 - 5 ppm F in taro. The amount of the daily supply of fluorides provided by the typicalPolynesian diet, however, is unknown. TABLE~.THBFLUORIDE CONCENTRATIONS (ppm)o~som
FRENCHPOLYNESUNWATERS
ANDSTAPLEFOODS
Water Number of samples Tap, River Lagoon Sea
Tahiti
Moorea
Huahine
Au&ales
6 0.26 1.20 1.0
4 0.43 1.15 1.39
O.lg :::3
3 0.47 1.12 2.13
Taro (Colocasia) Coconut meat Coconut water Taurua (Xanthosoma) Sweet potato Yam
4.0 2.9 0.55 2.3 0.8 0.8
(2.8-5.6) (2.4-3.4) (0.5-0.6) (2.3) (0.6-1.4) (0.7-O. 8)
Fluoride analysesby F. J. McClure,N.I.D.R., Bethesda,Md. (From Baume,1965). Information regarding the fluoride content of enamel in relation to dietary fluorides is very scanty and refers only to the concentration in total enamel (SOGNNAES,1962; SMITH, 1966). The values of 140 ppm reported from Tristan da Cunha by SOGNNAES, (1954) are in keeping with those found in comparable samples taken among Polynesians. ELLIOTTand SMITH(1960) indicated for enamel of adolescents of Toronto and Sarnia, without water fluoridation, a fluoride concentration of 47 ppm, for Stratford, where the water contains 1.3 ppm F, 128 ppm, and for St. John, with high dietary fluorides, 67 ppm. One significant result of the present study was the discovery of a relatively low fluoride concentration in yellow teeth (51 ppm) and of a relatively moderate concentration in the teeth of the caries-resistant young group (97 ppm). Differences in total fluoride concentration alone, however, hardly explain for the extremely high cariessusceptibility of the first group and the contrasting high caries-resistance of the second group. According to analyses of the fluoride concentration of enamel in relation to fluoride of water supply (MCCLURE and LIKINS, 1951), the amount found in the young yellow teeth would correspond to an intake of co.25 ppm through drinking water, while 97 ppm in the enamel of young caries-resistant Polynesians would correspond to 1.0 ppm waterborne fluoride. As will be shown in another report, yellow teeth of Tahitians, in addition to having a low fluoride concentration,
438
L. J. BAW ANDJ.-P. VIJLL&OZ
are also low in mineral concentration as they show microradiographical evidence of internal hypomineralization. The higher fluoride concentration of the total enamel of the older age group (average 140 ppm) agrees with the well-established fact that fluorides may be accumulated in enamel during a life-time (JENKINSand SPEIRS, 1953 ; JENKINS, 1966). The moderately high values observed in the teeth of caries-free Polynesians, including those observed in the permanent teeth dating from the pre-colonial times, are in keeping with the relationship established by DEAN(1942) and HODGEand SMITH(1954) for fluoride concentrations in drinking water and enamel fluorosis (mottling). As confirmed by BRUDEVOLD (1962), fluoride concentrations in enamel above 180 ppm, corresponding to l-2 ppm waterborne fluorides, are not associated with brown pigmentation. This is true for the Polynesian situation, where slight fluorosis was prevalent, suggesting that the fluoride intake during enamel formation did not exceed the corresponding level of 1 ppm waterborne fluoride intake. The two obviously brown mottled teeth examined contained 250 and 300 ppm, which would correspond to a water supply with 2.5 ppm flouride. Increased occurrence of brown mottling was described in littoral communities of Samoa which depended mainly on sea food (BAUME,1968). The remarkable caries resistance associated with the very slight fluorosis experienced by the inhabitants of the Austral Islands and Savaii seems to be well reflected by the moderately high fluoride concentration of their enamel. (2) DifSerences in enamel uptake between fluorides in drinking water and dietary fluorides Caution must be exercised in establishing parallels between the fluoride concentration in enamel and drinking water on the one hand, and the amount of dietary fluorides on the other, the latter being the main fluoride source for the Polynesians. This distinction is well illustrated by the results of the analysis of the layers. The outstanding observation of this study concerns the high fluoride concentration in the outermost enamel surface of caries-resistant permanent teeth and the relatively low concentration in primary teeth. Epidemiological evidence of an average fluoride concentration of 4517 ppm in the enamel of caries-free Polynesians remains so far unmatched in the literature. YOON et al. (1960) indicated a maximum value of 3707 ppm in teeth from middle-aged adults of Slaton (Tex.) with a water supply of 5 -2 ppm fluoride. Adolescents from areas with 3 ppm in the drinking water showed concentrations up to 1930 ppm; in teeth from persons in older age groups the concentration never exceeded 2290 ppm. The values given by ISAACet al. (1958) in respect of other high fluoride areas are of the same order of magnitude. Prophylactic enrichment of enamel with an amine fluoride, as reported by RINDERERet al. (1965), raised the surface fluoride concentration from 770 ppm to a maximal level of 2800 ppm, LITTLE et al. (1967) reported in sound intact enamel an increase in surface accumulation witb increasing age from 200 ppm to 400 ppm in sound intact teeth, and from 2000 to 3300 ppm in hypomineralized discoloured enamel. More recently MCCANN (1969) was able to obtain, after pretreatment of enamel with Al or Ti-salts followed by an application of an acidic phosphate fluoride solution, surface concentrations of 14000 to 19000 ppm, suggesting a role of other
PERMANENT
AND
PRIMARY
TEETH
OF POLYNESIANS
439
ions including possibly certain micronutritients in the retention of dietary fluorides in the enamel. Figure 2 presents the evidence that fluoride concentration on the enamel surface in old Polynesians may reach a maximum level of almost 7000 ppm. The rate of uptake of dietary fluorides apparently does not follow the pattern described by BRUDEVOLD et al. (1960) for enamel from areas with different levels of water-borne fluorides, according to which little increase occurs with increasing age in the fluoride accumulation in enamel in high fluoride areas while enamel in low fluoride areas shows a continuous augmentation. The remarkable feature of the high topical absorption of fluorides from food lies in the fact that it occurs under physiological conditions with no known untoward effects on general health such as would occur in correspondingly high water-borne fluoride of 5-10 ppm having the same topical effect. As stated by M~~HLER(1969), the metabolism of dietary fluorides warrants further study. As far as the topical effect is concerned, the steep gradient of the curves (Fig. 2) indicates that there was little penetration of these added fluorides into the enamel. Quantitative microradiographic analysis of the mineral content-to be reported elsewhere-clearly indicates a very dense mineralization of the surface structures. This may baulk deep fluoride penetration. The presence of hypomineralized areas in the subsurface, therefore, seems not to be a prerequisite for high fluoride accumulation, such as suggested by some authors (NEWBRUNand BRUDEVOLD,1960). The obviously continuous accumulation of F on the tooth surface through dietary fluorides probably affords the inhabitants of the Austral Islands and Savaii a lifelong protection from decay but does not prevent them from severe periodontal diseases (BAUME,1968). It would be easy to conjecture that high fluoride concentrations in food, in the absence of proper hygiene, would promote calcification of plaques which in return contributes to the development of periodontal diseases. (3) Variations in fluoride absorption in primary and permanent teeth The low concentrations found in the enamel surface of primary molars (average 555 ppm) are not easy to reconcile with the four-fold higher values found in young permanent teeth, as both sets of teeth were exposed for about an equal period of time to the same dietary environment. The phenomenon may be explained as a matter of fluoride supply and demand. As the second primary molars calcify during the perinatal period, relatively small amounts of fluorides may be provided through maternal blood and milk. Children of Savaii are breast-fed up to the age of 2 yr (BAUME,1968). After weaning, traditional eating habits are such that the children eat the rest of the meal left over first by the male members of the tribe and then that left over by the female members. The few figures available for the fluoride content of primary teeth also indicate that they contain a lower concentration than do permanent teeth (WEATHERELLand HARGREAVES,1965; JENKINS,1966). ISAACet al. (1958) found in Chicago children, in an environment with 0.1 ppm fluoride in the drinking water, 240 ppm on the outermost surface and 50 ppm in the innermost enamel portion, and BRUDEVOLD et al. (1956) a gradient from 448 to 56 ppm.
