Ontogeny of the human fetal, neonatal, and infantile basioccipital bone: traditional and extended eigenshape geometric morphometric analysis

Abstract

The basioccipital bone is an essential developmental component to the occipital bone, occipital condyles, foramen magnum, clivus, and cranial base. The basioccipital bone joins each exoccipital bone with a basiexoccipital synchondrosis and the basisphenoid / sphenoid bone with a sphenooccipital synchondrosis. The basioccipital is found intermediate to the petrous temporal bones and forms the bilateral petrooccipital / petroclival fissures otherwise known as the petrooccipital complex. Thus, the basioccipital bone is a central component to the developing cranial base. Despite the importance of basioccipital development in cranial ontogeny, there has been limited study of basioccipital ontogeny. This study assessed 98 disarticulated human basioccipital bones from a perinatal population ranging in age-at-death from 5-months intrauterine to 5-months post-natal development. Size and shape of basioccipital bones were assessed with traditional and extended eigenshape geometric morphometric analysis. The results of this study demonstrate that the basioccipital bone grows in width at a faster rate than it grows in length. The maximum basioccipital width surpassed the midsagittal length at approximately 7-months intrauterine development. Canonical variate analysis revealed statistically significant shape change occurring from a relatively narrow/elongate (anterior-to-posterior) basiocciput shape with mild concavity at the foramen magnum in the 5th and 6th intrauterine months to a relatively broad/stout basiocciput shape with more pronounced concavity in the postnatal months. Likewise, growth rate in total length was greater than midsagittal length, demonstrating enlargement of concavity in the anterior foramen magnum over time. This report provides insight into cranial development and aids in estimating age-at-death among fetuses and infants.

Introduction:

The human basioccipital bone is a principle developmental component to the occipital bone, occipital condyles, foramen magnum, clivus, and cranial base. The basioccipital bone joins the exoccipital bones with basiexoccipital synchondroses (anterior intraoccipital synchondroses) and the basisphenoid / sphenoid bone with a sphenooccipital synchondrosis. It is located intermediate to the petrous temporal bones and forms the bilateral petrooccipital / petroclival fissures, otherwise known as petrooccipital complexes. Likewise, the basioccipital bone is intermediate to the intracranial cavity and pharynx (Zdilla, 2017; Niel et al., 2019)

The ontogeny of the human basioccipital is of interest among several fields of science. With respect to evolutionary and developmental biology, the foramen magnum is positioned in a more central location in hominins than extant apes— a position that has been attributed to the upright posture, bipedalism, and larger brain size of humans (Dean and Wood, 1981; Nevell and Wood, 2008; Cates et al., 2017). The relatively central location of the human foramen magnum may result, in part, from the shortening of the basioccipital portion of the basicranium (Hoyte, 1975). From the perspectives of forensic and biological anthropology, the basioccipital bone tends to survive burial conditions and is relatively easy to recognize in the remains of an immature skeleton unlike many of the soft tissues and fragile bones of the fetus and infant (Burns, 2015). Since the basioccipital bone is an endochondral bone of relatively strong resilience, it may serve as a novel bone from which to determine age-at-death.

The development of the basioccipital bone is also important with regard to genetics, dysmorphology, and cranial base pathology. Genotypic variants are known to influence the development of the basioccipital bone (e.g., CHARGE syndrome, Cornelia de Lange syndrome) (Russell et al., 2001; Tayebi, 2008; Whitehead et al., 2015; Mahdi and Whitehead, 2018). There may be developmental bony discontinuities in the basioccipital bone such as the clival canal (canalis basilaris medianus) and clival foramen that can interconnect pharyngeal and intracranial structures and thus promote recurrent meningitis in the pediatric population (Martinez et al., 1981; Hemphill et al., 1982; Azizkhan et al., 1989; Ko et al., 2010; Zdilla, 2017). Because the basioccipital is associated with the notochord and perinotochordal sheath, the bone is subject to both non-neoplastic ecchordosis physaliphora and neoplastic chordomas arising from notochordal remnants, among tumors of other varied intrinsic or extrinsic tissues (Rai et al., 2018).

Despite the broad importance of basioccipital ontogeny, there have been limited studies of basioccipital size and shape change. The few studies that have analyzing basioccipital ontogeny have focused mainly on the linear parameters of length and width, without regard for shape (Fazekas and Kósa, 1978; Kósa, 1989), or, conversely, have focused mainly on shape without the analysis of size (Niel et al., 2019).

