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ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: deciduous dentition • development • eruption • pig • premolar • teeth
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Surprisingly, dental eruption in commercial breeds has not been formally examined except in classic growth experiments (Tonge and McCance, 1973; Wenham and Fowler, 1973). As such, normal profiles for the eruption of the deciduous dentition have not been previously reported. However, a recent study showed that premolar eruption was positively associated with the amount of time piglets spent at the creep feeder beyond 21 d of age (Tucker and Widowski, 2008), making dental eruption an area of interest for the commercial sector.
Within the swine industry, adequate feed consumption before and at the time of weaning is of critical importance. Failure to consume sufficient feed can increase susceptibility to disease (McCracken et al., 1999), decrease the absorptive capacity of the gastrointestinal system (Kelly, 1990; Pluske et al., 1996), and exacerbate other stressors commonly experienced at weaning (Close and Stanier, 1984; McCracken et al., 1995). Long-term effects include increased time needed to reach market weight (Tokach et al., 1992; Pollmann, 1993).
Although the swine industry has grown considerably with regard to improvements in feeds, feeding systems, and genetic potential for growth, studies considering the hardware required to consume that feed (i.e., teeth), and to thus fulfill that potential, have largely been neglected. It is important to know not only when deciduous teeth are erupting but also to identify factors that can affect their eruption. The purpose of this study was to examine dental development in commercial swine and identify maternal, litter, and piglet factors. Sequence of tooth eruption and reversals in eruption order (i.e., polymorphisms) were also examined.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Animals
Two hundred thirty-three Yorkshire piglets from 24 litters (8 litters per trial) were obtained from the University of Guelph Arkell Swine Research Station. Synchronized breeding of sows and, if necessary, inducement of parturition via intramuscular injection of 175 µg of Estrumate (Schering-Plough, Kenilworth, NJ) were employed to ensure all piglets were born at the same gestational age on the same day within each trial. All piglets were processed (tail-docked, injected with iron, ear-notched, boars castrated) before 3 d of age and remained with their sow in standard farrowing crates until 28 d of age, at which time they were weaned as litter groups. Only 7 piglets were weaned together from each litter (for use in a subsequent study), so that the final examination period (d 35) had only 168 individuals included. Piglets were chosen for weaning to best balance for sex and birth weight. Animals were weighed with a Cardinal 738 Digital Indicator (Cardinal Scale Manufacturing Co., Webb City, MO) on d 2, 6, 13, 20, 27, and 35; weekly ADG were calculated for each piglet.
Housing and Feeding
The farrowing room had natural lighting but was also illuminated with fluorescent light from 0530 to 1730 h. Temperature was maintained between 23 and 25°C, and floor heating was also provided. A commercial starter creep feed (Starter Advance Crumble, Floradale Feed Mill Limited, Floradale, Ontario, Canada) was added to triangular 14-gauge, 4-hole corner creep feeders (41 x 29 x 29 cm) on d 5 and was replaced every other day to ensure freshness. Water was provided ad libitum to piglets via nipple drinkers.
Determination of Gingival Emergence
For the purposes of this paper, all deciduous premolars are referred to simply by a lowercase p with a superscript (or subscript) number indicating its position within the maxilla (or mandible). For example, p3 is the third maxillary premolar, whereas p4 is the fourth mandibular premolar. Deciduous incisors and canines follow the same nomenclature but with the lowercase letter i and c, respectively.
At ages 2, 6, 9, 13, 16, 20, 23, 27, and 35 d, a complete oral exam was performed on each piglet. Emergence of teeth was considered to have occurred when any portion of the crown had penetrated the gingiva (Smith, 1994). Piglets were held in dorsal recumbency using a v-restrainer so that the researcher could look down into the oral cavity. The mouth of the piglet was gently held open with a speculum to visually examine all quadrants of the dental arches (right and left maxillary, right and left mandibular) in addition to the tongue, gums, cheeks, and throat. Occasionally, the use of a metal dental prod was necessary to determine whether the gingiva was still covering a tooth. The tactile sensation of metal on gum tissue vs. metal on hard dentine is quite distinct and effective at identifying whether a thin transparent gingival covering was still present over the tooth crown. For all piglets, every tooth within the oral cavity was recorded on a diagram as being erupted or not (Figure 1).
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Statistical Analysis
Age of Eruption.
