Correspondence between enamel hypoplasia and odontometric bilateral asymmetry in Australian twins.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 126:177–182 (2005) Correspondence Between Enamel Hypoplasia and Odontometric Bilateral Asymmetry in Australian Twins Robert S. Corruccini,1* Grant C. Townsend,2 and Wendy Schwerdt2 1 2 Department of Anthropology, Southern Illinois University, Carbondale, Illinois 62901-4502 Dental School, University of Adelaide, Adelaide 5005, South Australia KEY WORDS enamel hypoplasia; odontometrics; directional asymmetry; ﬂuctuating asymmetry; Australians; twins ABSTRACT Four aspects of enamel hypoplasia of the maxillary central incisor and mandibular canine (hypoplasia presence, width, cumulative width, and crown position) were correlated with directional and ﬂuctuating measures of bilateral odontometric asymmetry in a large panel (n ⫽ 950) of South Australian twins. Hypoplasia and asymmetry are thought to reﬂect general developmental disruption, but they show few correlations beyond the expected statistical type I error. This may relate to differences in their speciﬁc etiology, the composite nature of overall crown dimensions, a general lack of stress, and the extended period of formation of dental crowns. In contrast, asymmetry is marginally more detectable in a subsample separated according to hypoplastic teeth, suggesting that correspondence may be clearer in comparisons at the population rather than individual level. The most notable difference is the greater variability of asymmetry measures in hypoplastic individuals. Am J Phys Anthropol 126:177–182, 2005. © 2004 Wiley-Liss, Inc. Enamel hypoplasia (EH), a developmental defect visible on the external surface of teeth, and bilateral asymmetry (BA), an odontometric difference between antimeres, continue to attract substantial research attention. A review by Hoover (2001) cited 72 hypoplasia articles and 42 concerning asymmetry that pointed to disturbed growth due to developmental insult as the cause of these anomalies. For instance, Townsend (1983) found sharply increased dental ﬂuctuating asymmetry in Down’s syndrome individuals. Contemporary reviews established that generalized stress between ages 0 –5 years underlies most permanent tooth hypoplasias (Goodman and Rose, 1990, 1991; Hillson, 1996; Larsen, 1997), and this span need not be raised much to encompass the likely range of formation of detectable crown asymmetries. Perzigian (1977) noted increased asymmetry in the Indian Knoll sample as compared with later prehistoric and historic collections, and noted another study suggesting that Indian Knoll also had the most frequent hypoplasia; he did not report individual BA-EH correspondence. Surprisingly, only the analysis by Hoover (2001) seemed to approach this issue. However, some preceding analyses suggested that disrupted calciﬁcation and disturbed odontometric growth relate generally to each other (Rose and Pasley, 1980; McKee and Lunz, 1989; Manzi et al., 1997; Van Gerven et al., 1990), so direct analyses of hypoplasia and asymmetry correspondence seem overdue. On the other hand, there are various theoretical reasons to doubt such a BA-EH correspondence. Po- lar teeth in genetic “ﬁelds” (e.g., ﬁrst molars) may show increased effects of growth canalization but halted calciﬁcation in response to stress (Townsend and Brown, 1980; Goodman and Armelagos, 1985), while nonpole teeth may react differently. Speciﬁc stresses and their duration may affect BA and EH differently. Growth of pulp and dentin contributes to overall crown dimensions, not just enamel. Furthermore, the occluso-gingival position on tooth crowns differs for recording maximum mesiodistal and buccolingual crown diameters, and for the location of EH; perhaps only prolonged or repeated growth disruptions should signiﬁcantly coeffect EH and BA. Twins tend to undergo more morbidity and mortality than singleton human births (Taji et al., 2000; Bryan, 1983; Townsend and Richards, 1990). They are also systematically lower in