The resilience of the basioccipital with regard to the resistance of taphonomic degradation suggests that it might be a bone of interest with regard to the study of paleoanthropology, evolution and development, as well as forensic osteology and the identification of human remains. Additionally, the ontogeny of the basioccipital has important pathological and clinical implications. Therefore, this study aims to determine the morphometry and morphology of the basioccipital bone among human fetuses, neonates, and infants of varied age-at-death utilizing morphometric methods that address ontogeny in terms of both size and shape.

Materials and Methods:

This study assessed 98 disarticulated basioccipital bones ranging in age from 5-months intrauterine development to 5-months post-natal development via “traditional” and geometric morphometric methods. Basioccipital bones were accessed from the Johns Hopkins Human Fetal Skull Collection, housed in the Cleveland Museum of Natural History. Basioccipitals originated from individuals who died between the years 1916 and 1951 in Baltimore, Maryland (USA). The remains were gathered by Johns Hopkins University anatomist Adolph H. Schultz. Subsequently, in 1973, the bony remains were transferred to the Cleveland Museum of Natural History.

Archival records included descriptions of age documented in month increments as well as population affinity, which was limited in description to “black” and “white.” Archival records of age were utilized for data analysis. With regard to the demographics of the 98 basioccipitals, 42 were female, 56 were male; 53 were black, 45 were white; 60 were fetal, 38 were infantile (specifically, neonatal to 5-months post-natal age). A detailed breakdown of demographics according to sex, population affinity, and age may be found in Table 1 of the results section.

Table 1:

Average linear parameters of varied basioccipital structures expressed as mean ± standard deviation.

Month	n (n according to sex and population affinity)*	Midsagittal (mm)	Total Length (mm)	Width (mm)	Foramen Magnum (mm)	Spheno-occipital (mm)	Right Exoccipital (mm)	Left Exoccipital (mm)	Right Temporal (mm)	Left Temporal (mm)
05 IU	5 (2 FB; 1MB; 1FW; 1MW)	9.63±0.88	11.33±1.11	9.13±1.48	6.50±0.78	5.33±0.81	5.74±1.10	6.09±1.26	6.12±0.73	5.99±0.81
06 IU	5 (2 FB; 1MB; 3MW)	10.24±0.58	12.23±0.30	9.67±0.92	7.02±0.64	5.14±0.68	6.46±0.28	6.58±0.30	6.25±0.50	6.29±0.49
07 IU	7 (1 FB; 3MB; 1FW; 2MW)	10.56±1.06	13.24±1.25	11.17±1.11	8.37±0.97	6.86±0.72	7.07±0.85	7.20±0.84	6.76±0.54	6.90±0.54
08 IU	17 (8 FB; 3MB; 4FW; 2MW)	10.39±0.88	12.86±0.97	11.42±1.55	8.00±0.92	6.70±0.79	7.05±0.97	7.11±0.95	6.56±0.87	6.48±0.75
09 IU	12 (1 FB; 3MB; 1FW; 7MW)	11.94±1.11	15.39±1.26	13.47±1.01	9.76±1.35	7.93±0.99	8.14±0.63	8.28±0.82	8.00±1.00	8.00±0.65
10 IU	14 (2 FB; 8MB; 1FW; 3MW)	11.95±1.21	15.30±1.81	13.72±1.67	9.61±1.56	7.51±0.72	7.81±0.93	8.02±1.03	8.31±1.40	8.10±1.16
00 PN	14 (3 FB; 6MB; 2FW; 2MW)	12.28±0.90	15.65±1.23	14.19±1.77	9.90±1.23	7.84±0.70	8.41±0.95	8.60±0.87	8.11±1.23	8.02±1.45
01 PN	2 (1FW; 1MW)	13.17±1.16	16.67±0.22	14.94±0.36	11.05±0.51	8.74±0.29	8.84±0.40	9.78±1.00	8.45±0.72	8.00±1.22
02 PN	10 (3 FB; 2MB; 2FW; 3MW)	12.43±0.93	15.96±0.82	14.91±1.18	10.68±0.90	8.17±0.75	8.48±0.71	8.52±0.62	8.50±0.91	8.45±0.95
03 PN	6 (1 FB; 2MB; 1FW; 2MW)	12.76±0.90	16.13±1.28	14.64±0.81	10.65±1.20	8.20±0.61	8.58±0.52	8.70±0.58	8.43±1.10	8.47±1.15
04 PN	4 (1 FB; 2FW; 1MW)	13.55±1.46	17.26±0.79	15.88±0.95	12.46±1.90	8.61±1.63	9.01±1.12	8.92±0.92	9.11±0.33	9.73±0.45
05 PN	2 (2FW)	12.78±0.014	17.54±0.014	16.54±0.006	13.35±0.96	9.98±0.60	9.84±1.75	10.25±1.21	8.33±1.72	8.51±1.48