Because the emergence of a tooth might have occurred between actual examination periods, and thus bias results, a correction factor was added to better estimate the time of emergence. This correction factor was one-half of the time between the observation period when a tooth was seen to have emerged and the previous period when no emergence was recorded (Van Nievelt and Smith, 2005). For example, if a tooth was absent at d 9 but had erupted by d 13, the estimated time of emergence was d 11. If a tooth had not emerged in over 95% of the population by the last examination day then it was excluded from analysis. This occurred for the i2, p2, and p2.
Emergence times for both right and left dental arches were recorded, but discrepancies were minimal, so data from both sides were averaged. All data were formally examined for normality using the Shapiro-Wilk, Kolmogorov-Smirnov, Cramer-von Mises, and Anderson-Darling tests. Comprehensive residual analyses were conducted to assess the ANOVA assumptions. These included plotting the residuals against explanatory variables and predicted values to visually check for equality of variance, outliers, and other patterns in residuals. The eruption times for i1, i1, and p3 were log-transformed to ensure normality.
To determine what factors were associated with eruption times for each tooth within the oral cavity and needle teeth length, analyses of covariance (PROC MIXED) were used with the following model:
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where Yijklm = response variable (eruption time in days, needle teeth length), µ = overall mean, Gi = fixed effect of sex, BWj = BW, WGj = weekly BW gain, Pk = sow parity, Ak = sow age, NBAk = number of piglets born alive per litter, SBk = number of stillborns per litter, Mk = number of mummies per litter, MFk = male:female ratio of the litter, Tl = random effect of trial, Lm = random effect of litter, and eijklm = the random error term. All data were analyzed using SAS (SAS Inst. Inc., Cary, NC).
Sequence of Eruption.
Sequence of eruption was determined by numerically ranking emergence of each tooth (1 to 12) within each individual piglet and then calculating a mean rank for each tooth across all individuals (Van Nievelt and Smith, 2005). Ordering the mean rank values gave the chronology of eruption for this population.
Polymorphisms.
To examine how often deviations in eruption sequence occur, polymorphisms were examined. Polymorphisms in dental eruption (alternative eruption sequences) follow the conventions of Smith (1994), in which reversals occurring in over 15% of the population are significant enough to be included within a set of brackets within the sequence order [e.g., (p1 i1) p3 p2]. When polymorphisms occur in over 40% of the population, the 2 teeth will have an equal sign placed between them in brackets (e.g., [p1 = i1] p3 p2).
To test whether any polymorphism was indicative of a specific sex or pattern of growth, goodness of fit tests (chi-square) were employed. For birth weights and weekly ADG, the population was split into 3 categories. Large piglets (n = 37) were those with BW (or gaining) above 1 SD of the population mean, whereas small piglets (n = 37) were those with BW (or gaining) below 1 SD of the mean. All other piglets were considered to be of average in size and growth (n = 159).
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RESULTS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Of the 233 piglets examined, all piglets had their 8 needle teeth (i3, i3, c1, c1) erupted at birth. Additionally, 1 piglet was born with erupted i1, i1, p3, and p4, and 5 more piglets had their i1 erupted. All 6 individuals originated from 2 litters. On the last examination day (d 35), 7 piglets had their i2 erupted, 3 had their i2 and p2 erupted, 1 piglet had her i2 and p2 erupted, 3 had their p2 erupted, and 1 piglet had his p2 erupted. Nine of these piglets originated from 3 litters and the remaining 4 from separate litters. Seven piglets did not have their p4 erupted by age 35 d.
Heavy staining of the needle teeth from deep yellow to very dark brown was also noted in at least some piglets from every litter. Dental caries were noted in central incisors within a week of their eruption for many piglets.
Age of Eruption
The age at which deciduous dental eruption occurred is given in Table 1. Significant differences were found between the sexes for all molariform teeth (p3, P = 0.001; p4, P = 0.006; p4, P < 0.001) and for i1 (P = 0.004) with the teeth of females erupting earlier than the teeth of males. The average difference in timing between the sexes was relatively small for all teeth (range: 0.41 to 1.04 d).
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Maternal characteristics found to be significant were parity and age of the sow in the eruption of i1 (P = 0.025; P = 0.013), with the older and greater parity sows having piglets with earlier eruption. No litter characteristic (number of piglets born alive, number of stillborn piglets, number of mummified piglets, male/female ratio of the litter) was found to be significant in the eruption timing of deciduous teeth.