birth weight than singletons, and low-birth-weight and premature infants show increased enamel hypoplasia of both localized and generalized kinds (Seow, 1997). Therefore, twins offer a valid approach to exploring BA-EH associations. The University of Adelaide has a large collection of high-quality dental casts of © 2004 WILEY-LISS, INC. *Correspondence to: R.S. Corruccini, Anthropology Department, Southern Illinois University, Carbondale, IL 62901-4502. E-mail: firstname.lastname@example.org Received 28 January 2003; accepted 25 July 2003. DOI 10.1002/ajpa.20113 Published online 6 July 2004 in Wiley InterScience (www. interscience.wiley.com). 178 R.S. CORRUCCINI ET AL. twins that formed the basis of the study by Taji et al. (2000) of localized hypoplasia of deciduous teeth. In the same materials, Townsend and Farmer (1998), Townsend et al. (1999), and Dempsey et al. (1995) found rather extensive directional dental asymmetry but no more ﬂuctuating asymmetry than in singletons. Our purpose in this study is to analyze the hypoplasia correspondence to odontometric bilateral asymmetry according to the various quantiﬁcations of both entities, both among individuals and among samples. MATERIALS AND METHODS The dental stone casts, collected as part of an ongoing study of dental and facial development in twins being carried out at the Dental School, University of Adelaide, were obtained during two time periods: an earlier group between 1983–1993, and a second group commencing in 1995 and continuing today. In the ﬁrst project, 308 twin pairs of adolescent-to-adult Australians of European descent living in Adelaide were examined, and records were obtained to determine the relative contributions of genetic and environmental inﬂuences to observed variations in dento-facial morphology. With an approximate median age of 20 in 1985, this sample has a median year of birth of roughly 1965. Adequate casts presenting the appropriate teeth allowed incisor hypoplasia data to be collected for 590 individuals (275 males and 315 females) among these 616 cotwins. The second twin panel comprised 4 –5-year-olds, born in Australia and of European descent, living in Adelaide and Melbourne, whose parents had agreed could participate in a longitudinal study of dental and facial development. Follow-up castings of these children were obtained at around 8 –10 years in 1998 –2000; thus the sample had a modal year of birth of 1990 and fully erupted incisors, but usually did not yet present the erupted permanent canine. This sample comprised 296 pairs in 2001, of whom 360 individuals (176 boys and 184 girls) out of 184 twin pairs allowed adequate assessment of the incisor/M1 group, but only 53 of the canine/premolar group. Thus the total pooled sample size at maximum was 950, but the largest single BA to EH bivariate sample size (owing to missing data) was 818. Data collection methods were approved by the Committee on Ethics of Human Experimentation, University of Adelaide (approval no. H/07/84A), and all participants were informed volunteers. There were 147 monozygotic (MZ) and 148 dizygotic (DZ) pairs in the earlier cohort, and 83 MZ and 101 DZ in the later cohort. Zygosity was determined to more than 99% probability using 17 serum and protein polymorphisms in the earlier cohort, and 6 hypervariable DNA loci in the later cohort. The sex and zygosity variation would be expected more than 33% of the time with random sampling. The procedure one of us (R.S.C.) followed, to diagnose enamel hypoplasia prevalence was based on current recommendations (Goodman and Rose, 1990, p. 92, 1991, p. 281; Goodman et al., 1992, p. 121; Hillson, 1996, p. 172, 2000, p. 253; Larsen, 1997, p. 44 –50). Only two focal teeth most susceptible to hypoplastic calciﬁcation, the permanent maxillary central incisor and mandibular canine, were examined. If either antimere presented a macroscopic linear defect, hypoplasia was scored, provided one of the following conﬁrmatory signs was also present: 1) the defect was a palpable (by ﬁngernail) depression