^*FB represents female and “black”; MB represents male and “black”; FW represents female and “white”; MW represents male and “white”

Ventral surfaces of basioccipital bones were photographed with a digital camera (Canon PowerShot SX50 HS). Digital calipers (Mitutoyo 0–8 in (0–203.2mm) ABSOLUTE™ digimatic caliper series 500, accuracy ± 0.001 in (0.025 mm)) were positioned flush with the bone and photographed alongside each specimen in order to serve as a fiducial for photogrammetry.

Regarding photogrammetry, the basioccipital, unlike other bones, rests flat on a flat surface (i.e., table); therefore, it is easy to consistently position basioccipital bones “hands-free” and photograph them with consistency. The flat nature of the basioccipital provides it with inherent benefits regarding consistent positioning and reproducible photography and measurement that other bones, by their nature, lack.

In the case of this study, photogrammetry was performed with ImageJ software (Abramoff et al., 2004; Schneider et al., 2012). Linear measurements were taken of the maximum sagittal length and maximum transverse width as well as the midsagittal length of the basioccipital bones. Other measurements included those of perimeter segments including the sphenooccipital margin, temporal articular surfaces, exoccipital articular surfaces, and the width of the posterior projections of the basioccipital which mark the boundaries of the anterior aspect of the foramen magnum (Figure 1A).

Figure 1:

Ventral view of a basioccipital from a newborn. A: Articular surfaces are denoted. Also denoted is the location of the lateral projection (star). (SphenOcc: spheno-occipital articular segment; Temp: surface which articulates with the temporal bone; ExOcc: exoccipital articular segment; FMag: posterior segment of the basioccipital bone which forms the anterior margin of the foramen magnum); B: Maxima of the convexities along the contour of the basioccipital bone are located at the boundaries of articular surfaces. (Numbers 1–6 denote the maxima of convexities in the contour of the basioccipital bone that are consistently found among fetal and infant basioccipital bones from at least the fifth month of intrauterine development).

Descriptive statistics of the aforementioned parameters were calculated. Further, regression modeling was performed to determine the best-fit regression models of parameters as a function of developmental age (by month). The statistics were analyzed with GraphPad Prism statistical software, version 6.00 (GraphPad Software, La Jolla, CA, USA).

Geometric morphometric analysis was performed using tpsDig2 and MorphoJ software. An extended eigenshape analysis was performed (MacLeod, 1999). Extended eigenshape analysis blends standard homologous landmarks with sliding landmarks along an outline in a segmental way. Thus, a complex outline is subdivided into segments at well-defined homologous locations along an entire boundary. By subdividing the overall outline of the shape at homologous landmarks, interspecimen correspondence of intrasegmental sliding landmarks is improved. Likewise, individual segments of the contour can be assessed independent of other outline segments (MacLeod, 1999)

The extended eigenshape analysis of this study utilized six homologous landmarks along the basioccipital outline, with 7 equally spaced sliding landmarks between the aforementioned landmarks for a total of 48 points. The six points identified to mark segments of the extended eigenshape analysis included the two anterolateral maxima, forming the boundaries of the spheno-occipital segment of the perimeter, the two lateral projections which separated the temporal articular surface from the exoccipital articular segments, and two posterior-most projections (Figure 1B).

Canonical variate analysis was performed to assess ontogenic shape change between age groupings. Canonical variate analysis can yield inaccurate results in the case of too many landmarks and too few samples (Sheets et al., 2005; Webster and Sheets, 2017). Therefore, age groups with less than five basioccipital samples were excluded from analysis. Mahalanobis distances (unitless and scale-invariant measurement of the distance between a point and a distribution) were determined in the multivariate shape analysis to assess differences among basioccipital shape for each age group and permutation tests (10,000 rounds) were run to determine significance. The utilization of Mahalanobis distances were chosen for this study based on the relationship between the dimensionality of the data and data points in the dataset (Klingenberg and Monteiro, 2005).

Results:

The average linear measurements of the basioccipital bones are summarized in Table 1. The linear measurement averages are represented graphically as a function of age in Figure 2 which demonstrates that the midsagittal length is longer than the width until the 6th month of development (10.24 ± 0.58mm vs 9.67 ± 0.92mm) (Mean ± SD); however, the opposite is true in the 7th month of development— in which case the width becomes longer than the midsagittal length (11.17 ± 1.11mm vs 10.56 ± 1.06mm) and remains so throughout infancy (Figure 2).

