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Address for Correspondence: Shaibu Mohammed ATABO • E-mail: mohakosh@yahoo.com

Received Date: September 23, 2020 • Accepted Date: March 17, 2021 • DOI: 10.5152/actavet.2021.20060

Available online at actavet.org

Abstract

This study aimed to determine the development time of the sutures and foramina of the skull in fetuses of 350 sheep ob-tained from Northern Nigerian abattoirs. They were separa-ted into 7 age groups and their heads collected and proces-sed using the Alizarin technique. A total of 12 neurocranial sutures were observed in the first and second trimesters; 5 and 7 neurocranial and viscerocranial sutures respectively. In the neurocranium, the cornual and interfrontal sutu-res were established at 48th–50th day and 51st–53rd days of gestation respectively, whereas the occipital sutures were both identified at 61st–67th days of gestation. The anteri-or fontanelle appeared in the second trimester, although earlier in Yankasa than in Balami and Uda breeds. However, the posterior fontanelle, interparieto-parietal sutures, and

lambdoid sutures were absent. In the viscerocranium, the zygomaticomaxillary and maxilloincisive sutures appeared on the 45th–47th days. The frontonasal sutures were seen on the 54th–56th days; the lacrimomaxillary sutures, lacrimoz-ygomatic sutures, and frontolacrimal sutures appeared on the 61st–67th days. In the 3 breeds, the suture formation occurs at a similar time interval; sutural development is slower in the neurocranium than the viscerocranium; and intrasutural closure of the cornual, interfrontal, frontonasal, zygomaticomaxillary, and maxilloincisive sutures occur as early as the second trimester.

Keywords: Breeds, foramen, neurocranium, sheep, suture, vis-cerocranium

Development of the Sutures, Infraorbital, and Supraorbital Foramina of the Skull in Nigerian Balami, Uda, and Yankasa Breeds of Sheep

Shaibu Mohammed ATABO1, 2 , Abubakar Abubakar UMAR2 , Sani Abdullahi SHEHU2 , Adamu Abdul ABUBAKAR3 1Department of Veterinary Anatomy, Bayero University, Kano, Nigeria2Department of Veterinary Anatomy, Usmanu Danfodiyo University, Sokoto, Nigeria3Department of Veterinary Surgery and Radiology, Usmanu Danfodiyo University, Sokoto, Nigeria

Cite this article as: Atabo, S. M., Umar, A. A., Shehu, S. A., & Abubakar, A. A. (2021). Development of the Sutures, Infraorbital, and Supraorbital Foramina of the Skull in Nigerian Balami, Uda, and Yankasa Breeds of Sheep. Acta Veterinaria Eurasia, 47(2), 98-107.

ORCID IDs of the authors: S.M.A. 0000-0002-9811-4457; A.A.U. 0000-0002-7020-8355; S.A.S. 0000-0001-9573-4274; A.A.A. 0000-0001-8643-4413.

Original Article Acta Veterinaria Eurasia 2021; 47(2): 98-107

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Introduction

The skull sutures are fibrous (synarthrodial/immovable) joints that only occurs in the skull and join the bones of the neuro and viscerocranium (Dyce et al., 2010). The neurocranium su-tures usually have large membranous gaps in the fetus and young individuals usually referred to as fontanelles (anteri-or and posterior) (Slater et al., 2008). These fontanelles play a major role in the process of parturition and is also useful in age estimation and brain ultrasonography. Sutures and fontanelles have been extensively studied in humans (Arey, 1965) and mouse (Kaufman & Bard, 1999); however, till date

limited information (Lakshmi et al., 2013) is available on the development of sutures in domestic animals. To the best of our knowledge, this study is the first attempt to document the development in sheep. Similarly, supraorbital and infra-orbital foramina are the 2 major foramina of the skull with vital roles in clinical practices such as local anethesia during surgical procedures (Hall et al., 2000); however, their time of development is still unknown, especially in domestic animals. Therefore, this study aimed at filling the gap of knowledge on the developmental anatomy of the superficial sutures and infraorbital and supraorbital foramina of the skull in 3 breeds of Nigerian sheep.