440
L. J. BAUMEANDJ.-P.
VULL~~MOZ
TRIERS,ELLIOTTand SMITH(1968) did not find in the enamel of primary teeth, by contrast with permanent teeth, any higher fluoride concentration among children of St. John (47 ppm) with a known high dietary fluoride consumption than in Toronto and Sarnia (50 ppm) with a low dietary fluoride intake. WEATHERELL and HARGREAVE~ (1965, 1966) noted in bulk enamel as well as outer surface enamel distinctly higher concentrations in primary teeth from children living in areas with a high level fluoride in the drinking water (1.9-2.2 ppm) than in those of low fluoride areas (O-1 ppm); the latter from Yorkshire (U.K.) corresponded approximately to the Savaiian scatter of the means. The low fluoride concentration of the primary teeth may account for their relatively higher caries-susceptibility, which is well established in all surveys made among Polynesian children, notwithstanding their geographic location (BAUME,1969). The physiology of dietary fluorides appears to have many features in common with that of water-borne fluorides. From the point of view of toxicology, it shows, however, some new aspects such as the possibility of a very high topical enrichment of enamel without untoward aesthetic and systemic effects, which may be of particular interest for prophylactic measures to ensure a life-long resistance to caries. Acknowledgements-The authors wish to thank Dr. F. J. MCCLURE (Bethesda) for the fluoride analyses of the water and plant samples sent from French Polynesia, Dr. H. M~~HLEMANN (Zurich) for the assays of the enamel layers, and Dr. H. NEWESELY (Berlin) and Miss H. SCHMIDT(Geneva) for the in foto determinations. Part of this study has been financed by grant 3868 of the Fonds National Suisse. R~%um&Dansle cadre d’enquetes dentaires et alimentaires,
95 dents extraites ou perdues, ont CtC recueillies parmi trois groupes de Polynesiens dont la frequence de carie Ctait comrue, afin de determiner le taux de fluor darts l’email. Le premier groupe comprenait des dents permanentes “jaunes” hautement susceptibles a la carie, provenant de jeunes Tahitiens; le deuxieme groupe ttait compose de dents permanentes Iegerement fluorkes et resistantes a la carie, d’ecoliers et d’adultes des iles Australes (Polynesie francaise) et de Savaii (Samoa Occidentales), y compris des dents de cranes de l’epoque prkcoloniale; le troisieme groupe etait forme de secondes molaires temporaires perdues par des enfants de Savaii. Le taux de fluor a et6 determine darts I’email in toto (groupes 1 et 2) et par couches superticielles successives (groupes 2 et 3) dans des laboratoires reconnus. L’bmail des jeunes dents “jaunes” contenait dans sa totalite la moitie de la quantite de fluor (2 51 ppm) de l’email des dents jeunes resistantes a la carie. Les dents resistantes plus Lgees revelaient un contenu moyen plus eltve (2 140 ppm) demontrant une accumulation post-eruptive continue du fluor; les dents fluorees aux taches brunes atteignaient un maximum de 300 ppm; les dents jeunes de I’epoque prkcoloniale avaient un taux de fluor equivalent a celui de leurs homologues contemporaines. L’analyse par couches de l’email des dents permanentes resistantes a la carie a montre un accroissement de la concentration superticielle en fluor avec Page; la moyenne Btait de f 2222 pour la couche la plus exteme des dents permanentes jeunes, tandis qu’elle s’elevait ii 2 4517 ppm pour les dents plus agkes. Plus le taux Ctait tleve en surface, plus la diminution Btait rapide dans le premier dixieme de mm a I’interieur de Email. 11a Cte montre que, sans aucune autre mesure de fluoration que le fluor alimentaire, des concentrations de 6960 ppm ont ett atteintes, sans effets esthetiques ou generaux f&hew D’autre part, les secondes molaires temporaires provenant du meme kchantillonnage de population ont montrt une concentration superticielle Btonnamment plus basseen moyenne 4 fois moins-que dans les dents permanentes dun age correspondant.
PERMANENT ANDPRIMARYTEETHOF WLYNESIANS
441
Les valeurs diminuent peu avec la profondeur. Ce ph&nomene, dont les raisons ont et& discutees, va de pair avec la susceptibilitie a la carie relativement plus grande des dents temporaires de populations polynbiennes, r&v&m par ailleurs des dents permanentes r&&antes a la carie. En conclusion, on a reconnu que la remarquable resistance a la carie -la vie durant --de certaines collectivitts polynesiennes isol&es, est associ& a un enrichissement topique continu de l’email de leurs dents permanentes par le fluor alimentaire en extrememente haute quantite, sans effets secondaires facheux. Zusanunenfassung-Im Rahmen von epidemiologischen Erhebungen tiber die EmPhrungs- und Zahnverhlltnisse von 3 polynesischen Volksgruppen wurden 95 ausgezogene oder ausgefallene Zlhne auf den Fluorgehalt des Zahnschmelzes untersucht. Die 1. Gruppe bestand aus stark kariesanfalligen “gelben Ziihnen” von jugen Tahitiem; die 2. Gruppe aus kariesresistenten bleibenden Ziihnen mit leichter Fluorose von (a) jungen, (b) llteren Einwohnem des Australarchipels (Franzosisch Polynesien) und von Savaii (West Samoa) sowie (c) von jungen bleibenden Zlhnen vorgeschichtlicher Schldel aus den Tuamotu; die 3. Gruppe setzte sich aus ausgestossenen 2. Milchmolaren von Savaii (West Samoa) zusammen. Der Fluorgehalt wurde von daftir kalibrierten Laboratorien einerseits fur den gesamten Schmelz (Gruppe 1 und 2) andemseits schichtweise von der ObertXche her (Gruppe 2 und 3) bestimmt. Der Schmelz von “gelben Zlhnen” junger Tahitier enthielt nur fast halb soviel F (a 51 ppm) als der junger kariesresistenter Polynesier (2 97 ppm). Ahere bleibende Zahne enthielten mehr F (2 140 ppm), was auf eine kontinuierliche posteruptive Fluoranreicherung schliessen liess. Braunverfarbte Fluorosezahne zeigten mit 300 ppm die grossten F-Mengen, wahrend die prlkolonialen jungen Ziihne mit 101 ppm sich mit den heutigen Homologen auf der Waage hielten. Die Schichtenanalyse kariesresistenter bleibender Zahne zeigte mit fortschreitendem Alter der Individuen ebenfalls hbhere Konzentrationen; w%hrend diese in der lussersten Schicht der jungen Gruppe im Durchschnitt 2222 ppm betrug, stieg sie in der llteren