Sequence of Eruption and Polymorphisms
By d 35, only 11 piglets had their i2 erupted (4.7% of the population), 6 had their p2 erupted (2.6%), and 2 had their p2 erupted (0.9%); therefore, these teeth were not included in the sequence or polymorphism analyses.
The mean sequence of eruption as determined by rank order for all other teeth was i1, m4, and m3 for the mandible and p3, i1, and p4 for the maxilla. Overall, the mean sequence of eruption was i1, p3, p4, i1, p3, and p4. After examining polymorphisms within each quadrant for male and female animals (Figure 2), there were several consistently large polymorphisms (>40%). In gilts and barrows, the left p3 was seen to erupt before the left i1 in 59% of cases. Within the right maxilla, 56% of gilts and 57% of barrows had this same polymorphism. Within the mandible, the left i1 was seen to erupt before the left p4 for 44% of females and 57% of males. Within the right side this reversal occurred in 53% of females and 46% of males. Thus, the sequence of eruption should be rewritten as [i1 = p4] p3 for the mandible and [p3 = i1] p4 for the maxilla.
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Tooth Length
Incisor length was not measured in the final trial, resulting in only 154 animals from 16 litters being examined. Sex was the only factor influencing incisor length (P = 0.0263), with males having longer incisors than females (males, 5.71 ± 0.048 mm; females, 5.56 ± 0.055 mm).
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DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Because teeth are often considered to be more resistant than other body tissues to developmental and nutritional insults (Garn et al., 1965a,b), they are often studied both within and across species as indicators of somatic growth and maturation. This is the first study to examine the chronology and age of eruption of the deciduous dentition in domestic large breed pigs over a scale of time necessary to detect sex and growth differences. It is also the first to report on polymorphisms in any breed of swine.
Previous authors have listed tooth development in large breed pigs, but have only examined animals at intervals of birth, 4 wk, and 4 mo of age, and they combined data from both the mandibular and maxillary jaw (Tonge and McCance, 1973). Others have presented data in visual form but do not list any summary statistics (Wenham and Fowler, 1973). Although Tonge and McCance (1973) did not distinguish between the mandibular and maxillary teeth, several differences from the current study can be noted based on the information they provide. They list eruption of i1 along with the i3 and c as occurring at 93 d of gestation. In addition, they list both the p3 and p4 as erupted at birth. Likewise, Wenham and Fowler (1973) show eruption of p3 and p4 as having occurred at birth. Regardless of the jaw examined, none of these teeth were regularly seen to be erupted at birth in the current population (with the exceptions of c and i3), indicating the modern piglet may have later eruption times than those examined in the 1970s.
It has often been speculated that dental eruption may be advanced or delayed in response to changes in husbandry and breed selection. In the current study, we examined the same breed as Tonge and McCance (1973), and so it is interesting that they list the eruption of i1 as occurring at the fetal stage of 93 d, whereas we did not see mean eruption occurring until 4.60 to 10.02 d after birth. A difference of 24 to 30 d is difficult to attribute to any recording errors or methodological variation, especially when the definition for eruption is identical in both studies.
That the majority of all teeth examined erupted earlier in gilts than barrows is in contrast to several studies on miniature pigs in which no sex differences were found in the eruption or further development of teeth (Weaver et al., 1962, 1966, 1969; McKean et al., 1971). However, sex differences have been noted in other species, such as certain human populations (Tanguay et al., 1984; Uysal et al., 2004), sheep (Ho et al., 1989), mandrills (Setchell and Wickings, 2004), and squirrel monkeys (Galliaria and Colillas, 1985).
Interestingly, of all cheek teeth to erupt, it was only the molariform ones (p3, p4, and p4), and not the sectorial mandibular premolar (p3), that displayed sex differences. Herring and Wineski (1986) examined the relationship between dental development and chewing behavior in miniature pigs and found that initial chewing of nonfood items commenced after the first sectorial cheek teeth (p3) began erupting (within 1 wk postpartum), whereas mastication of food items began shortly after the molariform molars had erupted (at around 3 wk of age). In the current study, the sectorial p3 erupted after both the molariform p3 and p4, which indicates a difference between miniature and large breeds of swine.