on both antimeres at the same level of the crown; 2) a defect was also observed on a different tooth class of roughly equivalent calciﬁcation timing (i.e., I2 or I1/2 or less likely M1 in concert with I1, or mesial or distal premolars, here referred to as P1/2, or C1 supplementing an observation on C1 at roughly the same crown height); or 3) a lingual as well as labial manifestation of the line circumscribed the tooth. Illuminated magniﬁer observation was only used to conﬁrm and measure, not to initially diagnose, the hypoplasias (Goodman and Rose, 1990; Hillson, 2000). These criteria are in keeping with the current practice of delimiting “deﬁnite” cases. However, if a linear or limited (pitting) phenomenon seemed to be observed (or was only microscopically detectable) but none of the conﬁrmatory signs was found, this was considered a “possible” EH, in keeping with less stringent requirements that seem to have led to very high (90%⫹) hypoplasia prevalences reported for some modern (El Najjar et al., 1978) and many prehistoric (Goodman and Rose, 1990, 1991; Hoover, 2001) samples. Thus ﬁve ranks of scoring were employed (not, possibly, and deﬁnitely present, with two occasional intermediate stages noted between these three). In keeping with Blakey and Armelagos (1985), Hutchinson and Larsen (1988), Larsen and Hutchinson (1992), and especially Ensor and Irish (1995), hypoplasia width was ranked as a separate variable in stages of absent, present but less than 1 mm, between 1–1.5 mm, between 1.5–2 mm, and just one case of ⬎2 mm as judged by a handheld magniﬁer with a reticle. Vertical hypoplasia width may relate to duration of metabolic insult, although hypoplastic area might be a more revealing measure (Hoover, 2001). If there was more than one discrete hypoplasia, their width ranks were added together to create a third variable, total hypoplasia width. Finally, in cases of hypoplasia presence, it was noted whether the event occurred relatively early in calciﬁcation (occlusal 1/3 of crown location), intermediate (middle third), or late (apical 1/3), with borderline cases decided with the reticle. The maximum mesiodistal and buccolingual diameters of the crowns of all emerged permanent teeth were measured following the deﬁnitions of Seipel (1946) and Moorrees et al. (1957). Any teeth in which wear or restorations had affected dimensions were excluded, together with those in which HYPOPLASIA-ASYMMETRY CORRESPONDENCE the stage of emergence precluded measurement of maximum dimensions. Third molars were excluded. The measuring equipment comprised sharpened Mitutoyo digital vernier calipers connected via a multiplexer unit to a computer that provided readings to the nearest 0.1 mm. To estimate the reliability of the measurement procedure, all 56 tooth-size variables were remeasured in 50 individuals selected at random. Mean differences between repeated measurements were small, with none exceeding 0.1 mm. Only 2 of 56 values were signiﬁcantly different from zero, a ﬁnding that can be attributed to type 1 errors at the 5% probability level, and which indicate no systematic differences between ﬁrst and second measurements. The technical error of measurement, or Dahlberg statistic (Dahlberg, 1940), averaged 0.06 mm, with a range of 0.04 – 0.07 mm. The reliability of the measurement technique was also estimated as the ratio of true to observed variance, where the true variance was calculated as the observed minus the error variance. For our test-retest data, the estimated reliability of measuring the dental casts was 0.98, on average. Odontometric directional asymmetry was calculated as (L ⫺ R)/((L ⫹ R)/2) for each mesiodistal and buccolingual dimension. When using the absolute value of (L ⫺ R), the formula gives ﬂuctuating asymmetry which is irrespective of the larger side. A common alternative formula, log(L) ⫺ log(R), produces directional asymmetries more than 99% correlated with the ﬁrst formula over narrowly varying dimensions such as these. While ﬂuctuating asymmetry has been