Gruppe auf 4517 ppm an. Je hiiher die Oberhiichenkonzentration umso steiler war der Abfall gegen die tiefen Schichten innerhalb der gemessenen ersten 100 CL.Vergleich mit Berichten aus der Literatur zeigten, dass mit keiner anderen Fluoridierungsmassnahme als mit der aliment&n Ursprung eine so grosse Anreicherung wie maximal 7000 ppm in der Oberhlche ohne sichtbare Schmelzschiiden oder Allgemeinstorungen zustande kommen kann. Die Milchzlihne gleichen lokalethnischen Ursprunges zeigten dagegen 4mal niedrigere Oberlikhenkonzentrationen als gleichaltrige bleibende Ziihne. Die Werte verringerten sich wenig mit zunehmender Tiefe. Die Griinde fiir dieses verschiedene Verhalten des Milchzahn-Schmelzes sind, wie diskutiert, noch wenig klar. Statistisch ist es eine Tatsache, dass in den polynesischen Volksgruppen mit fast totaler Kariesfreiheit im bleibenden Gebiss, die Milchziihne immer eine gewisse Kariesanfalligkeit aufwiesen. Auf Grund dieser vorllufigen Analysen liegt der Schluss nahe, dass die lebensganglithe Kariesresistenz isolierter polynesischer Gemeinschaften durch eine dauemde Anreicherung ihres Zahnschmelzes in extrem hohen Quantitlten aus fluorreichen Nahrungstoffen zustande kommt, ohne dass allgemeine oder lokale Fluorschlden auftreten. REFERENCES BARMES,D. E. 1967. Dental and nutritional surveys of primitive peoples in the Pacific Islands. Aust. dent. J. 12, 442-454. BARMES,D. E. 1969. Caries etiology in Sepik villages-Trace element, micronutrient and macronutrient content of soil and food. Caries Res. $44-59. BAUME, L. J. 1965. Erhiihrungs- und Zahnverhiiltnisse bei 12.000 Kindem in Polynesien. Dt. zahniirztl. Z. 20, 510-513. BAUME,L. J. 1968. Rapport preliminaire sur une enqu&te dentaire dans les Samoa Occidentales. Rev. mens. Suisse Odonto-stomat. 78, 729-752. BAUM~, L. J. 1969. Caries prevalence and caries intensity among 12,344 schoolchildren of French Polynesia. Archs oral Biol. 14, 181-205.
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BAUME,L. J. and MEYER,J. 1966. Dental dysplasia related to malnutrition. J. dent. Res. 45,726741. BAUMLER,J. and GLINZ, E. 1964. Bestimmung von Fluoridionen im Mikrogrammbereich. Mitt. Geb. Lebensmittelunters. Hyg. 55, 250-264. BRUDEVOLD,F. 1962. Chemical composition of the teeth in relation to caries. In: SOGNNAES,R. F. Chemistry and Prevention of Dental Caries, Chap. 2, pp. 32-88. Thomas, Springfield, Illinois. BRUDEVOLD,F., GARDNER,D. E. and Sm, F. A. 1956. The distribution of fluoride in human enamel. J. dent. Res. 35,420-429. BRUDEVOLD,F., STEADMAN,L. T. and SMITH,F. A. 1960. Inorganic and organic components of tooth structure. Ann. N. Y. Acud. Sci. 85, 110-132. DAVIES,G. N. 1965. The significance of epidemiological studies in relation to caries resistance. In. WOLSTENHOLME, G. E. W., and O’CONNOR, M. Eds: Caries-resistant Teeth, p. 7. Churchill, London. DEAN, H. T. 1942. The investigation of physiological effects by the epidemiological method. In:. MOULTON,F. R. Fluorine and Dental Health, p. 23. Am. Ass. Adv. Sci., Washington (1942). ELLIOTT,C. G. and SMUH, M. D. 1960. Dietary fluoride related to fluoride content of teeth. J. dent. Res. 39,93-98. HODGE, H. C. and Sr.or~, F. A. 1954. Some public health aspects of water fluoridation. In: SHAW, J. H., Ed., Fluoridation as Public Health Measure, pp. 79-109. Am. Ass. Adv. Sci., Washington. ISAAC, S., BRUDEVOLD,F., Shnru, F. A. and GARDNER,D. E. 1958. The relation of fluoride in the drinking water to the distribution of fluoride in enamel. J. dent. Res. 37, 318-325. JENKINS,G. N. 1966. Chemical composition of teeth. In: The Physiology of the Mouth (3rd Ed.), pp. 71-75. Blackwell, Oxford. JENKINS,G. N. and SPEIRS,R. L. 1953. Distribution enamel. J. Physiol. 121, 21. Abstract. L~ITLE, M. F., CASCIANI, ROWLEY,J. 1967. Site of fluoride accumulation erupted human Archs oral Biol. 12,839-847. MCCANN, H. G. 1969. The effect of fluoride complex formation enamel. Archs oral Biol. 14, 521-531. LIKINS, R. C. 1951. Fluorine in human teeth in relation to fluorine in the drinking water. J. dent. Res. 30, 172-176. MILLER, I. J. 1965. Dental Fluorose of International Science Publishers, removal of enamel layers and its suitability MUHLER, J. C. 1969. Ingestion Health, Vol. I, pp, 11-34, 11-49, W. H. O., MUMMERY,R. F. 1869. On the relations amongst the inhabitants amongst existing aboriginal
Microradiographic PICKERILL,
Studies on the physical properties 38-674.
enamel. I.
studies among primitive
Oxford. L., SCHAIT,A. and M~HLEMANN,H. R. 1965. Loss of fluoride from dental enamel after topical fluoridation (Preliminary report). Heh. odont. Acta 9, 148-150. Shah, F. A. 1966. Handbook of Experimental Pharmacology. XX/l. Pharmacology of Fluorides. Part I. Springer Vet-lag, Berlin. SOGNNAES,R. F. 1954. Oral Health Survey of Tristan da Cunha. Results of the Norwegian scientific expedition to Tristan da Cunha, 1937-1938, No. 24. Published by Det Norske VidenskapsAkademi, Oslo. SOGNNAES,R. F. 1962. Chemistry and Prevention of Dental Caries. Publication NO. 466, American Lecture Series. Thomas, Springfield, Illinois. Tamas, D., E~~o’rr, C. G. and SMITH,D. 1968. Further studies on the relationship of dietary fluoride to fluoride content of human teeth. J. dent. Res. 47, 1171-1175. RINDERER,
PERMANENTANDPRIMARYTEETHOFPOLYNESLANS VULLIEMOZ, J.-P. and BAUME, L. J. 1966. Les structures
443
des “dents jaunes”, de dents fluon% et de dents anciennes de provenance polyntsienne: leurs rapports avec la carie dentaire et I’alimentation. Rev. mens. Suisse Oabnto-stomat. 76, 409-434. WEATHERELL, J. A. and HARGREAVES,J. A. 1965. Variation of Fluoride Concentration in Human Deciduous Teeth. In: Advances in FIuorine Research and Dental Caries Prevention, ORCA, Vol. 3, pp. 247-254. Pergamon Press, Oxford. WEATHERELL, J. A. and HARGREAVES, J. A. 1966. The fluoride content of surface enamel from permanent and deciduous teeth. In: Advances in Fluorine Research and Dental Caries Prevention, ORCA, Vol. 4, pp. 181-191. Pergamon Press, Oxford. YOON, S. H., BRUDEVOLED, F., GARDNER,D. E. and SMWH, F. A. 1960. Distribution of fluoride in teeth from areas with different levels of fluoride in the water supply. J. dent. Res. 39, 845-856.
