Prenatal and postnatal development of the New Zealand white rabbit (Oryctolagus cuniculus) teeth: An emphasis on histological and computed tomography aspects

doi:10.21203/rs.3.rs-3471526/v1

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Prenatal and postnatal development of the New Zealand white rabbit (Oryctolagus cuniculus) teeth: An emphasis on histological and computed tomography aspects

https://doi.org/10.21203/rs.3.rs-3471526/v1

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published 02 Apr, 2024

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The study reveals that New Zealand white rabbit teeth do not exhibit histomorphogenesis. The teeth development was examined in 28 rabbits from prenatal ages (E19, E23, E25, and E28), neonates (E30), and postnatal age (one and fourteen days). Rabbit teeth first appeared at 19 days of prenatal life as an ectodermal epithelial thickening on each side of the mouth opening. At E23, tooth regular construction is framed from enamel, dentine, and pulp cavity. The peg incisor appearance is visible on the lingual surface of the upper major incisor. Teeth prenatal development went through successive stages like initiation, bud, cap, late bell, maturation, and crown stages. The teeth are composed of the enamel organ and dense mesenchymal tissue. Teeth develop consistently throughout life, having expanded enamel thickness, being diphyodont teeth, having two continuous dentitions, being deciduous and perpetual, with long crown teeth and an open root.

Histomorphogenesis

Rabbit

Teeth

Cementum layer

Enamel organ

Lagomorphic mammals known as rabbits can be distinguished from rodents by their two sets of upper incisive teeth, in which the second pair is located shortly beyond the large incisor, as well as their two designated stake incisors, known as the assistant and beneficial incisors [1]. Moreover, unlike felines, canines, ferrets, and hedgehogs, rabbits lack canine teeth [2]. The rabbit teeth are heterodont teeth of various sorts and different sizes just as assorted shapes (incisors, premolar, and molar) types [3, 4]. The rabbits are most appropriate as the favored exploratory creature for early-stage research because of their high rearing rate, the number of springs, and fast proliferation cycle [5, 6].

The mammalian teeth are fundamental for their life. In the herbivorous mammals, the dental adaptations to accessible eating regimens also archived, for example, a morphological transformation of a finish edge course of action or biting muscle size to amplify biting adequacy [7–9]. The development of teeth is extremely planned in; mice [10], fish [11], or reptiles [12]. Concerning substitution [13].

The rabbit is an appropriate model to contemplate mammalian tooth substitution as opposed to the mouse, as the mouse has a solitary, unreplaced (permanent) tooth set [14]. Moreover, rabbits are alluring model creatures to contemplate tooth development since they are benefiting from wide sorts of vegetation's; besides, they have ceaselessly developed teeth all through life, as every lasting tooth in the hare has a collection of the mesenchymal and epithelium undifferentiated cells in its developing portion, as in all hypselodont animals [15], their dental hygiene was significantly examined in the animal science research [16, 17]; the constantly ever-increasing (hypselodont) teeth of numerous rodents and lagomorphs [18], by increased enamel thickness [19]. The rabbit is extraordinary compared to other comprehensively utilized reenactments for surveying dental embed [20].

The rabbit teeth have certain unmistakable mammalian highlights; they are diphyodont teeth replaced their teeth only once along with their life, [14] for example two continuous dentitions; (deciduous and permanent dentition) and a radicular hypsodont (long crown but no true root) open root [3, 21].

The current investigation is planned to briefly demonstrate and inspect the development of the rabbit teeth using various morphological approaches and some histological staining techniques due to the lack of data illustrating the histomorphogenesis development of rabbit teeth. Therefore, the obtained results may serve as a tool for determining the tooth age of the rabbit embryo and fetus.

Collection of the different examined age-stages of animals

Twelve embryos of New Zealand white rabbits from each of the examined prenatal age phases (E19, E23, E25, E28), neonates (E30), and postnatal age (week and two weeks) were obtained from the pregnant rabbits acquired from the Public Service Center for Veterinary Inspection in the University of Sadat City (USC), Egypt. The day after mating between male and female rabbits has been indicated as embryonic day (E0), as the ovulation in rabbits occurred only after mating by 10–12 hours [22]. Apparently healthy rabbit embryos at days (19, 23, 25, 28), neonates (day 0), and the postnatal age at week and two-week age stages were subjected to euthanasia, in which the rabbits were sedated by anesthesia using sevoflurane (United States Pharmacopeia (USP)) as an inhalational agent to lose consciousness and then slaughtered in the cervical region following euthanasia techniques.