the norm for most stress assessments in both humans and nonhuman experiments, Corruccini and Potter (1981), Corruccini et al. (1982), Boklage (1987), Hoover (2001), and Townsend et al. (1999) provided cautionary evidence that the directional variant may be just as or even more indicative of environmental responses (especially in nonpolar teeth). For the time being, we relinquish consideration of root mean square and other methods for assessing dentition-wide asymmetry levels, as well as possible multivariate correspondence between assessments of hypoplasia and asymmetry in multiple groups of teeth. These shall remain topics for possible future studies. Correspondence was assessed by using productmoment and rank-order correlations over the entire sample. The former might be the better indicator of strength of relationship. The latter might be more reliable for assessing probabilities for the null hypothesis in the presence of non-normal distributions. The distribution of the ﬂuctuating type of asymmetry and of all hypoplasia measures except crown position (i.e., early vs. late) was decidedly non-normal. In two-sample comparisons, t-tests were used, which with these large sample sizes should be fairly robust despite the non-normalities. 179 As we are testing numerous null hypotheses with the same sample, an adjusted Bonferroni probability of 0.05/N should be the proper critical probability, where N is the number of different variables tested. The use of twins could raise an objection of redundancy of sampling. Genetically, this would be true, but hypoplasias and asymmetries are putatively environmental markers. Nevertheless, one might expect environmental covariance to be channeled by similar genotypes, so a correlated response to environmental exposure could be possible. However, most “deﬁnite” hypoplasias (77%) are discordant between cotwins (Corruccini and Townsend, 2003), and the genetic variance of asymmetries is very low (Corruccini et al., 1988; Corruccini and Sharma, 1989). RESULTS In this and previous studies, there are no obvious consistent differences between males and females or between MZ and DZ individuals for either hypoplasia or asymmetry, justifying pooling into one sample. Correlations between hypoplasia and asymmetry variables total 448 (four hypoplasia variables for each of the two teeth, and both directional and ﬂuctuating types of asymmetry over the 28 mesiodistal and buccolingual dimensions; thus, 8 ⫻ 56). Rankorder correlations and their probability levels differ by minuscule amounts from parametric Pearsonian correlation coefﬁcients, usually only in the third decimal place, as is the conventional wisdom when sample sizes are very large. Therefore, only the productmoment correlations are presented here, despite non-normality. The various hypoplasia measures intercorrelate at about r ⫽ ⫹0.19 between canines and incisors. The width and total width measures very consistently give correlations very close to those for the variable of simple presence (usually differing in only the third decimal place), but also consistently slightly lower. This suggests that no extra information resides in thickness variables as regards their correspondence to asymmetries, so further consideration of the former is omitted here. It is somewhat surprising that usually slightly lower but otherwise thoroughly redundant correlations are found for those thicknesses. Of the 112 correlations between the two hypoplasia positions and 56 asymmetry variables, just four attain the critical probability of P ⬍ 0.05, which is less than expected at random for type I error (0.05 ⫻ 112 ⫽ 5.6), and all are well below the r ⫽ 0.20 level. Therefore, hypoplasia location (whether near or far from the occlusal apex) is considered unrelated to asymmetries of any tooth class. Table 1 shows the remaining information, i.e., nine asymmetry variables which correlate signiﬁcantly with hypoplasia presence. Eight of these involve incisor hypoplasia, and only one involves hypoplastic canines. These are all very