DIETARY FLUORIDE UPTAKE INTO THE ENAMEL OF CARIES-SUSCEPTIBLE “YELLOW” PERMANENT TEETH AND OF CARIES-RESISTANT PERMANENT AND PRIMARY TEETH OF POLYNESIANS L. J.
BAUME
and
J.-P. VULLI~MOZ
South Pacific Commission-Noumea, New Caledonia School of Dental Medicine, Medical Faculty, University of Geneva Switzerland Sunnnary-Within the frame of a dental and dietary survey, 95 shed and extracted intact teeth were collected from three groups of Polynesians of a known caries intensity for determination of the fluoride concentration in the enamel. The first group consisted of “yellow” highly caries-susceptible permanent teeth of young Tahitians; the second group comprised slightly fluorosed caries-resistant permanent teeth of schoolchildren and adults of the Austral Islands (French Polynesia) and Savaii (Western Samoa), including some teeth from pre-colonial skulls; the third group was composed of shed second primary molars of Savaiian children. The fluoride concentration was determined for the enamel in toto (Groups 1 and 2) and for successive surface layers (Groups 2 and 3) by tests carried out by well-calibrated laboratories. Enamel of young “yellow” teeth contained only half the concentration (51 ppm) of their caries-resistant counterparts. Older caries-resistant teeth showed a higher average concentration (140 ppm) reflecting a continuous post-eruptive accumulation of fluoride; brown mottled teeth (300 ppm) ranked highest; pre-colonial young ones matched the modem counterparts in fluoride concentration. Analysis of the surface layer of caries-resistant permanent teeth showed increasingly higher concentrations with advancing age, averaging in the outermost surface layer of young permanent teeth 2222 ppm, and 4517 in the older ones. The higher the surface concentration, the steeper was the decrease within the iirst tenth of millimetre depth measured. It was shown that, with no fluoridation measure other than dietary fluorides, concentrations as high as 6960 ppm have been reached in the enamel without untoward aesthetic and systemic effects. Primary second molars drawn from the same population sample, on the other hand, showed strikingly lower surface concentrations-on the average 4-times less than permanent teeth of corresponding age. The values decreased little with progressive depth. The reasons for this phenomenon are discussed. It reflected the relatively greater caries suceptibility of primary teeth of Polynesian populations showing a low caries frequency in the permanent teeth. Hence the remarkable caries resistance through life recorded in some isolated Polynesian collectivities was associated with a continuous topical enrichment of the enamel of their permanent teeth with dietary fluorides in extremely high quantities.
INTRODUCTION
A DENTAL survey of the school population of French Polynesia revealed marked differences in the geographic distribution of caries attack in the permanent teeth (BAUME, 1969). Tahitians, on the one hand, showed a prevalence of 90 per cent and 431
432
L. J. BAUM~ ANDJ.-P. V~JLL&MOZ
an average intensity rate of 12 DMF teeth per person at the age of 15. Pupils of the remote Austral Islands, on the other hand, remained for the most part caries-free, showing an average attack rate of 3 DMF teeth at the age of 14. Among Tahitians a condition called “yellow teeth” proved to be particularly vulnerable to early rampant decay (VULLIEMOZ and BAUME,1966). Dietary surveys pointed to a possible background of malnutrition characterized by an excessive intake of refined (imported) carbohydrates and an insufficient consumption of foods containing calcium and protein (BAUME,1965). Children in the Austral Islands who still adhered to the traditional Polynesian diet absorbed, through the consumption of fish, taro and coconut, sufficiently high quantities of fluorides so that slight to moderate fluorosis of the permanent teeth was a predominant feature. A recent survey carried out among 10,000 inhabitants of Western Samoa showed that an identical condition of a high caries resistance associated with slight enamel fluorosis also prevailed among the inhabitants of the island of Savaii (BAUME,1968). The primary teeth of the French Polynesian children, on the other hand, showed little difference in caries intensity when the results were tabulated by geographic location. The average d.f. rate at the age of 5 was 7.5 in Tahitians and 5 *Oin children in the Austral Islands. Similar lowered caries resistance in the primary teeth has been reported from other isolated Polynesian communities (BARMES,1967). These variations in caries susceptibility of the permanent teeth by geographic location on the one hand, and of primary and permanent teeth on the other, among persons of the same closed populations have been related to host factors including the chemical and physical composition of the teeth as determined by diet and nutrition (DAVIES, 1965). An attempt was made therefore to collect samples of intact teeth which, according to related epidemiological data, were representative of distinct caries-resistant and caries-susceptible groups. In an earlier series of studies, the histopathological aspects of specific conditions such as infantile “melanodontia” and “odontoclasia” as well as “yellow permanent teeth” have been reported (BAUMEand MEYER, 1966). In this second series of studies, quantitative analyses of the fluoride and mineral content of three samples of teeth of caries-susceptible and caries-resistant groups were assessed. It is the purpose of the present pilot study to report on data of the fluoride concentration of the enamel, and to discuss its relation to dietary fluorides. MATERIAL AND METHODS The three samples of caries-free teeth were constituted as follows : Group 1 of highly caries-susceptible permanent teeth. This group was composed of 18 yellow teeth from Tahitian schoolchildren between the ages of 10 and 18 years which exhibited the characteristics described by VULLIEMOZand BAUME(1966). The portions not used for median ground sections of 8 caries-free yellow teeth were used for fluoride analyses of the enamel in toto. Group 2 of caries-resistant permanent teeth. This group was composed of 38 incisors and molars showing signs of very slight to slight fluorosis of the enamel l&-2* according to the scale of MILLER (1965), and two with brown discolourations (scale 3). They were divided into two subgroups according to the age of the patients:
PERhfANEW AND PRIMARY TEETH OF POLYNESIANS
433