Figure 2:

Linear measurements of varied parameters of fetal and infant basioccipital bones ranging in age from 5 months intrauterine (IU) age to 5 months postnatal (PN) age. A: Midsagittal length, total sagittal length, and maximum width as a function of age. Of special note, average total width of the basioccipital becomes larger than midsagittal length from 6 months intrauterine age and 7 months intrauterine age. Also, the basioccipital grows in width at a faster rate than in its length. B: The average lengths of the articular surfaces of the basioccipital bones. The temporal and exoccipital measurements, as well as that of the spheno-occipital measurement after the 7^th developmental month, increase similarly (SphenOcc: spheno-occipital articular segment; Temporal: surface which articulates with the temporal bone; ExOcc: exoccipital articular segment; FMag: posterior segment of the basioccipital bone which forms the anterior margin of the foramen magnum).

A comparison of regression models revealed that linear regression provided the best-fit. All regression slopes analyzed by F-tests were determined to have slopes significantly different than zero (p<0.0001) (Table 2). The parameter with the lowest r² value was that of the right temporal distance, followed by left temporal distance (r²= 0.3551 and 0.4026, respectively) (Table 2). The parameter with the best-fit regression was that of width and was given by: Age = (Width − 6.651)/0.6486; r²= 0.60 (Table 2, Figure 3).

Table 2:

Details of best-fit linear equations representing age as a function of varied linear measurements.

	Slope±Standard Error	95% CI	Best-fit Equation*	r2	F	p
Midsagittal	0.3538± 0.03855	0.2771 to 0.4304	$Age=\frac{Midsagittallength-8.117}{0.3538}$	0.4673	84.21	<0.0001
Total Length	0.5455± 0.04937	0.4474 to 0.6437	$Age=\frac{Totallength-9.293}{0.5455}$	0.5598	122.1	<0.0001
Width	0.6486± 0.05383	0.5416 to 0.7556	$Age=\frac{Width-6.651}{0.6486}$	0.602	145.2	<0.0001
Foramen Magnum	0.5165± 0.04527	0.4265 to 0.6065	$Age=\frac{Foramenmagnumdistance-4.283}{0.5165}$	0.5755	130.2	<0.0001
Spheno-occipital	0.3224± 0.03323	0.2564 to 0.3885	$Age=\frac{Spheno-occipitaldistance-4.221}{0.3224}$	0.4951	94.14	<0.0001
Right Exoccipital	0.2963± 0.03293	0.2308 to 0.3618	$Age=\frac{Rightexoccipitaldistance-4.865}{0.2963}$	0.4574	80.94	<0.0001
Left exoccipital	0.2929± 0.03424	0.2248 to 0.3609	$Age=\frac{Leftexoccipitaldistance-5.049}{0.2929}$	0.4325	73.18	<0.0001
Right Temporal	0.2875± 0.03954	0.2089 to 0.3661	$Age=\frac{Righttemporaldistance-4.822}{0.2875}$	0.3551	52.87	<0.0001
Left Temporal	0.3058± 0.03801	0.2302 to 0.3813	$Age=\frac{Lefttemporaldistance-4.608}{0.3058}$	0.4026	64.7	<0.0001

^*Age expressed as months of development.

BOLD: represents the p–value from the F test that denotes that the slope that is significantly different than zero

Figure 3:

Best-fit linear regression of width as a function of developmental age. The linear regression equation is represented as: Age = (Width − 6.651)/0.6486; r²= 0.60. The 95% confidence interval is shaded.

With regard to geometric morphometric analysis, canonical variate analysis revealed shape change occurring from a relatively narrow/elongate (anterior-to-posterior) basiocciput shape with mild concavity at the foramen magnum in the 5th intrauterine month to a relatively broad/stout basiocciput shape with more pronounced concavity in the postnatal months (Figure 4). Also, lateral projections were less evident in intrauterine basioccipitals relative to postnatal basioccipitals (Figure 4). All age groups separated entirely in the morphospace (when bounded by a convex hull) and only the 7^th and 8^th month intrauterine age groups had any overlap of 95% confidence ellipses (Figure 4). Furthermore, Mahalanobis distances were significantly different between all age groups (Table 3).

Figure 4:

Canonical variate analysis (CV1 vs CV2) among age groups (organized according to months) represented by colors. Ellipses, representing 95% confidence, correspond to each age group. Shape change is shown along each axis via basiocciput outlines. CV1 accounts for 41.5% of variance, while CV2 accounts for 23.9%.