If molariform teeth are a developmental precursor to initial chewing of solid food, and sex differences were found, we might expect evidence for sex differences in solid feed intake. Delumeau and Meunier-Salaün (1995) did find that gilts performed more creep feeding behavior before weaning and had greater estimated feed intakes both before, and in the first 4 d after, weaning. These authors suggested that gilts may have greater adaptive performance, whereby they are more efficient at learning a novel behavior (i.e., feeding) as compared with barrows. Likewise, Bruininx et al. (2001, 2002, 2004) reported that gilts had shorter latencies to their first meal, consumed more feed in the 24 h after their first meal, visited the feeder more frequently, and consumed more in their first 2 wk of weaning. It is unlikely that molar eruption alone could explain those sex differences, although other dental characteristics such as occlusion may contribute to them.
The fact that molars might be erupting later in modern pigs may have consequences for when piglets naturally shift from the suckling stage of ingestion to independent ingestion. Currently, commercial weaning in North America occurs between 17 and 21 d of age, at which time piglets must begin consuming a solid diet. As previously mentioned, initial consumption of solid food in miniature breeds of pigs was seen to commence when the molariform molars had erupted at around 3 wk of age (Herring and Wineski, 1986). Unfortunately, in the present study, we examined only the initial eruption of molars and not complete eruption or occlusion. However, we know that voluntary consumption of solid feed has repeatedly been shown to begin only after commercial piglets reach 20 to 21 d of age (Pajor et al., 1991; Delumeau and Meunier-Salaün, 1995; Puppe and Tuchscherer, 2000), thus the prospect that further molar eruption and occlusion might influence this dietary shift is very intriguing, especially given that other body and growth measures have been equivocal in explaining why piglets begin consuming solid feed. It also provides an example of how relevant physiological information may assist us in choosing an appropriate weaning age for the young piglet.
Delays in eruption for all teeth have been attributed to several causes. In humans, 3 distinct etiologies have been identified, though only the third may be relevant to the animals in this study. The first involves any mechanism of physical disturbance such as trauma, infection, abnormal tissue growth or fusion, crowding, or supernumerary teeth (for review see Wise et al., 2002). The second originates from abnormal bone development, such as with craniofacial dysostosis, hormone insufficiencies like hypothyroidism and hypopituitarism, in addition to several genetic syndromes (Wise et al., 2002). The third, which has been evidenced in numerous human populations (Shaw, 1970; Delgado et al., 1975; Moore et al., 1986), is systemic stress that is often nutritional in nature.
In domestic swine, several authors have shown the effects of severe undernutrition on the development of teeth and bone (McCance and Ford, 1961; Tonge and McCance, 1973). Retarded growth in both the maxillary and mandibular jaw led to permanent disorganization of the dentition with malocclusion, overcrowding, and impaction seen in all teeth. Although both the deciduous and permanent dentitions were delayed in their eruption, the growth disturbance was not equivalent to that of the jaws because eruption did eventually occur, regardless of whether their supporting bones could ever attain the size necessary to accommodate them. The authors note that "the growth of teeth were closely linked to chronological age, more so than the bones." (Tonge and McCance, 1973). These authors also give ample evidence to suggest that teeth are responsive to nutritional disturbance beyond just a delay in eruption because some molars failed to develop completely, whereas other molar crowns were reduced in size and many molar roots were stunted. Attrition (tooth-to-food wear) in deciduous teeth and permanent teeth was also more severe in nutritionally restricted animals, which the authors speculated was due to their extended retention or by "some growth disturbance in the structure and chemistry of the teeth" (McCance and Ford, 1961).
Given that teeth begin developing in utero, it follows that maternal condition would be influential to this process. In mice, maternal stress imposed during late gestation has been shown to delay the eruption of teeth in offspring (Meek et al., 2000). However, no such relationship has yet been investigated in other species. Sows are often both restrictively fed and confined during gestation, and these conditions have the potential to decrease the overall welfare of the sow (Appleby and Lawrence, 1987; Rhodes et al., 2005); thus, these practices may influence the timing of tooth eruption for piglets, though further research is needed in this area. Regardless of their size and metabolic differences, sows are generally fed by volume in commercial units so their individual nutritional planes are unlikely to be the same. However, no sow in this study was seen to be in a noticeably low nutritional plane, based on routine visual inspection of their body condition. Water quality, which can vary in its mineral content and also affect dental development (Rugg-Gunn and Hackett, 1993), was supplied from the same source and was unlikely to be a cause of variability within this study.