(a) Fifteen teeth of younger persons between the ages of 10 and 20 yr: 6 teeth from Savaii were analyzed for the fluoride content of the entire enamel and 5 teeth from Savaii and the Austral Islands respectively for analysis of fluoride uptake by successive layers. Four molars removed from skulls found on Makatea (Tuamotu) were analyzed by Dr. MCCLURE. (b) Twenty-three teeth of persons over the age of 30 yr who were suffering from advanced periodontal diseases: 8 from Savaii were used for total fluoride determination and 15 (9 from Savaii, 6 from the Austral Islands) for fluoride assay of successive layers of the enamel surface. Group 3 of caries-resistant primary teeth. This group included 39 shed primary second molars from children of Savaii. These teeth were used exclusively for analysis of the fluoride content of successive layers. Records of the teeth selected at random in each group included both macrophotographs in black and white as well as in colour made with a Nikon equipment and 2 radiographs of both the mesiodistal and buccolingual aspects made with a dental X-ray machine. For the determination in toto, the F separation method by diffusion of BWMLER and GLINZ (1964), modified according to NEWESELY(personal communication), was applied. The final calorimetric F determination using alizarin complexan was carried out according to the method of QUENTIN(1965). These analyses were supervised by H. NEWESELY. For the analysis of fluoride in successive layers of external enamel, the crowns were first cleaned with pumice applied by an electrical toothbrush for 1 min. Then the roots and the marginal third of the crowns were covered with wax. Afterwards, in order to remove successive enamel layers the crowns were exposed separately and successively to 5 ml 2%perchloric acid. Exposure times were 5, 10 and 15 set, and two sequences of 3 x 15 sec. After each demineralization, the crowns were washed with 5 ml of distilled water which were added to the perchloric acid solution. Each demineralizing solution was analyzed for phosphorus and fluoride according to methods described by M~~HLEMANN, SCHAITand KOENIG (1964) who performed the analyses. Since the roots of the primary molars were absent owing to resorption some difficulties arose in the performance of micromeasurements of layer thickness. The ratio of “dissolved microlayer” and “total of phosphorus” in the diffusate varied between 4.9 and 29 *3. The average ratio gained from 40 measurements was 11.4. This value was used for the calculations of the layer thickness according to the phosphorus content of the diffusate. For these reasons, a relatively larger sample of primary molars was assayed. RESULTS Data of fluoride concentration of the total enamel are shown in Table average of Group 1 “yellow teeth” was 51 f 14 ppm, the lowest figure being the highest 65 ppm. Caries-resistant enamel of the younger Group 2a contained twice as much fluoride, namely 97 f 30 ppm, the lowest figure being 55 and the
1. The 35 and almost highest
434
L. J. BAUMEAND J.-P. VULL&MOZ
125 ppm. This difference between the means of two groups proved to be statistically significant (t = 3 ~66). The average of the Group 2 b caries-resistant enamel of older persons was 140 f 72 ppm, the lowest figure being 60 and the highest 300 ppm. It suggests an increase in fluoride concentration with increasing age. The difference between older and young resistant teeth was not statistically significant, possibly because the range of 20 and 50 yr in this older age group was too wide. The enamel of the 2permanent molars taken from skulls of young adults of the caries-free pre-colonial times contained an average of 99 ppm (90-l 10). TABLE 1. MEAN FLUORIDECONCENTRATION (PPM) OF ENAMELin foto OF POLYNESIAN NA'IWES
Group
Tooth sample
n
R
S. D.
1
“Yellow” teeth
8
51
xtl4
2a
Young caries-resistant
6
96
*29
2b
Old, caries-resistant
8
140
*71
2c
Young prccolonial
4
99
t test
=3.662 =1*109
f8
Analyses supervised by H. Newesely (Berlin).
Data of the assay of the layers reflect a consistent pattern of fluoride distribution within the enamel of caries-resistant teeth. The concentration was greatest in the outermost surface layer and reduced in a curvilinear fashion within the first tenth of mm depth. The gradient of decrease was proportionate to the end value at the outermost layer; in other words the higher this value, the steeper was the gradient. As can be seen from Table 2, the fluoride concentrations found in the outermost surface of permanent teeth were 20 times higher than the total average. TABLE 2. AVERAGECONCENTRATION OFF (ppm) FOUNDIN THEOUTER-
MOSTSURFACELAYER(O-4/&) Group 2a
2b
3
Tooth sample Young permanent Savaii and Australes Savaii Australes Adult permanent Savaii and Australes Savaii Australes Primary 2nd molars Savaii
Analyses made by Miihlcmann,
1930-2660 (2)
(2460)
15 (9) (6)
4517 (4402) (4690)
303@6960
39
555
270-1180
Schait and K&rig (Ziirich).
435
PERMANENT AND PRJMARX TEETH OF POLYNESIANS
In the young permanent teeth of Group 2a, the outermost surface uptake amounted to 2222 ppm on the average, the lowest figure being 1930 and the highest 2660 ppm. In Fig. 1 for each individual young tooth assayed, values of each layer are plotted against the corresponding depth in microns from the surface. There is a slightly increasing gradient toward the outermost surface, indicating a slowed penetration into the depth of the enamel.
0
I
I
I
IO
20
Permanent teeth of caries resistant
Savoi i
OXA
Polynesians IO-20
Austmles
n l
years
I
I
I
I
I
30
40
50
60
70
Depth,
I 80
I 90
p
1. Fluoride concentration (ppm) of enamel of young permanent teeth of 5 cariesresistant Polynesians (Group 2a) at advancing enamel depth &) from the surface (0). Interrupted lines indicate incisors, plain lines molars.
FIG.
Permonent teeth of tories msistent Polynesians older than 20 years
Sovoi i X 0 * v * Austmles++*nao
00
X +
---__
4
IZOO-
6000
I IO
I 20
I 30
I 40
I 50 Depth,
I
I
I
I
I
60
70
80
so
100
p
Fluoride concentration (ppm) of enamel of old permanent teeth of 15 cariesresistant Polynesians (Group 2b) at advancing enamel depth Q from the surface (0). Interrupted lines indicate incisors, plain lines molars.
FIG.
436
L. J. BAUMEANDJ.-P. VULL&MOZ
In the older permanent teeth of the Group 2b, the outermost surface absorption ranged from 3030 to 6960 ppm with an average of 4517 ppm (Table 2) suggesting a continuing accumulation of dietary fluorides into the surface layers with age. There was no obvious variation by geographic distribution as the samples from the Austral Islands and Samoa both fitted into the general pattern characterized by an agespecific gradient. The innermost layer measured at 70-100 p depth yielded no values lower than 600 ppm; this may be indicative of a further decrease in fluoride concentration in the enamel at greater depth. In Fig. 2, the concentration of fluoride at successive layers for each tooth of Group 2b were connected by interpolating curves. E 8
1200 900
Primary
second
molars from Savaii
Depth,
/J
,z. 600 Lt. 300 0
0
FIG. 3. Fluoride concentration of enamel (ppm) of shed primary second molars of children from Savaii at advancing enamel depth from the surface (0). The 8 cases are representative for the range of variation of the sample of 39, the average concentration being 554-S ppm at the outermost surface layer.