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ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Method

Sample Collection and AgingA total of 350 samples comprising of fetal heads from 70 Balami and 140 each of Yankasa and Uda breeds of sheep were used for this study. The Balami was obtained from the Gombe Township abattoir from the Northeast, the Yankasa from Kaduna and Zam-fara state abattoirs, and Uda from Sokoto state abattoir from the Northwest, all in Nigeria. All the heads were discarded fetuses from slaughtered pregnant ewes, and the crown to vertebral rump length (CVRL) of the fetuses used ranged from 3.0–15.0 cm. The pregnant ewes were mated with rams of the same breed. The ages of the fetuses were determined by measuring their CVRL with a tape rule, from the anterior fontanelle down to the base of the tail across the vertebral column, and using the for-mula below. They were divided into 7 age groups within first to second trimester, ranging from 42–67 days of gestation. The fe-tuses were transported in an ice pack to the Veterinary Histology Laboratory of Usmanu Danfodiyo University Sokoto for staining. The study was approved by Institutional Animal Care and Use Committee of Usmanu Danfodiyo University Sokoto (UDUS/FAREC/2019/AUP-RO-5). The fetuses were processed using the Alizarin staining protocol modified from Salaramoli et al. (2015).

A=2.1 (B+17),where A= gestational age (in days) and B=CVRL (cm) (Arthur et al.,1989)

Alizarin Staining ProtocolThe heads together with the neck of the fetuses were skinned and dissected from the body at the base of the neck using a

scalpel blade and fixed in 95% ethanol (Lobal Chemie, Mumbai, India) for 8 hours. The fixed samples were stained in a .3% Aliza-rin red (Lobal Chemie, Mumbai, India) for 17 hours. The samples were macerated using 5% potassium hydroxide (KOH) (Lobal Chemie, Mumbai, India) for 6–24 hours and 10% KOH for 20–24 hours for small and large-sized fetuses respectively. The mac-erated samples were cleared with increasing concentrations of glycerin (Lobal Chemie, Mumbai, India) in distilled water (20%, 50%, and 80%) for 14 hours. It was then placed in a glycerin-dis-tilled water mixture and examined on a stereomicroscope (Kyo-wa Optical Co., Ltd, Sagamihara, Japan, Model number GL99B). The skulls were microdissected on the stereomicroscope from the cervical vertebrae of the neck at the atlanto-occipital joint using the beveled edge of a 24 gauge needle. They were exam-ined and stereo-micrographs captured using a 7.2 megapixel Panasonic Lumix digital camera. The stereo-micrographic im-ages were uploaded on a personal computer, and mapping of sutures and foramina were performed using FastStone Image viewer (FastStone soft, Tburon, CA, USA) to further express the morphological outline of the developing sutures and foramina.

Results

Development and Structure of Sutures of the Skull in Yankasa, Uda, and Balami Breeds of SheepThe landmarks of the sutures begin to appear as the ossifica-tion of the skull bones (neurocranium and viscerocranium) sets in. As the sutures become visible on stereomicroscope, they ap-pear open and wide initially and gradually close.

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Figure 1A Stereomicrograph (a) and Bone Map (b) of The Lateral View of the Skull in a 48-Day-Old Uda Fetus Showing a Transverse Cornual Sutures (CS), Zygomatic Process of Temporal Bone (ZPt), Frontal Bone (FT), and Parietal Bone (PA), Alizarin Red Stain (×6.5)

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Neurocranial SuturesThe landmarks of the neurocranium sutures of the skull ap-peared within the 7 age groups (first and second trimesters) of the Alizarin stained samples. The sutures observed were the occipital sutures (OcS), interfrontal sutures (IFS), anterior fonta-nelle (AF), and fronto-parietal suture/cornual sutures (CS). The times of appearance of these sutures were the same in all the breeds, except in the AF.

On the 48th-50th days of gestation, the CS (fronto-parietal su-ture/cornual sutures ) in the 3 breeds of sheep appeared as a thin, transverse, and membranous tissue on the left and right lateral aspect of the cranium between the bone spicules of the parietal and frontal bones (Table 1, Figure 1). On the 51st–60th days of gestation, the CS of both sides were closed, concaved ventrally, and extended from the caudal margin of the orbit to the fontanelle (Figures 2 and 3).