Table 3:

Mahalanobis distances among basioccipital shape groupings according to age

AGE		Intrauterine Age (months)						Postnatal Age (months)
		5	6	7	8	9	10	0	1	2	3	4
Intrauterine Age (months)	6	15.7
		****
	7	13.4	16.5
		***	****
	8	13.8	13.7	9.7
		****	****	****
	9	19.0	21.9	12.0	13.0
		***	****	****	****
	10	18.5	16.1	12.6	7.9	15.3
		****	****	****	****	****
Postnatal Age (months)	0	19.6	14.5	15.7	9.9	18.7	7.1
		****	****	****	****	****	****
	1
	2	22.0	21.0	16.0	15.5	17.9	12.0	13.4
		****	***	****	****	****	****	****
	3	25.3	21.0	24.4	20.7	26.8	19.8	16.1		18.9
		***	***	****	****	****	****	****		***
	4
	5

^***p<0.0005

^****p<0.0001

p-vales are from permutation tests (10,000 rounds) for Mahalanobis distances among groups.

Note: Postnatal age groups of 1, 4, and 5 months were excluded from analysis due to limited sample size

Discussion:

In addition to adding valuable context for the development of the human cranial base, this research has important implications for evolutionary and developmental biology as well as biological and forensic anthropology, especially since the endochondral-derived basiocciput is relatively durable and resistant to taphonomic degradation when compared to the fragile intramembranous bones of the fetal and infant cranium (Burns, 2015; Manifold, 2015). The results of this research also reveal that the basioccipital size and shape are useful in the estimation of age-at-death from fetal, neonatal, and infantile remains.

Concurrence with Other Studies

Prior assessments of midsagittal length and maximum width of fetal basioccipital bones by Fazekas and Kósa (1978) and Kósa (1989) revealed that, when the maximum width exceeds the midsagittal length, the fetus is likely to be at least eight months old. Similarly, in an assessment of ten fetal Egyptian crania from the Roman Period, Tocheri and Molto (2002), noted that if the maximum width exceeds the midsagittal length the fetus is likely to be older than eight months. Further, Scheuer and MacLaughlin-Black (1994) suggested that the individual is more than seven months in utero when the maximum width exceeds the midsagittal length. This study, performed on basioccipitals of modern black and white Americans, demonstrates that the maximum width exceeds the midsagittal length at seven months of development and remains so until at least five-months post-natal age (the upper age limit of this study). The agreement among prior studies assessing common linear parameters concur suggests that, regardless of population affinity, sex, geography, or temporal factors, the ratio of the common linear parameters of midsagittal length and maximum width is capable of determining if a fetus is less-than or greater-than seven months in age.

This study included basioccipital bones from individuals of a maximum of five-months post-natal age. In this case, the maximum width of the basioccipital never exceeded the maximum length, regardless of age. However, it is important to note that prior studies, including that of a Yugoslavian skeletal series (A.D. 1400–1475) and that of an Egyptian series (A.D. 200–400), which included basioccipitals from older infants, suggest that the maximum width exceeds the maximum length at six months of post-natal age and older (Redfield, 1970; Tocheri and Molto, 2002). Therefore, the maximum-length-to-maximum-width ratio should be considered a valuable forensic metric in addition to the aforementioned midsagittal-length-to-maximum-width ratio identified in this study.

A study performed by Irurita Olivares and Alemán Aguilera (2016), which included a sample from individuals aged five-months gestation to six years postnatal, identified useful logarithmic regression equations for linear measurements including that of the maximum length of the basioccipital; however, it must be kept in mind that, of the 114 basioccipital sample of Irurita Olivares and Alemán Aguilera (2016), only 9 basioccipitals were of fetal age— more than five-times less than the number included in this study. In the case of this study, linear regression models provided a better goodness-of-fit than those of logarithmic regressions for the fetal, perinatal, and infantile demographic. The discrepancy is likely explained by the relatively rapid growth rate of the basioccipital in the fetal age and slower growth rate in early childhood.

The Usefulness of Extended Eigenshape Analysis

This study is unique in that it is the first to assess the ontogeny of the basioccipital bone with an extended eigenshape analysis. Because human fetal and infantile basioccipital bones have homologous structures (i.e., the two posterior-most projections, the two antero-lateral maxima, forming the boundaries of the spheno-occipital segment of the perimeter, and the two lateral projections which separated the temporal articular surface from the exoccipital articular segments) extended eigenshape analysis can be performed among both age groups with little difficulty. Moreover, basioccipital bones of varied species share their basic configuration with that of humans, including common research species like those of mice (Cates et al., 2017) and rats (Vilmann, 1972). Thus, interspecies homologous landmarks may allow for interspecies analysis and comparative anatomical assessment. Accordingly, the techniques utilized in this study may be applied to research comparing basioccipital ontogenic differences among control and test laboratory animals (e.g., mouse models).