low correlations, 180 R.S. CORRUCCINI ET AL. TABLE 1. Correlations that achieved statistical significance between hypoplasia presence and asymmetry at ordinary p ⬍ 0.05 level and at Bonferroni level of 0.05/112 ⫽ p ⬍ 0.00051 Variable r n I1 hypoplasia M1 MD DA C1 MD DA I2 MD DA I2 BL DA P1 BL DA I2 MD FA M1 BL FA P2 BL FA C1 hypoplasia C1 BL FA 0.115* ⫺0.159** ⫺0.084* ⫺0.105* 0.103* 0.120* ⫺0.091* ⫺0.102* 707 469 565 485 459 565 809 436 0.123* 426 1 MD, mesiodistal; BL, buccolingual; DA, directional asymmetry; FA, ﬂuctuating asymmetry. * p ⬍ 0.05. ** p ⬍ 0.0005. so while there may be a signiﬁcant correspondence, there certainly is not a very useful or predictive one. The strongest correlation, r ⫽ ⫺0.159 between incisor hypoplasia and C1 mesiodistal directional asymmetry, does not inspire us with its strength, and furthermore seems rather illogical, as canines and incisors have fairly different calciﬁcation and eruption schedules. However, this correlation alone among the 112 between hypoplasia presence and asymmetry variables falls below a critical Bonferroni probability of 0.0005 (0.05/112). This adjusted alpha probability is divided by the number of repeat tests performed on the same sample of subjects, raising conﬁdence that this might reﬂect a real biological relationship. Another problem in Table 1 is that 2 of 4 correlations involving ﬂuctuating asymmetry are negative, illogically suggesting that hypoplastic individuals tend to show less asymmetry. However, the nine total signiﬁcant ﬁndings exceed an expected type I error rate of 5% (0.05 ⫻ 112 ⫽ 5.6), and there are 33 positive as opposed to 23 negative correlations for the ﬂuctuating asymmetries overall, where 28 each would be the perfectly random expectation. Perhaps therefore there is a real (but very faint) overall hypoplasia-asymmetry correspondence at the level of the individual. There is clearly a difference (Corruccini and Townsend, 2003) in the sharply lowered hypoplasia frequencies in the later (born ca. 1990) twin cohort. This may bear a strong relation to the introduction of ﬂuoridated city water in the study population. Frequencies are about four times as high in the earlier cohort for the “possible” I1 hypoplasias, and all other incisor and canine contrasts are even stronger. In view of the time lag involved in measuring the two cohorts and the paucity of hypoplasias in the later one, pairwise sample comparison of asymmetries according to whether the case did or did not evince a hypoplasia was limited to the earlier cohort. Table 2 shows only those asymmetry variables that differ between the incisor hypoplastic and con- trol subsamples of twins. Of 56 t-tests, only 6 attain a signiﬁcant difference at P ⬍ 0.05, with none at a Bonferroni level of P ⬍ 0.001. Much like the correlation analysis, this gives a weak signal. One result, for buccolingual ﬂuctuating asymmetry of M1, is illogical in that the nonhypoplastic individuals averaged higher values. Logically expectable results attaining convincing levels of statistical improbability for the null hypothesis are attained only when comparing the variability of the asymmetries. One quarter of the 56 F tests for variance are signiﬁcant at P ⬍ 0.05; 6 of these 14 are signiﬁcant even at P ⬍ 0.001. There is consistency also in that most of the BA effects according to EH involve teeth in the same, earlier erupting calciﬁcation group, i.e., permanent incisors and ﬁrst molars. The hypoplastic individuals are quite consistently more variable in asymmetry. This signal is much clearer than it is for any central tendency of asymmetry. The only exception is the buccolingual M1 dimension in both ﬂuctuating and directional asymmetry, where the hypoplastic subsample is signiﬁcantly less variable. In examining the raw data, no outlier values are obvious for this dimension, but in contrast to all the other asymmetries, the largest values for M1 buccolingual asymmetry are consistently associated with individuals showing smaller or reversed asymmetries in other dimensions, and