In the 3 breeds of sheep, the interfrontal sutures (IFS) appeared as a wide caudo-rostral membranous gap between the left and right halves of the developing frontal bones on the 51st–53rd days of gestation (Table 1, Figure 4). On the 54th–56th days of gestation, the membranous gap gradually reduced to a thin longitudinal suture across the length of both halves of the frontal bones (Figure 5), and finally closed on the 56th–60th days

of gestation as the growth of the 2 opposite frontal bones ap-proached each other (Figure 2). On the 61st–67th days of gesta-tion, the IFS fused completely with no trace of the suture line (Figures 3).

The AF appeared on the 57th–60th days in Yankasa and on the 61st–67th days of gestation in Balami and Uda (Table 1, Figure 3). It began as a wide star-shaped soft membranous space at the junction between the parietal and left and right halves of the frontal bones and gradually reduced as the fetuses aged (Figures 2–4). On the 61st–67th days of gestation, the AF re-duced, leaving a small triangular membranous gap (AF), which separated the left and right lateral halves of the parietal bones (Figure 2). Unlike the frontal bones, complete closure of both halves of the parietal bones did not occur in any of the 7 age groups (first to second trimester).

The landmarks of the occipital sutures (OcS) began with the appearance of a coma shaped ossification center of the occipi-tal squamous and bone spicules of the interparietal part of the occipital bone. On the 61st–67th days of gestation (second tri-mester), the OcS became established and appeared as a thin, transverse membranous gap between the ossifying occipital squamous and interparietal part of the occipital bone (Table 1, Figure 6).

ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Table 1Time and Sequence of Appearance of the Neurocranial Sutures of the Skull in the 3 Breeds of Sheep

Age groups (days) BreedsNeurocranial sutures

LS/OISCS IFS AF OcS IPS PFOne Yankasa - - - - - - -(42–44) Uda - - - - - - -First trimester Balami - - - - - - -Two Yankasa - - - - - - -(45–47) Uda - - - - - - -First trimester Balami - - - - - - -Three Yankasa Appeared - - - - - -(48–50) Uda Appeared - - - - - -First trimester Balami Appeared - - - - - -Four Yankasa Closed Appeared - - - - -(51–53) Uda Closed Appeared - - - - -Second trimester Balami Closed Appeared - - - - -Five Yankasa Closed Appeared - - - - -(54–56) Uda Closed Appeared - - - - -Second trimester Balami Closed Appeared - - - - -Six Yankasa Closed Closed Appeared - - - -(57–60) Uda Closed Closed - - - - -Second trimester Balami Closed Closed - - - - -Seven Yankasa Closed Closed Appeared Appeared - - -(61–67) Uda Closed Closed Appeared Appeared - - -Second trimester Balami Closed Closed Appeared Appeared - - -

Note. AF = Anterior fontanelle; CS = Cornual sutures; IFS = Interfrontal sutures; IPS = Interparieto-parietal sutures; LS = Lambdoid sutures; OcS = Occipital sutures; OIS = Occipiointerparietal sutures; PF = Posterior fontanelle

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ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Figure 3A Stereomicrograph (a) and Bone Map (b) of a Dorsal View of the Skull in a 65-Day-Old Balami Fetus Showing a Triangular-Shaped Anterior Fontanelle (AF), a Completely Closed Interfrontal Suture (IFS), Frontal Bone (FT), and Parietal Bone (PA), Alizarin Red Stain (×5)

a b

Figure 2A Stereomicrograph (a) and Bone Map (b) of the Caudo-Rostral View of the Skull in a 51st Day Old Yankasa Fetus Showing an Inter-Frontal Suture (IFS), with a Wide Rostral Part of Inter-Frontal Sutures, Star-Shaped Developing Anterior Fontanelle (AF), Frontal Bone (FT), and Parietal Bone (PA), Alizarin Red Stain (x10)

a b

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ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Table 2Time and Sequence of Appearance of the Viscerocranial Sutures of the Skull in the Three Breeds of Sheep