This study was conducted in accordance with ethical guidelines and approved by the Institutional Animal Care and Use Committee. All animal control procedures were carried out following the Rules of the Institutional Animal Care Committee (Alexandria University and the University of Sadat City, Egypt), the Egyptian Ethical Code for studies on experimental animals, and the Use Committee (IACUC), with prior approval for using the animals.

For Histological Examinations:

Six whole embryos from each examined different developmental age-stages of the rabbits (E19, E23, and E25) and the head of fetuses (precanium) along the length of the nasal cavity, i.e., the frontal sutures of E28, neonates, and postnatal age were achieved and fixed in 10% neutral-buffered formalin for examination by light microscopic. The collected tooth specimens from different examined ages of rabbits were pounded briefly in tap water, then fixed in 10% formaldehyde for 48 hours at pH 7.4, then dehydrated in a graded series of ethanol, cleared with xylene, and immersed in melted paraffin. The paraffin-embedded tissues were cut into 4-µm sections using a Leica rotatory microtome (RM 20352035; Leica Microsystems, Wetzlar, Germany) and stained with hematoxylin and eosin [6]. Then, the specimens were grouped: group stained with Haematoxylin and Eosin (H&E) [23] for examination of the general histological features; group stained with Masson’s trichrome [24] for collagen and muscle fiber investigations; and group stained with toluidine blue stains [25]. All stained sections were inspected on the Olympus CHS microscope (Olympus Optical Co., Ltd., Tokyo, Japan).

Photomicrography

The digital images were captured with a digital camera (Olympus DP71 camera) attached to a stereomicroscope (Olympus VM VMF 2x, Eyepiece 10x Stereo Microscope, Japan). An image analysis program, DP Controller, and DP Manager Software were used. There was no adjustment of the captured images except for the adjustment of contrast and brightness in Adobe Photoshop Elements (Adobe Systems, Tokyo, Japan).

Computed tomography (CT scan):

Six whole embryos from each examined different developmental age-stages of the rabbits (E19, E23, and E25) and the head of fetuses (precanium) of (E28), neonates, and postnatal age were achieved and applied using a 64-detector row CT scanner (Somtam Sensation, Siemens, Forcheim, Germany) at 120 kV and 117 mAs, a 10 cm FOV with a slice thickness of 1 mm. The computed tomographical images were reconstructed in dorsal and sagittal planes via software (Syngo CT 2006G, ICS VB28B, Siemens, Munich, Germany).

Histomorphological examinations

Rabbit teeth implicate the ectoderm, which gives enamel, and the mesodermal, which gives rise to dentine and pulp. Rabbit teeth appear firstly as an ectodermal epithelial thickening on each side of the mouth opening entrance appears firstly at embryonic age (E19), as shown in (Fig. 1). At embryonic age (E23), the typical structure of a tooth was formed: an enamel layer, dentine, and pulp cavity, encircled by trabecular bony plates of the maxilla and mandible (which appear within the alveolar bone, either of the maxillary bone or the mandible), as shown in (Fig. 2–4). The rabbit teeth develop consistently all through life; they have increased enamel thickness; they are diphyodont teeth; they have two consecutive dentitions (deciduous and permanent), just as they are portrayed by a long crown tooth with an open root. Rabbits have four upper incisors (major and minor), as shown in (Fig. 3). The minor one is located at the lingual surface of major upper incisors and is called assistant incisors (peg teeth), as appeared in (Fig. 3).

Embryos of rabbit from 16–19 day of gestation:

At the 19-day prenatal rabbit embryo (E19), the tooth primordial showed up as an ectodermal epithelial thickening observed on both sides of the entrance opening to the mouth opening (Fig. 1A-B). Microscopically, these areas were comprised of undifferentiated epithelium cellular collections that constituted the initial indication of tooth development in rabbits (Fig. 1A–D).

Embryos of rabbit at 21 days of gestation:

At the 21-day prenatal rabbit embryo (E21), the upper incisor tooth developed and advanced as a tooth bud. To create the tooth bud, the lower dental layer appeared broader and more aggregated. This type of tooth bud, which was surrounded by mesenchymal connective tissue and was made up of many condensed epithelium cells, could be simply differentiated from the larger, less condensed vestibular layer (Fig. 2A). However, the lower incisor tooth first emerged as a cap phase in the second phase of tooth formation. The enamel layer and underlying thick mesenchymal tissues made up the cap-shaped tooth. The exterior enamel epithelial cells, the interior enamel epithelial cells, and the stellate reticulum were distinguished as the three layers of the enamel layer. From cuboidal to columnar epithelial cells, exterior and internal enamel epithelium cells were produced. Polygonal, faintly pigmented epithelium cells made up the majority of the stellate reticulum. The dental papilla was created from the tooth mesenchyme that was located beneath the internal enamel epithelial and appeared to have been condensed. The tooth follicle is created by the mesenchyme that covers the tooth germ (Fig. 2B).