Recently, the shape of the basioccipital was assessed via elliptical Fourier analysis, a method of using harmonics for contour analysis (Niel et al., 2019). The utilization of harmonics to assess global shape has several drawbacks when compared to the segmental analysis of bony shape. These drawbacks include the relative mathematical complexities of elliptical Fourier analysis as well as the practical application of the method. Conversely, extended eigenshape analysis is relatively simple and conceptually less obscure than elliptical Fourier analysis. It is also well-suited for practical applications. For example, if only partial remnants of a basioccipital were available for analysis, the data from a segment of eigenshape analysis could be utilized to identify the age of remains. For instance, if only the anterior-most portion of the basioccipital were found (i.e., the spheno-occipital aspect), the antero-lateral maxima could still be utilized to determine age. Similarly, the segmental analysis of the basioccipital has benefit over Fourier analysis in the case of discontinuity in the boundary of the basioccipital that might occur in, for example, the case of a transverse basilar fissure.

Likewise, the nine regression equations regarding “traditional” linear parameters presented in this report can be utilized in concert; however, they can also be utilized piece-meal in the event that the basioccipital is not intact. For example, if only the left-sided exoccipital aspect of the basioccipital were available, an investigator could utilize a regression equation to approximate age; furthermore, an investigator could pair this analysis with the utilization of the left exoccipital segment of the extended eigenshape analysis.

Additional methods have been utilized in the assessment of the basioccipital among other species. For example, Cates et al. (2017) performed shape analysis of the basioccipital bone in Pax7-deficient mice by way of particle-based modeling. The particle-based modeling methodology provides a three-dimensional representation of the bone. Further, in addition to the analysis of an added dimension, particle-based modeling may aid in the identification of subtle shape variation (Cates et al., 2017).

A three-dimensional analysis of the basioccipital may identify variations on the dorsal and ventral surfaces of the basioccipital bone. Three-dimensional analysis can identify useful information with regard to basioccipital development; however, such an analysis may be tainted by common anatomical variation or varied pathologies. For example, the ventral aspect of the basioccipital frequently presents the fossa navicularis which varies in its shape (Ersan, 2017; Sheikh et al., 2017; Magat, 2019). Likewise, the fossa navicularis may be pronounced and otherwise known as a fossa navicularis magna (Beltramello et al., 1998; Murjani et al., 2021). Likewise, precondylar tubercles (Vasudeva and Choudhry, 1996; Jaffar, 2014), variation of the pharyngeal tubercle, or a third occipital condyle (Tubbs et al., 2013) can influence shape analysis. The dorsum of the basioccipital also has structures which may affect three-dimensional analysis including the clival canal, clival foramen, and myriad patterns of foveae and foveolae (Zdilla, 2017). Additionally, any sort of pathological process or entity that affects the ventral of dorsal basioccipital surface (e.g., chordoma) may also influence three-dimensional analysis.¹

Forensic Significance

From both a biological and forensic anthropological perspective, age-at-death estimation is of the utmost importance. From a bioarcheological standpoint, children have been referred to as “canaries in the coal mine” for population stress because their developing immune function and nutritional requirements for adequate growth are more susceptible to stressors (Lewis, 2007; Halcrow and Ward, 2018). Certainly, the same notion can be applied to fetuses and infants. Moreover, fetal and infantile growth and development may be reflective of maternal health and stressors that might affect the pregnant or post-partum woman. With regard to forensics, age-at-death estimation is warranted for criminal abortion, neonaticide, and infanticide. Further, from age-at-death estimation, one may be able to retrospectively ascertain when conception had taken place which might aid in identification of the parents of the deceased individual.