are also associated with contrasting values in the individual cotwin. Perhaps some sort of mirror imagery is involved. DISCUSSION The few asymmetry-hypoplasia correlations attaining nominal statistical signiﬁcance do not attain statistical usefulness, such as an r of greater than ⫹0.50. Overall there is just a hint of meaningful correspondence at the level of the individual, comparable to the results of Hoover (2001). Perhaps the scoring of hypoplasias only in the more susceptible polar teeth of incisor and canine genetic ﬁelds affected results, because such teeth are likely more canalized in their growth response to the same stressors. However, if that were the case there should have been detectable asymmetric responses in the lateral incisors (compared to the maxillary central), and in the premolars and M2 compared to the canine tooth. Nevertheless, it could be that comparisons across stressed and unstressed samples (rather than individuals) could reveal shared differences in asymmetry and hypoplastic calciﬁcation. This approach will be more proﬁtable in prehistoric archeological samples with more variable infection and nutrition proﬁles than the present afﬂuent Westernized subjects. Perhaps in these Australians there simply is insufﬁcient stress of any kind to bring about sufﬁcient growth disruption to cause any measurable correlated response. However, Hoover (2001) found quite similar results among nonelite Imperial Romans. 181 HYPOPLASIA-ASYMMETRY CORRESPONDENCE TABLE 2. Descriptive statistics of asymmetry in earlier (ca. 1965) born subsample divided by maxillary central incisor hypoplasia1 Measure n Directional asymmetry Mesiodistal M1 41 C1 38 M1 38 I2 45 Buccolingual 1 M 42 C1 35 2 I 40 M1 40 P1 39 Fluctuating asymmetry Mesiodistal M1 41 I1 46 M1 38 P2 38 I2 45 Buccolingual 25 M2 M1 42 1 C 35 M1 40 I1 45 Hypoplastic mean (S.D.) n Nonhypoplastic mean (S.D.) F t ⫺0.0014 (0.0384) ⫺0.0121 (0.0296) ⫺0.0146 (0.0480) 0.0036 (0.0477) 474 432 470 524 ⫺0.0003 (0.0271) 0.0029 (0.0263) ⫺0.0006 (0.0240) 0.0013 (0.0337) 2.01** 1.27 3.99** 2.00** ⫺0.17 ⫺3.34* ⫺1.79 0.31 ⫺0.0010 (0.0162) ⫺0.0045 (0.0368) ⫺0.0188 (0.0579) 0.0096 (0.0259) 0.0185 (0.0317) 511 393 446 506 422 ⫺0.0054 (0.0212) ⫺0.0028 (0.0283) ⫺0.0006 (0.0541) 0.0119 (0.0213) 0.0066 (0.0309) 1.71* 1.69* 1.15 1.47* 1.05 1.65 ⫺0.27 ⫺2.03* ⫺0.54 2.29* 0.0243 (0.0296) 0.0183 (0.0206) 0.0243 (0.0437) 0.0280 (0.0267) 0.0343 (0.0329) 474 507 470 393 524 0.0212 (0.0169) 0.0177 (0.0156) 0.0182 (0.0156) 0.0259 (0.0206) 0.0258 (0.0217) 3.06** 1.74* 7.83** 1.67* 2.30** 0.65 0.17 0.85 0.47 1.70 0.0307 (0.0183) 0.0122 (0.0106) 0.0307 (0.0201) 0.0185 (0.0203) 0.0283 (0.0285) 284 511 393 506 511 0.0233 (0.0174) 0.0158 (0.0152) 0.0217 (0.0183) 0.0192 (0.0151) 0.0264 (0.0224) 1.10 2.06* 1.20 1.81* 1.62* 2.01* ⫺2.04* 2.78* ⫺0.20 0.44 1 F is a variance ratio and tests difference in variability, t-tests are of mean difference. * Ordinary two-tailed signiﬁcance at p ⬍ 0.05. ** signiﬁes Bonferroni corrected signiﬁcance at p ⬍ 0.001 (0.05/56). The major noteworthy ﬁnding concerns the increased variability of asymmetry in individuals constituting the hypoplastic sample. Hypoplastic individuals calcify tooth crowns that are both more and less asymmetrical than controls, increasing variance. Perhaps two different processes are at work, one disrupting development and mutually increasing the risk of hypocalciﬁcation and asymmetry, while another sort or intensity of stress incurs canalization of development and therefore decreases asymmetry. Cusps are separately calcifying crown components, whereas overall mesiodistal and buccolingual dimensions are the odontometric norm but probably mask possible asymmetries of individual cusps. Ritter (1991) and Hoover (2001) explicitly demonstrated that cuspal diameters show different associations with known developmental stress and with hypoplasia, are about equally strongly related to hypoplasias, and in some ways may show stronger correlations with hypoplasias. 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