Embryos of rabbit from 23–25 day of gestation:

At the 23-day prenatal rabbit embryo (E23), the differentiation of the tooth germ happens at this age compared to previous age stages. Two upper roots of major and minor incisor teeth (peg incisor) that are termed assistant incisor teeth emerged in the rostral part of the embryo head embedded in the alveolar socket of the maxilla, separated by maxillary symphysis. The peg incisor appeared only on the lingual surface of the upper major incisor teeth (Fig. 3A). According to our histological investigations, the incisor tooth had the appearance of the late bell phase. The outside enamel epithelium was connected to the long, pointed dental papilla. It seemed to be rotating into the tooth pulp and becoming highly vascularized. In consequence of the overproduction of tooth enamel at this phase, the inner enamel epithelial cells were differentiated into ameloblasts and became darkly stained. The odontoblasts are formed by cuboidal or low-columnar epithelial differentiation of the tooth pulp's external layer. As a result of the cells' dentin secretions, these cells had a faintly stained color. The enamel matrix was noticeable all around the tooth. The dental pulp seems to have good blood flow. Dental hard tissue growth was linked to the late bell phase of tooth development (Fig. 3A–F).

In addition, at these ages, at the cross-section in the middle part of the head of the embryo, the molar tooth appeared in the form of the crown stage. The tooth crown established the final form and shape in which it expanded, condensed, and made up around 2/3 of the length of the tooth. Also, the dentin was thick; it was thicker closer to the tooth's crown (proximally), and it was thinner downhill till it completely vanished at the tooth's neck. Near the proximal part of the crown, enamels were extremely thick and dense and grew thinner farther away (distally). The pulp of the tooth seemed narrow throughout the crown tooth length while it compressed distally, generating a very short neck at the crown apex (Fig. 4A-C).

The molar tooth germs also achieved their most advanced development around the 25th day of pregnancy (E25), taking the form of cusps in a cross-section in the posterior part of the embryo's head (Fig. 5A). The distal fissure was missing its earlier obliquity and currently extended in a straight pattern across the tooth, while the fissures between the cusps were deeper and more upright. There have been instances where the central cusp has been fragmented into two or three smaller cusps (Fig. 5B). The exterior enamel epithelium's cells have begun to lose their cuboidal form and flattened appearance, penetrating the stellate reticulum as the blood vessels now pierce it (Fig. 5B).

Embryos of rabbit from 28–30 day of gestation:

In a 28–30-day prenatal rabbit embryo (E28–30), the stereomicroscopic observation of the cross-section of the rabbit embryo head revealed the presence of two upper molar teeth and two lower molar teeth (Fig. 6A–B). Both upper and lower teeth were symmetrical to each other in shape (Fig. 6A-F). It consisted of a crown and a root. The root was bifurcated into two halves. By light microscopic examination, the upper molar tooth was formed from a dentin core. The enamel organ covered the dentin on both the labial and lingual sides, while it was absent on the lateral surfaces. A layer of cementum covered the tooth all around on the enamel on both the labial and lingual sides while not contacting the dentine on the lateral side, forming a distance called enamel space (Fig. 7). The lower molar tooth was similar to the upper molar tooth. It was shown that in the lower molar teeth, well-developed ameloblasts were detected with a thin layer of enamel matrix, while the ameloblasts were not present on the other side (Fig. 8).

One to two weeks rabbit:

Teeth grow continuously throughout life; they have increased enamel thickness; they are diphyodont teeth; they have two consecutive dentitions; they are deciduous and permanent; and they have long crown teeth with open roots due to enamel space. At one week, the stereomicroscopic examination revealed that the root of the upper incisor teeth was separated by the maxillary symphysis (Fig. 9A). The upper major and minor incisor check teeth (premolar and molar) were curved (Fig. 9B). The root and crown of the upper incisor (Fig. 9C). In a two-week rabbit, the computed tomographical examination revealed that the upper and lower incisor teeth and check teeth (premolar and molar) were well-developed (Fig. 10A). The stereomicroscopic examination revealed that the root of the upper molar teeth (Fig. 10B).