Among adults, there are myriad accurate methods for determining age-at-death. However, among fetuses and infants, there is a paucity of information detailing age-at-death from remains. The estimation of age from skeletal remains of fetuses, neonates, and infants is uniquely complicated, oftentimes, more so than adult remains. For example, long bones of fetuses and infants, which typically provide accurate assessment of age, (Scheuer, 2002; Chávez-Martínez et al., 2016) are easily degraded by taphonomic processes (Irurita Olivares and Alemán Aguilera, 2016). Dental age estimates have long been used as one of the major age assessment techniques in criminology and anthropology. The Demirjian system is often considered the gold standard in dental age assessment and was first described by Demirjian et al. in 1973. The system utilizes calcification stages of the permanent seven teeth on the left side of the mandible. Other dental age estimate techniques have been created utilizing gingival emergence, eruption sequence, and radiographs. Dental age estimates, however, are limited in assessing the age of neonatal and infant populations due to variations in tooth development. Soft tissues are valuable in the estimation of fetal/infantile age (Kumar and Pillay, 1996; Chikkannaiah et al., 2012; Udaykumar et al., 2016); however, soft tissues are especially susceptible to degeneration.

The basioccipital is an endochondral bone of strong resilience, capable of resisting taphonomic degradation. And, based upon the results of this study, the basioccipital linear dimensions as well as its general shape correspond to age. Therefore, the basioccipital bone should be included in the assessment of fetal and infantile post-mortem age-at-death estimation.

Evolutionary and Developmental Perspective: Expansion in the Concavity of the Posterior Basioccipital Facilitates Centralization of the Human Foramen Magnum

During fetal growth, humans and non-human primates differ with regard to the relative proportioning of the posterior crania fossa. Among humans, anterior-posterior growth of the basioccipital is proportionately less than that of the other components of the posterior cranial fossa. The opposite scenario occurs in nonhuman primates (Lieberman et al., 2000). In humans, the nuchal plane rotates downward to orient relatively horizontally in comparison to nonhuman primates where the plane becomes more vertical (Duterloo and Enlow, 1970; Lieberman et al., 2000). As a result, the foramen magnum becomes situated in the center of the human neonatal basicranium and, in comparison, relatively posterior in nonhuman primates (Lieberman et al., 2000).

The resorptive and depository growth responsible for the movement of the nuchal plane and, accordingly, the foramen magnum location, has been localized to the exoccipital and squamous occipital posterior to the foramen magnum (Lieberman et al., 2000). However, the results of this study advance that the ontogeny of the fetal and infantile basioccipital also contributes to the centralization of the foramen magnum. Specifically, the posterior aspect of the basioccipital, representative of the anterior margin of the foramen magnum, becomes more concave and broad over the course of fetal and infantile development. Indeed, with regard to the six border segments assessed in this study, the foramen magnum segment expanded at the greatest rate with regard to age (Table 2, Figure 2). The foramen magnum parameter, along with basioccipital width were the two best-related linear parameters related to developmental age (Table 2). Thus, the expansion of the posterior basioccipital concavity in both anterior-to-posterior dimension and breadth centralizes the foramen magnum in concert with nuchal plane rotation and basicranial flexion.

The growth in the concavity of the posterior basioccipital is demonstrated in both size and shape. Regarding size, this study identifies a greater rate of change in the total basioccipital length compared to the midsagittal length spanning from the spheno-occipital synchondrosis to the basion (Table 2, Figure 2). The relationship between the linear parameters coordinates with the analysis of shape change over time (Table 3, Figure 4). Sensibly, the elongation of the total basioccipital length must be paired with a relatively slower elongation in the midline to facilitate the centralization of the foramen magnum while at the same time accommodating for growth, in general.

From an evolutionary perspective, a prevailing notion is that basicranial flexion allows for a larger brain size relative to cranial base length among humans (Lieberman et al., 2000; Rengasamy Venugopalan and Van Otterloo 2021). A widely accepted hypothesis is that midline cranial base angle correlates with brain volume relative to basicranial length. Thus, the basioccipital is of importance with regard to both the cranial base angle and the basicranial length and may be reflective of changes in local soft tissue structures including the brain.

In this study, cranial base angles could not be assessed in conjunction with the ontogeny of the basioccipital. However, regardless of specific cranial base angles, it is well-known that the human cranial base angle is obtuse, in general. Accordingly, concavity in the posterior basioccipital facilitates the centralization of the foramen magnum and thus, accommodates the medulla oblongata and spinal cord as well as the relatively pronounced flexion of the human central nervous system. Further, the concavity accommodates the passage of vascular structures located anterior to nervous system structures (e.g., vertebral arteries). In addition to intracranial structures, the results of this study also have implications with regard to the development of exocranial structures including nasopharynx, larynx, and face (Laitman et al., 1978; Laitman and Heimbuch, 1982; Pagano and Laitman, 2015).