One factor relating to growth in utero, and which had a significant effect on eruption time for all teeth examined (except i1), was birth weight. Larger piglets generally had earlier eruption in all their teeth. Although litter size was accounted for in the analysis, smaller BW for age piglets are often observed in larger litters (Van der Lende and de Jager, 1991; Milligan et al., 2002). Because the swine industry has increased sow productivity tremendously since previous dental studies on large breed pigs were conducted (Tonge and McCance, 1973; Wenham and Fowler, 1973), it may be that our observed differences in eruption times do in fact relate to a greater proportion of smaller individuals being born in the population.
The facts that many piglets were seen to have discolored teeth at birth and developed dental caries soon after birth are also related to conditions in utero. Staining of teeth has been noted in miniature breeds of swine, although age of onset was not provided (Gier, 1986). Intrinsic staining of dental tissues occurs during tooth development and can be caused by several metabolic disorders, excess fluoride intake, tetracycline administration, vitamin D deficiency, or any disturbance affecting the normal development of dentine or enamel (for review see Watts and Addy, 2001). Fluoride can be inadvertently supplied in excess to pigs in the diet or in water, and this has been shown to affect both the bones and teeth of parent and offspring (Speirs, 1980; Morés et al., 1999). Likewise, tetracycline is a common antibiotic administered to sows during gestation, even though it is strictly avoided during human pregnancies for its calcification into fetal dentine and enamel (Watts and Addy, 2001).
The fact that dental caries were occurring within weeks of birth indicates that enamel was not laid down sufficiently in utero. Enamel protects underlying dentine against environmental and nutritional insults and is laid over dentine during the formation of the tooth. Defects in this tissue are permanent and can greatly reduce the integrity and longevity of the tooth (Kierdorf et al., 2004).
Needle Teeth Length
Piglets are born with 8 sharp needle teeth comprising the 3rd incisors (i3, i3) and canines (c) in each quadrant of the mouth. These teeth angle outwards and are used when establishing a teat order during the first days of life. Fraser and Thompson (1991) suggested that these teeth evolved as weapons against siblings in response to competition for teats. Indeed, they demonstrated that among smaller piglets, those having intact needle teeth had greater BW gains and were more successful in gaining access to anterior teats compared with piglets which had their needle teeth removed by clipping. Those authors suggested that an arms race in weaponry (i.e., dental development) may have resulted in the highly advanced dentition seen in piglets at birth.
Our examination and analysis of needle teeth length resulted in only a difference in sexes being observed such that males displayed longer incisors than females. Although it might be expected that males have longer canines simply because their adult counterparts become extended into tusks, we did not expect to find such a difference in incisors simply because their function within the deciduous and permanent dentition would appear similar for both males and females. Because length measurements were taken only once, and on a single tooth, we cannot know whether this sexual dimorphism is also a trend for the rest of the dentition. Interestingly, we did not see any relationship between the size of needle teeth at birth and future growth of piglets, which might be expected if an arms race was actively occurring. However, the forces of natural selection can be either highly constrained or left untouched under commercial rearing conditions; thus, our lack of evidence supporting this hypothesis cannot be taken as proof against it.
Sequence of Eruption and Polymorphisms
Yorkshire piglets in this study had a different sequence of eruption from the Pitman-Moore strain of miniature swine. In Yorkshire piglets, the first maxillary incisors erupted after their third premolars, compared with erupting before them as in the case of miniature pigs (Weaver et al., 1966). This variation was found to be highly represented within the current population and can be considered a highly significant polymorphism. Because the eruption sequence within a species is considered to be a highly adapted feature, with changes often giving insight as to how an animal adapts to its environment over time (Smith, 1994), we can only speculate as to what selection pressures may have led to these changes and whether they are in fact adaptive.
In conclusion, this is the first study to examine deciduous tooth eruption and the key factors influencing eruption times in domestic large breed commercial pigs. These results clearly indicate that considerable variation in eruption times exists among individuals and litters. As well, substantial differences in the timing of molar eruption were found between the current study and earlier studies, indicating the need for current knowledge regarding the developmental physiology of our domestic animals. Further research investigating the relationship between tooth eruption and feeding behavior in the young pig is needed to provide a more comprehensive picture of feeding ability and feeding potential. As well, additional research is needed to determine how dental integrity and dental health influence feeding ability and overall health in the herd.
1 Corresponding author: atucker{at}uoguelph.ca
Received for publication September 19, 2008. Accepted for publication March 19, 2009.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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