The rabbits are considered a decent model in embryological examination [6], particularly in dental research. The tooth formative investigations in rabbits were vital to knowing and understanding the components of tooth substitution and improvement in vertebrates [14, 20, 26]. Rabbit teeth lack true roots and have a long anatomical crown. These teeth have open roots and frequently erupt; molar teeth have two laminae and two apical apertures. [3] stated that as a countermeasure to ongoing tooth damage, different forms of dentine precipitate in the pulp chamber of continually growing teeth. According to [27], the mandibular premolars erupt twenty-three days after birth, the mandibular permanent molars erupt nine days later, and the mandibular deciduous molars erupt four days after birth. However, [28] claimed that they typically lose their deciduous teeth before or soon after birth and are born with their permanent teeth. Rabbit teeth lack true roots and have a long anatomical crown. These teeth have open roots and frequently erupt; molar teeth have two laminae and two apical apertures. Histologically, the morpho-differentiation and histo-differentiation occur, and the tooth germs develop to the late bell phase and the cusps phase. However, it is important to note that the timing of tooth eruptions can vary among individual rabbits; additionally, the lack of true roots in rabbit teeth allows for continuous growth throughout their lifespan, which necessitates regular dental care to prevent overgrowth and related health issues.

Our results revealed that the rabbit teeth implicate the ectoderm, which gives enamel, and the mesoderm, which gives rise to dentine and pulp. Additionally, our results observed that the teeth appear firstly as an ectodermal epithelial thickening on each side of the entrance opening to the mouth opening. Likewise, the teeth appeared first on the 19th day of prenatal embryonic age (E19), as an ectodermal epithelial thickening on each side of the entrance opening to the mouth consisted of undifferentiated epithelium cellular collections that represented the first sign of tooth development in rabbits. These obtained results came in agreement with [29] in 2cm CVRL in the Egyptian buffalo embryos and with [30] in the molecular determinants of mouse tooth development. In the interim [31], expressed that, the first tooth appeared in the jugal region at 16-day prenatal embryo life (E16), the bud stage appeared from 17-19-day prenatal embryo age (E17-19), the cap stage on 20-day prenatal embryo age (E20), the early bell stage at 25-day prenatal embryo age (E25), and the late bell, the cusps on 28-30-day prenatal embryo age (E28-30), and the beginning of dentinogenesis, amelogenesis, and cementogenesis from 15 to 30.

According to S Glasstone [32], the epithelium of the mouth began to thicken locally at the 13-day prenatal embryonic age (E13), and this thickening only results in the formation of a thin continuous band in the molar region. The general dental lamina was formed by the thicker epithelial cells that penetrated the underlying tissue about 24 hours later. This lamina was composed of two distinct layers of cubical epithelial cells in the transverse section, along with a dense collection mass of erratically organized flattened epithelium cells between them. There was also a bud-shape thickening structure that constituted the tooth germ's initial appearance by the 15th day of prenatal development (E15). At approximately eighteen days of prenatal embryonic age (E18), the cusps started to develop as a modest dipping of the internal enamel epithelial into the dentine papilla. Two cusps—the disto-lingual and the middle-lingual—have separated after 48 hours. In a comparable direction, the author looked at the differences between rats and rabbits. The tooth germ in the rat is elliptical, whereas the one in the rabbit has the customary bell shape. In the rat, the enamel cord is better defined and lasts for a day after cusp-formation has started, while in the rabbit, it starts to deteriorate as soon as the cusps start to show. The external enamel epithelial cells in the rat maintain their cubic shape until they start to degenerate, while in the rabbit, they do not appear.

Our findings at the 21-day prenatal rabbit embryo (E21) reported that the upper incisor tooth development appeared in the form of a tooth bud, in which this bud was composed of many condensed epithelium cells, was simply identified from the larger with less condensed vestibular lamina, and was surrounded by mesenchymal connective tissue while the lower incisor took the cap stage. In addition, our study noticed the cap-like tooth consisted of an enamel structure and underlying dense mesenchymal tissue. The enamel consisted of three layers: the external and internal enamel epithelium and the stellate reticulum. These perceptions match [29] in 11 and 21 cm CVRL buffalo embryos. Our findings at 23-day prenatal embryonic age (E23) demonstrated that the typical tooth structure is formed from the enamel layer, the dentin, and the pulp cavity, which are surrounded by trabecular bony plates of the maxilla and mandible (which appear within the alveolar bone, either the maxillary bone or the mandible).