It will be noted that the gradient toward the outermost surface is definitely steeper than in Fig. 1 relating to the group of young teeth. The fluoride concentrations of the temporary molars of Group 3 averaged on the outermost surface 555 ppm, the minimum being 270 and the maximum 1180 ppm (Table 2). The lowest concentrations in the innermost layer measured amounted to 50 ppm. Figure 3 presents the plotted data for r-individual teeth representative of the range of variation. Most of the teeth (27 out of 39) come within the range of 280-680 ppm in the outermost surface concentration. The curves are very flat for the samples with low concentration and only in those with high concentration does the curvilinear recession become obvious. DISCUSSION (1) The role of dietary fluorides in producing dentaljuorosis
and resistance to caries
The epidemiological evidence of a resistance of primitive populations to caries was, to a great extent, contained in studies made among early Polynesians (MUMMERY, 1869; PICKERILL, 1912; PRICE, 1938). The increasing caries susceptibility of some of these islanders in recent times was related to changes in dietary habits, in particular to increasing consumption of imported refined carbohydrates (DAVIES, 1965; BARMES, 1967). Not until recently were any field and laboratory studies carried out in the territories in question to determine the relationship between caries resistance and a possible high fluoride consumption. The observation of mottled enamel among French Polynesians whose drinking water contained practically no fluorides pointed to the possible sources of dietary fluorides in the sea food and staple food (BAUME,
437
PERMANENT ANDPRIMARYTEETHOPPOLYNESIANS
1965). From Table 3 it will be noted that the fluoride content of the sea and lagoon water is unusually high, a factor influencing the vegetation and fauna that draws its water supply from these sources. The high fluoride concentration in taro and sago roots has since been confirmed by BARQUES (1969) who found in New Guinea up to 14 - 5 ppm F in taro. The amount of the daily supply of fluorides provided by the typicalPolynesian diet, however, is unknown. TABLE~.THBFLUORIDE CONCENTRATIONS (ppm)o~som
FRENCHPOLYNESUNWATERS
ANDSTAPLEFOODS
Water Number of samples Tap, River Lagoon Sea
Tahiti
Moorea
Huahine
Au&ales
6 0.26 1.20 1.0
4 0.43 1.15 1.39
O.lg :::3
3 0.47 1.12 2.13
Taro (Colocasia) Coconut meat Coconut water Taurua (Xanthosoma) Sweet potato Yam
4.0 2.9 0.55 2.3 0.8 0.8
(2.8-5.6) (2.4-3.4) (0.5-0.6) (2.3) (0.6-1.4) (0.7-O. 8)
Fluoride analysesby F. J. McClure,N.I.D.R., Bethesda,Md. (From Baume,1965). Information regarding the fluoride content of enamel in relation to dietary fluorides is very scanty and refers only to the concentration in total enamel (SOGNNAES,1962; SMITH, 1966). The values of 140 ppm reported from Tristan da Cunha by SOGNNAES, (1954) are in keeping with those found in comparable samples taken among Polynesians. ELLIOTTand SMITH(1960) indicated for enamel of adolescents of Toronto and Sarnia, without water fluoridation, a fluoride concentration of 47 ppm, for Stratford, where the water contains 1.3 ppm F, 128 ppm, and for St. John, with high dietary fluorides, 67 ppm. One significant result of the present study was the discovery of a relatively low fluoride concentration in yellow teeth (51 ppm) and of a relatively moderate concentration in the teeth of the caries-resistant young group (97 ppm). Differences in total fluoride concentration alone, however, hardly explain for the extremely high cariessusceptibility of the first group and the contrasting high caries-resistance of the second group. According to analyses of the fluoride concentration of enamel in relation to fluoride of water supply (MCCLURE and LIKINS, 1951), the amount found in the young yellow teeth would correspond to an intake of co.25 ppm through drinking water, while 97 ppm in the enamel of young caries-resistant Polynesians would correspond to 1.0 ppm waterborne fluoride. As will be shown in another report, yellow teeth of Tahitians, in addition to having a low fluoride concentration,
438
L. J. BAW ANDJ.-P. VIJLL&OZ
are also low in mineral concentration as they show microradiographical evidence of internal hypomineralization. The higher fluoride concentration of the total enamel of the older age group (average 140 ppm) agrees with the well-established fact that fluorides may be accumulated in enamel during a life-time (JENKINSand SPEIRS, 1953 ; JENKINS, 1966). The moderately high values observed in the teeth of caries-free Polynesians, including those observed in the permanent teeth dating from the pre-colonial times, are in keeping with the relationship established by DEAN(1942) and HODGEand SMITH(1954) for fluoride concentrations in drinking water and enamel fluorosis (mottling). As confirmed by BRUDEVOLD (1962), fluoride concentrations in enamel above 180 ppm, corresponding to l-2 ppm waterborne fluorides, are not associated with brown pigmentation. This is true for the Polynesian situation, where slight fluorosis was prevalent, suggesting that the fluoride intake during enamel formation did not exceed the corresponding level of 1 ppm waterborne fluoride intake. The two obviously brown mottled teeth examined contained 250 and 300 ppm, which would correspond to a water supply with 2.5 ppm flouride. Increased occurrence of brown mottling was described in littoral communities of Samoa which depended mainly on sea food (BAUME,1968). The remarkable caries resistance associated with the very slight fluorosis experienced by the inhabitants of the Austral Islands and Savaii seems to be well reflected by the moderately high fluoride concentration of their enamel. (2) DifSerences in enamel uptake between fluorides in drinking water and dietary fluorides Caution must be exercised in establishing parallels between the fluoride concentration in enamel and drinking water on the one hand, and the amount of dietary fluorides on the other, the latter being the main fluoride source for the Polynesians. This distinction is well illustrated by the results of the analysis of the layers. The outstanding observation of this study concerns the high fluoride concentration in the outermost enamel surface of caries-resistant permanent teeth and the relatively low concentration in primary teeth. Epidemiological evidence of an average fluoride concentration of 4517 ppm in the enamel of caries-free Polynesians remains so far unmatched in the literature. YOON et al. (1960) indicated a maximum value of 3707 ppm in teeth from middle-aged adults of Slaton (Tex.) with a water supply of 5 -2 ppm fluoride. Adolescents from areas with 3 ppm in the drinking water showed concentrations up to 1930 ppm; in teeth from persons in older age groups the concentration never exceeded 2290 ppm. The values given by ISAACet al. (1958) in respect of other high fluoride areas are of the same order of magnitude. Prophylactic enrichment of enamel with an amine fluoride, as reported by RINDERERet al. (1965), raised the surface fluoride concentration from 770 ppm to a maximal level of 2800 ppm, LITTLE et al. (1967) reported in sound intact enamel an increase in surface accumulation witb increasing age from 200 ppm to 400 ppm in sound intact teeth, and from 2000 to 3300 ppm in hypomineralized discoloured enamel. More recently MCCANN (1969) was able to obtain, after pretreatment of enamel with Al or Ti-salts followed by an application of an acidic phosphate fluoride solution, surface concentrations of 14000 to 19000 ppm, suggesting a role of other