Age groups (days) Breeds

Viscerocranial sutures

MIS ZMS FNS LMS/LZS FLS/NLS

One Yankasa - - - - -(42–44) Uda - - - - -First trimester Balami - - - - -Two Yankasa Appeared Appeared - - -(45–47) Uda Appeared Appeared - - -First trimester Balami Appeared Appeared - - -Three Yankasa Appeared Appeared - - -(48–50) Uda Appeared Appeared - - -

First trimester Balami Appeared Appeared - - -Four Yankasa Appeared Appeared - - -(51–53) Uda Appeared Appeared - - -Second trimester Balami Appeared Appeared - - -Five Yankasa Closed Closed Appeared - -(54–56) Uda Closed Closed Appeared - -Second trimester Balami Closed Closed Appeared - -Six Yankasa Closed Closed Appeared - -(57–60) Uda Closed Closed Appeared - -Second trimester Balami Closed Closed Appeared - -Seven Yankasa Closed Closed Appeared Appeared Appeared(61–67) Uda Closed Closed Appeared Appeared AppearedSecond trimester Balami Closed Closed Appeared Appeared Appeared

Note. FLS = Frontolacrimal sutures; FNS = Frontonasal sutures; LMS = Lacrimomaxillary sutures; LZS = Lacrimozygomatic sutures; MIS = Maxilloincisive sutures; NLS = Nasolacrimal sutures; ZMS = Zygomaticomaxillary sutures

Figure 4A Stereomicrograph (a) and Bone Map (b) of a Caudo-Rostral View of the Skull in a 60th Day Old Yankasa Fetus Showing Complete Closure of the Inter-Frontal Sutures (IFS) and a Reducing/Developing Anterior Fontanelle (AF), Frontal Bone (FT), Parietal Bone (PA), and Interparietal Part of Occipital Bone (IO), Alizarin Red Stain (×5)

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Through the first and second trimesters, the posterior fonta-nelle (PF) was absent across the 3 breeds of sheep. Similarly, the interparietal bone-related sutures such as the lambdoid su-tures/occipiointerparietal sutures (LS/OIS) and interparieto-pa-rietal sutures (IPS) were yet to develop throughout the 7 age groups from days 42–67 of gestation (Table 1).

Facial (Viscerocranial) SuturesA total number of 7 facial sutures were observed during the first and second trimesters of the 7 age groups. These sutures were frontonasal sutures (FNS), frontolacrimal sutures (FLS), lacrimo-zygomatic sutures (LZS), lacrimomaxillary sutures (LMS), zygo-maticomaxillary sutures (ZMS), nasolacrimal sutures (NLS), and maxilloincisive sutures (MIS).

The ZMS and MIS appeared as a very thin, oblique, and mem-branous gap between the zygomatic and maxillary bones (cau-dally) and the maxillary and incisive bones (cranially), respec-tively, on the 45th–47th days of gestation across the 3 breeds of sheep (Figure 7). On the 54th–56th days of gestation, the 2 sutures were closed throughout their length (Figures 8 and 9, Table 2).

The FNS were seen on the 54th–56th days of gestation across the 3 breeds and appeared as 2 separate and short transverse membranous gaps between the corresponding left and right halves of the developing frontal and nasal bones (Table 2, Fig-ure 10). The gap shrank gradually as the bones developed; and on the 65th day of gestation, the FNS closed (Figure 10).

ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Figure 5A Stereomicrograph (a) and Bone Map (b) of the Caudo-Rostral View of the Skull in a 56-Day-Old Yankasa Fetus Showing a Small Interfrontal Sutures (IFS) and Reducing/Developing Anterior Fontanelle (AF) between the Left and Right Frontal Bones (FT), Parietal Bone (PA) and Interparietal Part of Occipital Bone (IO), Alizarin Red Stain (×10)

a b

Figure 6A Stereomicrograph (a) and Bone Map (b) of a Nuchal View of a 62-Day-Old Balami Fetus Showing the Interparietal Part of Occipital Bone (IO), Occipital Sutures (OcS), and Occipital Squamous (OS), Alizarin Red Stain (×5)

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b

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The LMS, LZS, FLS, and NLS appeared on the 61st–67th days in the developing fetus of the 3 breeds. The membranous gaps of the 3 sutures were joined to form a small right-angled mem-branous gap with the developing lacrimal bone between the 3 sutures (Table 2, Figure 10).