Additional Developmental Considerations

A morphological classification of basioccipital bones utilizing the foveae and foveolae found at the dorsal surface of the basioccipital has been developed (Zdilla, 2017). The aforementioned morphological classifications revealed a model of basioccipital development: During the fifth through seventh months of intrauterine development, the basioccipital tends to have a pronounced dorsal impression that usually has a bony strut located at, or in very close proximity to the midline, thus forming a bifid impression which may be devoid of foveae or foveolae but usually contains shallow foveae or foveolae. From the eighth month of intrauterine development to at least the fifth postnatal month, the basioccipital tends to exhibit two paramedian foveae or foveolae intermediate to the lateral projections. From the age of 1 year, the basioccipital resembles that of the homologous aspect of the clivus in the adult occipital bone (Zdilla, 2017). Therefore, in addition to the size and shape data regarding the en face boundary of the basioccipital of this report, the dorsum of the basioccipital may provide additional information regarding age.

The basioccipital may also have features including the clival canal or clival foramen which represent vascular channels (Zdilla, 2017). They can be found in fetuses, neonates, and infants as well as adults (Zdilla, 2017). However, clival canals and foramina are inconsistent and their presence or absence is unlikely to provide valuable information with regard to age.

The basioccipital bone is the precursor to the anterior aspect of the adult occipital bone— ultimately forming the anterior margin of the foramen magnum and anterior portions of the occipital condyles. A recent morphometric analysis of the foramen magnum among adult crania of populations of varied population affinity and sex identified that the foramen magnum is larger in males than females, regardless of population affinity; though, foraminal shapes do not differ between sexes (Zdilla et al., 2017). Further, the study revealed that foramen magnum shapes differ between crania of varied population affinity (Zdilla et al., 2017). Additionally, the occipital condyles have been demonstrated to be sexually dimorphic (Gapert et al., 2009). Because the anterior margin of the foramen magnum and anterior aspects of the occipital condyles are ultimately derived from the posterior boundary of the basioccipital bone, and because the aforementioned structures differ among varied populations of adult crania, further assessment of basioccipital shape in perinatal populations of varied demographics must be performed to determine if basioccipital shape variance among different population affinities and sexes occurs at an early stage in development.

If the development of the anterior foramen magnum were to be investigated, the utilization of extended eigenshape analysis would be particularly useful since, by the nature of the landmark methodologies, a particular segmental component of shape can be independently assessed from composite landmark data while excluding segmental components of little interest (e.g., the contour of the sphenooccipital synchondrosis). Thus, structures like basion tubercles along the foramen magnum margin would be emphasized rather than being de-emphasized by extraneous landmarks. The same segmental analysis cannot be done with other methods such as the aforementioned harmonics-based Fourier analysis or particle-based modeling methods. Accordingly, the notion of independent segmental contour analysis that applies to the foramen magnum shape component also applies to the exoccipital contour components, temporal contour components, or sphenooccipital contour component of the basioccipital bone.

Limitations

This study incorporated all available samples from a unique museum collection of fetal and infantile specimens. Due to the limited collection size, sample sizes for varied developmental ages were not homogeneous. Samples in some age groups only consisted of two specimens (e.g., one-month and five-month post-natal groups) whereas other groups had larger samples (e.g., eight-months intrauterine; n=17). The unbalanced nature of the sample was an unavoidable limitation to the study. However, it is important to note that standard deviations (or difference between maximum and minimums, in the case of two-sample groups) in linear parameters among small groups was akin to that of larger groups, if not smaller (Table 1). Nevertheless, in addition to imbalances in age, there were also imbalances in sex and population affinity among several age groups (Table 1). Thus, limitations in sample size and demographics prevented the reasonable comparison of ontogeny among sub-populations.

Conclusion:

With regard to the utilization of the information found in this report. The authors underscore the following key points: 1) the basioccipital can be used to estimate the age-at-death of human fetuses, neonates, and infants; 2) maximum basioccipital width surpasses the midsagittal length at approximately 7 months intrauterine development; 3) the basioccipital size parameters most closely related to developmental age are maximum width and foramen magnum distance and can be approximated with the equations given age = (width − 6.651)/0.6486 and age = (foramen magnum distance − 4.283)/0.5165, respectively; 4) the shape of the basioccipital bone changes over time from relatively elongated and narrow to relatively stout and broad; 5) Total basioccipital length increases at a faster rate than that of midsagittal length, demonstrating an enlargement of posterior basioccipital (anterior foramen magnum) concavity over time; and 6) in conjunction with traditional morphometric methods, extended eigenshape analysis is a simple geometric morphometric method that is well-suited for the analysis of the basioccipital bone.