PERMANENT
AND
PRIMARY
TEETH
OF POLYNESIANS
439
ions including possibly certain micronutritients in the retention of dietary fluorides in the enamel. Figure 2 presents the evidence that fluoride concentration on the enamel surface in old Polynesians may reach a maximum level of almost 7000 ppm. The rate of uptake of dietary fluorides apparently does not follow the pattern described by BRUDEVOLD et al. (1960) for enamel from areas with different levels of water-borne fluorides, according to which little increase occurs with increasing age in the fluoride accumulation in enamel in high fluoride areas while enamel in low fluoride areas shows a continuous augmentation. The remarkable feature of the high topical absorption of fluorides from food lies in the fact that it occurs under physiological conditions with no known untoward effects on general health such as would occur in correspondingly high water-borne fluoride of 5-10 ppm having the same topical effect. As stated by M~~HLER(1969), the metabolism of dietary fluorides warrants further study. As far as the topical effect is concerned, the steep gradient of the curves (Fig. 2) indicates that there was little penetration of these added fluorides into the enamel. Quantitative microradiographic analysis of the mineral content-to be reported elsewhere-clearly indicates a very dense mineralization of the surface structures. This may baulk deep fluoride penetration. The presence of hypomineralized areas in the subsurface, therefore, seems not to be a prerequisite for high fluoride accumulation, such as suggested by some authors (NEWBRUNand BRUDEVOLD,1960). The obviously continuous accumulation of F on the tooth surface through dietary fluorides probably affords the inhabitants of the Austral Islands and Savaii a lifelong protection from decay but does not prevent them from severe periodontal diseases (BAUME,1968). It would be easy to conjecture that high fluoride concentrations in food, in the absence of proper hygiene, would promote calcification of plaques which in return contributes to the development of periodontal diseases. (3) Variations in fluoride absorption in primary and permanent teeth The low concentrations found in the enamel surface of primary molars (average 555 ppm) are not easy to reconcile with the four-fold higher values found in young permanent teeth, as both sets of teeth were exposed for about an equal period of time to the same dietary environment. The phenomenon may be explained as a matter of fluoride supply and demand. As the second primary molars calcify during the perinatal period, relatively small amounts of fluorides may be provided through maternal blood and milk. Children of Savaii are breast-fed up to the age of 2 yr (BAUME,1968). After weaning, traditional eating habits are such that the children eat the rest of the meal left over first by the male members of the tribe and then that left over by the female members. The few figures available for the fluoride content of primary teeth also indicate that they contain a lower concentration than do permanent teeth (WEATHERELLand HARGREAVES,1965; JENKINS,1966). ISAACet al. (1958) found in Chicago children, in an environment with 0.1 ppm fluoride in the drinking water, 240 ppm on the outermost surface and 50 ppm in the innermost enamel portion, and BRUDEVOLD et al. (1956) a gradient from 448 to 56 ppm.
440
L. J. BAUMEANDJ.-P.
VULL~~MOZ
TRIERS,ELLIOTTand SMITH(1968) did not find in the enamel of primary teeth, by contrast with permanent teeth, any higher fluoride concentration among children of St. John (47 ppm) with a known high dietary fluoride consumption than in Toronto and Sarnia (50 ppm) with a low dietary fluoride intake. WEATHERELL and HARGREAVE~ (1965, 1966) noted in bulk enamel as well as outer surface enamel distinctly higher concentrations in primary teeth from children living in areas with a high level fluoride in the drinking water (1.9-2.2 ppm) than in those of low fluoride areas (O-1 ppm); the latter from Yorkshire (U.K.) corresponded approximately to the Savaiian scatter of the means. The low fluoride concentration of the primary teeth may account for their relatively higher caries-susceptibility, which is well established in all surveys made among Polynesian children, notwithstanding their geographic location (BAUME,1969). The physiology of dietary fluorides appears to have many features in common with that of water-borne fluorides. From the point of view of toxicology, it shows, however, some new aspects such as the possibility of a very high topical enrichment of enamel without untoward aesthetic and systemic effects, which may be of particular interest for prophylactic measures to ensure a life-long resistance to caries. Acknowledgements-The authors wish to thank Dr. F. J. MCCLURE (Bethesda) for the fluoride analyses of the water and plant samples sent from French Polynesia, Dr. H. M~~HLEMANN (Zurich) for the assays of the enamel layers, and Dr. H. NEWESELY (Berlin) and Miss H. SCHMIDT(Geneva) for the in foto determinations. Part of this study has been financed by grant 3868 of the Fonds National Suisse. R~%um&Dansle cadre d’enquetes dentaires et alimentaires,
95 dents extraites ou perdues, ont CtC recueillies parmi trois groupes de Polynesiens dont la frequence de carie Ctait comrue, afin de determiner le taux de fluor darts l’email. Le premier groupe comprenait des dents permanentes “jaunes” hautement susceptibles a la carie, provenant de jeunes Tahitiens; le deuxieme groupe ttait compose de dents permanentes Iegerement fluorkes et resistantes a la carie, d’ecoliers et d’adultes des iles Australes (Polynesie francaise) et de Savaii (Samoa Occidentales), y compris des dents de cranes de l’epoque prkcoloniale; le troisieme groupe etait forme de secondes molaires temporaires perdues par des enfants de Savaii. Le taux de fluor a et6 determine darts I’email in toto (groupes 1 et 2) et par couches superticielles successives (groupes 2 et 3) dans des laboratoires reconnus. L’bmail des jeunes dents “jaunes” contenait dans sa totalite la moitie de la quantite de fluor (2 51 ppm) de l’email des dents jeunes resistantes a la carie. Les dents resistantes plus Lgees revelaient un contenu moyen plus eltve (2 140 ppm) demontrant une accumulation post-eruptive continue du fluor; les dents fluorees aux taches brunes atteignaient un maximum de 300 ppm; les dents jeunes de I’epoque prkcoloniale avaient un taux de fluor equivalent a celui de leurs homologues contemporaines. L’analyse par couches de l’email des dents permanentes resistantes a la carie a montre un accroissement de la concentration superticielle en fluor avec Page; la moyenne Btait de f 2222 pour la couche la plus exteme des dents permanentes jeunes, tandis qu’elle s’elevait ii 2 4517 ppm pour les dents plus agkes. Plus le taux Ctait tleve en surface, plus la diminution Btait rapide dans le premier dixieme de mm a I’interieur de Email. 11a Cte montre que, sans aucune autre mesure de fluoration que le fluor alimentaire, des concentrations de 6960 ppm ont ett atteintes, sans effets esthetiques ou generaux f&hew D’autre part, les secondes molaires temporaires provenant du meme kchantillonnage de population ont montrt une concentration superticielle Btonnamment plus basseen moyenne 4 fois moins-que dans les dents permanentes dun age correspondant.