Development of the Supraorbital ForamenOn the 45th–47th days of gestation in Yankasa and on the 48th–50th days of gestation in Uda and Balami, during the ossification of the frontal bone spicules, the left and right supraorbital foramen with a prominent groove appeared on the lateral ends of both halves of the frontal bone just above the medial portion of the orbital margins (Table 3, Figure 11).

Development of the Infraorbital ForamenThe left and right infraorbital foramen (IoF) was seen devel-oping from the center part of the ossifying maxilla on the 45th–47th days of gestation in the 3 breeds of sheep (Table 3, Figure 11).

Discussion, and Conclusion and Recommendations

In this study, sutures appeared as unossified gaps between ossi-fying bones and closed as the bone grew. According to Dyce et al. (2010), the sutures allow the bones to move during the birth process. They act like an expansion joint, allowing the bone to en-large evenly as the brain grows and the skull expands, resulting in a symmetrically shaped head. Despite the importance of these sutures, studies on its development in animals are scanty. The findings of this study suggest that the development and growth of the suture is a slow and gradual process that agrees with the work of Rice (1999). The AF was present, and the PF was absent in this study. This agrees with the findings reported by Lakshmi et al. (2013) who have stated that the PF was not encountered in the skull of the Indian prenatal buffalo. Furthermore, the per-sistence occurrence of the AF in all the fetal age groups in this study (first to second trimester) is also consistent with the work

ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Figure 7A Stereomicrograph (a) and Bone Map (b) of the Lateral View of a 45-Day-Old Yankasa Fetus Showing the Zygomaticomaxillary (ZMS), Maxilloincisive Sutures (MIS), Zygomatic Process of Temporal Bone (ZPt), Zygomatic Bone (ZG), Premaxilla Bone (PM), Maxilla Bone (MA), and Lower Jaw (LJ), Alizarin Red Stain (×10)

a

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Figure 8A Stereomicrograph (a) and Bone Map (b) of a Dorsal View of the Skull in a 54-Day-Old Uda Fetus Showing the Frontonasal Suture (FNS), Nasal Bone (NA), Frontal Bone (FT), and Interfrontal Sutures (IFS), Alizarin Red Stain (×10)

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b

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of Sivachelvan et al. (1995) where they have asserted that in Sa-hel goat the AF disappeared before birth. Similarly, according to Hena and Sonfada (2012), a transient soft spot marking the AF was visible before birth, which appeared prominent during the first trimester of pregnancy and tended to obliterate in the 3rd

trimester before birth. In some breeds of dogs, the fontanelle re-main opens throughout life (Dyce et al., 2010). In humans, the PF is present and closes during the fetal phase; however, the AF was said to persist after birth referred to as the soft spot, which closes after 2 years of birth (Rice, 2008). The closure of the fontanelle fetal phase could indicate complete ossification before birth. In humans, several studies have shown that the AF is located on the anterior/rostral part of the skull (Rice, 2008). In humans, the AF is located on the cranial part of the neurocranium; in the camel, it is

ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Figure 9A Dorsal View of a Stereomicrograph (a) and Bone Map (b) of the Skull of a 65-Day-Old Balami Fetus; Showing an Advanced Stage of Developing Frontonasal Suture (FNS), Nasal Bone (NA), Frontal Bone (FT), and Interfrontal Sutures (IFS), Alizarin Red Stain (×10)

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Figure 10A Stereomicrograph (a) and Bone Map (b) of a Lateral View of the Facial Part of the Skull in a 65th Day Old Balami Fetus Showing; Closed Frontonasal Suture, Opened Right Angle Shaped Fronto-Lacrimal Sutures (FLS), Lacrimomaxillary Sutures (LMS), Opened Nasolacrimal Sutures (NLS), Lacrimozygomatic Sutures (LZS), Lacrimal Bone (LC), Maxilla Bone (MA), and Infraorbital Foramen (IoF), Nasal Bone (NA), Frontal Bone (FT), and Alizarin Red Stain (×10)