At the current investigated 28–30-day prenatal embryo age (E28–30), the developed tooth consisted of a crown and root. The root was bifurcated into two halves, and with the help of the examination under the light microscope, it had a dentin core. An enamel organ covered the dentin on both the labial and lingual sides, while it was absent on the lateral surfaces. A layer of cementum covered the tooth all around the enamel on both the labial and lingual sides while not contacting the dentine on the lateral side, forming a distance called enamel space. The current work reported that the lower molar tooth was similar to the upper molar tooth. It was shown that in the lower molar, well-developed ameloblasts were detected with a thin layer of enamel matrix, while the ameloblasts were not present on the other side. These observations were accepted by [3, 28, 31, 33]. The pulp chamber included typical pulp tissue and was lined by an odontoblastic layer that was covered by the dentine and enamel layers from its outside surface. Cellular cementum, enamel, and dentine layers were covered on the side facing the groove between the two laminae. Additionally, it was clear that the enamel layer lining the groove was thinner than the enamel layer covering the cementum-coated exterior tooth surface.

[34] claims that two days prior to the enamel formation, at around 21 days into the pregnancy, blood vessels began to enter the rat's enamel organ. Contrarily, the current research found that in rabbits, blood vessels do not enter the enamel structure at any point during tooth formation, despite the fact that many blood vessels exist at the time of enamel development close to the degenerating stellate reticulum. The lingual portion of the deciduous precursor is where new teeth in mammals begin to form [35]. Similar to the ferret and fruit bat, the development of the dental lamina at the lingual side of the tooth initiates the replacement of teeth in rabbits [36, 37]. After then, there may or may not be a gap between the dental lamina replacement, the oral epithelium, and the first primordial teeth. The tooth's link to the oral epithelium was lost first. The rabbit dental lamina replaces the mesenchyme prior to the development of permanent teeth, as was described in pigs [38] and with reference to the fruit bat or the ferret [35, 37].

A study in New Zealand found that rabbit teeth do not exhibit histomorphogenesis. The teeth development was examined in 28 rabbits from prenatal ttill postnatal ages. The teeth first appeared at 19 days of prenatal life as an ectodermal epithelial thickening. The teeth went through stages like initiation, bud, cap, late bell, maturation, and crown stages. The teeth are composed of an enamel organ and dense mesenchymal tissue. The enamel organs are segmented into three layers: external, internal, and stellate reticular. The cement layer covers the teeth on both the labial and lingual sides, forming enamel space. Teeth develop consistently throughout life, with expanded enamel thickness, diphyodont teeth, two continuous dentitions, deciduous and perpetual teeth, long crown teeth, and an open root.

Data Availability Statement: Research data are not shared

Funding: Open access funding is provided by the Scientific, Technology, and development Funding Authority (STDF) in cooperation with the Egyptian Knowledge Bank (EKB). The current study has not received any funds from any organizations or institutions.

Competing interests: None of the authors have any financial or personal relationships that could inappropriately influence or bias the content of the paper.

Ethical approval and Consent to Participate:

This study was carried out with the ethical permission from the faculty of Veterinary Medicine, Alexandria University, and approved by Institutional Animal Care and Use Committee (ALEXU-IACUC) (Approval code: 182/2022/31/10/2022). All methods were performed in accordance with relevant guidelines and regulations by the Basel Declaration and the International Council for Laboratory Animal Science (ICLAS). The anatomical nomenclature was applied according to Nomina Anatomica Veterinaria[39].

Consent for publication: Not applicable.

Consent to participate: Not applicable.

Availability of data and materials:

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgment

The researchers would like to acknowledge all members of team work of this research in the university of Sadat city and Alexanderia university.

Author contributions

S.H., Seham Haddad; N.A., Nazema Abdel-Meged; M.A., Mohamed Abumnadour.

S.H., M.A., and N.A. wrote the manuscript. S.H. and N.A. collected the sample, performed the histology, M.A. prepared the figures, and M.A. and S.H. revised the manuscript..

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No competing interests reported.

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Prenatal and postnatal development of the New Zealand white rabbit (Oryctolagus cuniculus) teeth: An emphasis on histological and computed tomography aspects

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Journal Publication

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Abstract

Figures

Introduction

Material &Methods

Collection of the different examined age-stages of animals

For Histological Examinations:

Photomicrography

Computed tomography (CT scan):

Results

Histomorphological examinations

Embryos of rabbit from 16–19 day of gestation:

Embryos of rabbit at 21 days of gestation:

Embryos of rabbit from 23–25 day of gestation:

Embryos of rabbit from 28–30 day of gestation:

One to two weeks rabbit:

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1