PERMANENT ANDPRIMARYTEETHOF WLYNESIANS
441
Les valeurs diminuent peu avec la profondeur. Ce ph&nomene, dont les raisons ont et& discutees, va de pair avec la susceptibilitie a la carie relativement plus grande des dents temporaires de populations polynbiennes, r&v&m par ailleurs des dents permanentes r&&antes a la carie. En conclusion, on a reconnu que la remarquable resistance a la carie -la vie durant --de certaines collectivitts polynesiennes isol&es, est associ& a un enrichissement topique continu de l’email de leurs dents permanentes par le fluor alimentaire en extrememente haute quantite, sans effets secondaires facheux. Zusanunenfassung-Im Rahmen von epidemiologischen Erhebungen tiber die EmPhrungs- und Zahnverhlltnisse von 3 polynesischen Volksgruppen wurden 95 ausgezogene oder ausgefallene Zlhne auf den Fluorgehalt des Zahnschmelzes untersucht. Die 1. Gruppe bestand aus stark kariesanfalligen “gelben Ziihnen” von jugen Tahitiem; die 2. Gruppe aus kariesresistenten bleibenden Ziihnen mit leichter Fluorose von (a) jungen, (b) llteren Einwohnem des Australarchipels (Franzosisch Polynesien) und von Savaii (West Samoa) sowie (c) von jungen bleibenden Zlhnen vorgeschichtlicher Schldel aus den Tuamotu; die 3. Gruppe setzte sich aus ausgestossenen 2. Milchmolaren von Savaii (West Samoa) zusammen. Der Fluorgehalt wurde von daftir kalibrierten Laboratorien einerseits fur den gesamten Schmelz (Gruppe 1 und 2) andemseits schichtweise von der ObertXche her (Gruppe 2 und 3) bestimmt. Der Schmelz von “gelben Zlhnen” junger Tahitier enthielt nur fast halb soviel F (a 51 ppm) als der junger kariesresistenter Polynesier (2 97 ppm). Ahere bleibende Zahne enthielten mehr F (2 140 ppm), was auf eine kontinuierliche posteruptive Fluoranreicherung schliessen liess. Braunverfarbte Fluorosezahne zeigten mit 300 ppm die grossten F-Mengen, wahrend die prlkolonialen jungen Ziihne mit 101 ppm sich mit den heutigen Homologen auf der Waage hielten. Die Schichtenanalyse kariesresistenter bleibender Zahne zeigte mit fortschreitendem Alter der Individuen ebenfalls hbhere Konzentrationen; w%hrend diese in der lussersten Schicht der jungen Gruppe im Durchschnitt 2222 ppm betrug, stieg sie in der llteren Gruppe auf 4517 ppm an. Je hiiher die Oberhiichenkonzentration umso steiler war der Abfall gegen die tiefen Schichten innerhalb der gemessenen ersten 100 CL.Vergleich mit Berichten aus der Literatur zeigten, dass mit keiner anderen Fluoridierungsmassnahme als mit der aliment&n Ursprung eine so grosse Anreicherung wie maximal 7000 ppm in der Oberhlche ohne sichtbare Schmelzschiiden oder Allgemeinstorungen zustande kommen kann. Die Milchzlihne gleichen lokalethnischen Ursprunges zeigten dagegen 4mal niedrigere Oberlikhenkonzentrationen als gleichaltrige bleibende Ziihne. Die Werte verringerten sich wenig mit zunehmender Tiefe. Die Griinde fiir dieses verschiedene Verhalten des Milchzahn-Schmelzes sind, wie diskutiert, noch wenig klar. Statistisch ist es eine Tatsache, dass in den polynesischen Volksgruppen mit fast totaler Kariesfreiheit im bleibenden Gebiss, die Milchziihne immer eine gewisse Kariesanfalligkeit aufwiesen. Auf Grund dieser vorllufigen Analysen liegt der Schluss nahe, dass die lebensganglithe Kariesresistenz isolierter polynesischer Gemeinschaften durch eine dauemde Anreicherung ihres Zahnschmelzes in extrem hohen Quantitlten aus fluorreichen Nahrungstoffen zustande kommt, ohne dass allgemeine oder lokale Fluorschlden auftreten. REFERENCES BARMES,D. E. 1967. Dental and nutritional surveys of primitive peoples in the Pacific Islands. Aust. dent. J. 12, 442-454. BARMES,D. E. 1969. Caries etiology in Sepik villages-Trace element, micronutrient and macronutrient content of soil and food. Caries Res. $44-59. BAUME, L. J. 1965. Erhiihrungs- und Zahnverhiiltnisse bei 12.000 Kindem in Polynesien. Dt. zahniirztl. Z. 20, 510-513. BAUME,L. J. 1968. Rapport preliminaire sur une enqu&te dentaire dans les Samoa Occidentales. Rev. mens. Suisse Odonto-stomat. 78, 729-752. BAUM~, L. J. 1969. Caries prevalence and caries intensity among 12,344 schoolchildren of French Polynesia. Archs oral Biol. 14, 181-205.
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BAUME,L. J. and MEYER,J. 1966. Dental dysplasia related to malnutrition. J. dent. Res. 45,726741. BAUMLER,J. and GLINZ, E. 1964. Bestimmung von Fluoridionen im Mikrogrammbereich. Mitt. Geb. Lebensmittelunters. Hyg. 55, 250-264. BRUDEVOLD,F. 1962. Chemical composition of the teeth in relation to caries. In: SOGNNAES,R. F. Chemistry and Prevention of Dental Caries, Chap. 2, pp. 32-88. Thomas, Springfield, Illinois. BRUDEVOLD,F., GARDNER,D. E. and Sm, F. A. 1956. The distribution of fluoride in human enamel. J. dent. Res. 35,420-429. BRUDEVOLD,F., STEADMAN,L. T. and SMITH,F. A. 1960. Inorganic and organic components of tooth structure. Ann. N. Y. Acud. Sci. 85, 110-132. DAVIES,G. N. 1965. The significance of epidemiological studies in relation to caries resistance. In. WOLSTENHOLME, G. E. W., and O’CONNOR, M. Eds: Caries-resistant Teeth, p. 7. Churchill, London. DEAN, H. T. 1942. The investigation of physiological effects by the epidemiological method. In:. MOULTON,F. R. Fluorine and Dental Health, p. 23. Am. Ass. Adv. Sci., Washington (1942). ELLIOTT,C. G. and SMUH, M. D. 1960. Dietary fluoride related to fluoride content of teeth. J. dent. Res. 39,93-98. HODGE, H. C. and Sr.or~, F. A. 1954. Some public health aspects of water fluoridation. In: SHAW, J. H., Ed., Fluoridation as Public Health Measure, pp. 79-109. Am. Ass. Adv. Sci., Washington. ISAAC, S., BRUDEVOLD,F., Shnru, F. A. and GARDNER,D. E. 1958. The relation of fluoride in the drinking water to the distribution of fluoride in enamel. J. dent. Res. 37, 318-325. JENKINS,G. N. 1966. Chemical composition of teeth. In: The Physiology of the Mouth (3rd Ed.), pp. 71-75. Blackwell, Oxford. JENKINS,G. N. and SPEIRS,R. L. 1953. Distribution enamel. J. Physiol. 121, 21. Abstract. L~ITLE, M. F., CASCIANI, ROWLEY,J. 1967. Site of fluoride accumulation erupted human Archs oral Biol. 12,839-847. MCCANN, H. G. 1969. The effect of fluoride complex formation enamel. Archs oral Biol. 14, 521-531. LIKINS, R. C. 1951. Fluorine in human teeth in relation to fluorine in the drinking water. J. dent. Res. 30, 172-176. MILLER, I. J. 1965. Dental Fluorose of International Science Publishers, removal of enamel layers and its suitability MUHLER, J. C. 1969. Ingestion Health, Vol. I, pp, 11-34, 11-49, W. H. O., MUMMERY,R. F. 1869. On the relations amongst the inhabitants amongst existing aboriginal
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