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b

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located on the mid and topmost part of the neurocranium (Hena & Sonfada, 2012); whereas in this study, it is located on the cau-dal part of the neurocranium. This difference is because of the lengthy frontal bones which extend caudally to articulate with the parietal bone in the Nigerian breeds of sheep. In this study, the AF appears faster in the Yankasa than in Balami and Uda, sug-gesting that the ossification of surrounding neurocranial bones occurs faster in the Yankasa. The similarity in the origin of the site of the appearance of the ossification centers and sutures in this study further agrees with several study, including the one by Rice (2008) who reported that the sutures were not merely articulations between bones, but were the primary sites of os-teogenesis mediating much of the growth of the neurocranium and viscerocranium. This study showed that the viscerocranial sutures appeared before the neurocranial sutures, which is asso-ciated to the early appearance of the ossification centers of the viscerocranial bones. This contrasts with the results of a study in humans by Persson (1995). The absence of the lambdoid and IPS in the 3 breeds across the first and second trimester age groups was associated with the absence of ossification of the interpari-etal bone.

The supraorbital and infraorbital foramen developed on the frontal and maxilla bones respectively. The former developed earlier than the later in Balami and Uda, but they developed within the same age groups in the Yankasa breed. The age of the development of these foramen corresponds with the time of ossification of the frontal and maxilla bones respectively. This suggests the proximity of the ossification centers and the foramina. This agrees with the report of McGonnell and Akba-reian (2018). Cranial foramina are holes in the skull through which nerves and blood vessels pass to reach both deep and superficial tissues. They are often overlooked in the literature; however, they are complex structures that form within the de-veloping cranial bones during embryogenesis and then remain open throughout life, despite the bone surrounding them un-dergoing constant remodeling. They are invaluable in assign-ing phylogeny in the fossil record and their size has been used, by some, to imply the function of the nerve and/or blood vessel that they contain. Despite this, there are very few studies in-vestigating the development or normal function of the cranial foramina (McGonnell & Akbareian, 2018).

ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Figure 11A Stereomicrograph (a1) and Bone Map (a2) of the Lateral Viscerocranium in a 48-Day-Old Uda Fetus, Stereomicrograph (b1) and Bone Map (b2) of the Lateral Neurocranium of a 54-Day-Old Uda Fetus Showing Supraorbital Foramen (SoF), Infraorbital Foramen (IoF), Cornual Sutures (CS), Parietal Bone (PA), Frontal Bone (FT), Nasal Bone (NA), Premaxilla Bone (PM), Maxilla Bone (MA), Zygomatic Bone (ZG), and Lower Jaw (LJ), Alizarin Red Stain (×10)

a1

a2

b1

b2

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One major limitation of this study was acquiring the Balami fetal samples as this particular breed is rare and scarcely dis-tributed; and therefore, the sample size was small in this study.

The suture formation in the 3 breeds of sheep occurs at a simi-lar time interval; however, sutural development is slower in the neurocranium than in the viscerocranium; and intrasutural clo-sure of the cornual, interfrontal, frontonasal, zygomaticomax-illary, and maxilloincisive sutures occur as early as the second trimester.

Ethics Committee Approval: The study was approved by Institution-al Animal Care and Use Committee of Usmanu Danfodiyo University Sokoto (UDUS/FAREC/2019/AUP-RO-5).

Peer-review: Externally peer-reviewed.

Author Contributions: Concept - S.M.A.; Design –S.M.A; Supervision - A.A.U., S.A.S., A.A.A.; Resources - S.M.A.; Materials - S.M.A.; Data Collec-tion and/or Processing - S.M.A.; Analysis and/or Interpretation - S.M.A.; Literature Search - S.M.A.; Writing Manuscript - S.M.A.; Critical Review - A.A.U., S.A.S., A.A.A.

Conflict of Interest: The authors have no conflicts of interest to de-clare.

Financial Disclosure: The authors declared that this study has received no financial support.

References

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Dyce, K. M., Sack, W. O., & Wensing, C. J. G. (2010). Text book of Veter-inary anatomy. In K. M. Dyce, W. O. Sack, C. J. G. Wensing (Eds.), Veterinary Anatomy Text book (pp.16, 375, 644, 728-742). Saunders Elsevier Inc. 3251 Riverport Lane St. Louis, Missouri 63043.

Hall, L. W., Clarke, K. W., & Trim, C. M. (2000). Wright’s Veterinary Anaesthesia and Analgesia (10th ed., pp. 45-60). London, ELBS and Baillierre Tindall,.

Hena, S. A., & Sonfada, M. L. (2012). Morphological studies on the prena-tal development of calvaria in dromedarian camel. Journal Animal Science Advances, 2(6), 551-557.

Kaufman, M. H., & Bard, J. B. L. (1999). The Anatomical Basis of Mouse Development. In M. Gillian (Ed.), Atlas of Mouse Development Sup-plement (pp. 209-17). Academic press, London. [Crossref]

Lakshmi, M. S., Rao, T. S. C., & Rajalakshmi, K. (2013). Development of fontanelle and paranasal sinuses in the skull of prenatal buffalo (Bubalus bubalis). Korean Journal of Veterinary Research, 53(2), 69-71. [Crossref]

McGonnell, I. M., & Akbareian, S. E. (2018). Like a hole in the head: de-velopment, evolutionary implications and diseases of the cranial foramina. Seminars in Cell and Developmental Biology, 91, 23-30. [Crossref]

Persson, M. (1995). The role of sutures in normal and abnormal craniofacial growth. Acta Odontologica Scandinavica, 53, 152-161. [Crossref]

Rice, D. (1999). Molecular Mechanisms in Calvarial Bone and Suture De-velopment [PhD thesis, Helsinki University]. Helsinki, Helsinki Uni-versity Press.

Rice, D. P. (2008). Developmental anatomy of craniofacial sutures. Fron-tiers Oral Biology, 12(1), 1-21. [Crossref]

Salaramoli, J., Sadeghi, F., Gilanpour, H., Azarnia, M. & Aliesfehani, T. (2015). Modified double skeletal staining protocols with Aliza-rinred and Alcian blue in laboratory animals. Annals of Military and Health Sciences Research, 13(2), 76-81

Sivachelvan, M. N., Hajara, B. U. & Chibuzor, G. A. (1995). Fetal devel-opment of the calvarium in Sahel goat: its post-natal significance. Tropical Veterinarian, 13 (3), 109-118.

Slater, B. J., Lenton, K. A., Kwan, M. D., Gupta, D. K. M., Wan, D. C., & Lon-gaker, M. T. (2008). Cranial sutures: a brief review. Plastic and Re-constructive Surgery, 121(4), 170e-178e. [Crossref]

ATABO et al. Development of Sutures and Foramina of the Skull in Nigerian Breeds of SheepActa Veterinaria Eurasia 2021; 47(2): 98-107

Table 3Time and Sequence and of Development of the Skull Foramina

Age groups (days) Breeds Skull foramina

IoF SoF

One Yankasa - -

(42–44) Uda - -

First trimester Balami - -

Two Yankasa Appeared Appeared

(45–47) Uda Appeared -

First trimester Balami Appeared -

Three Yankasa Appeared Appeared

(48–50) Uda Appeared Appeared

First trimester Balami Appeared Appeared

Four Yankasa Appeared Appeared

(51–53) Uda Appeared Appeared

Second trimester Balami Appeared Appeared

Five Yankasa Appeared Appeared

(54–56) Uda Appeared Appeared

Second trimester Balami Appeared Appeared

Six Yankasa Appeared Appeared

(57–60) Uda Appeared Appeared

Second trimester Balami Appeared Appeared

Seven Yankasa Appeared Appeared

(61–67) Uda Appeared Appeared

Second trimester Balami Appeared Appeared

Note. IoF = Infraorbital foramen; SoF = Supraorbital foramen