Journal Information
Vol. 94. Num. 6.November - December 2018
Pages 571-692
Share
Share
Download PDF
More article options
Visits
668
Vol. 94. Num. 6.November - December 2018
Pages 571-692
Original article
DOI: 10.1016/j.jped.2017.08.009
Open Access
Tongue development in stillborns autopsied at different gestational ages
Desenvolvimento da língua em natimortos autopsiados em diferentes idades gestacionais
Visits
668
Laura S. Aguiara, Guilherme R. Julianoa, Luciano A.M. Silveirab,
Corresponding author
drluciano@hotmail.com

Corresponding author.
, Mariana S. Oliveiraa, Bianca G.S. Torquatoa, Gabriela R. Julianoa, Márcia F. Araújoa, Sanivia Aparecida L. Pereiraa, Vicente de Paula A. Teixeirac, Mara Lúcia F. Ferraza
a Universidade Federal do Triângulo Mineiro (UFTM), Uberaba, MG, Brazil
b Universidade Federal do Triângulo Mineiro (UFTM), Departamento de Cirurgia, Programa de Pós-Graduação em Ciências da Saúde, Uberaba, MG, Brazil
c Universidade Federal do Triângulo Mineiro (UFTM), Instituto de Ciências Biológicas e Naturais, Uberaba, MG, Brazil
This item has received
668
Visits

Under a Creative Commons license
Article information
Abstract
Full Text
Bibliography
Download PDF
Statistics
Figures (3)
Show moreShow less
Tables (1)
Table 1. Constitutional and morphometric data of the 55 stillborns autopsied by the discipline of General Pathology at the Clinical Hospital of the Federal University of Triângulo Mineiro (HC/UFTM), Uberaba, State of Minas Gerais, Brazil, from 1994 to 2015.
Abstract
Objectives

This study aimed to analyze, through the morphometric method, the perimeter and length of the tongue, the collagen fibers, and the perimeter of blood vessels at different gestational ages and fetal weights.

Material and methods

Tongues (n=55) of stillborns autopsied at 23–40 weeks of gestational age were macroscopically analyzed, and their length and perimeter were measured. Fifty-five tongue fragments were collected through a longitudinal section in the region that accompanies the median lingual sulcus and histologically processed. Slides were stained with picrosirius and immunolabeled with CD31 antibody. Quantification was performed on collagen fibers under polarized light, and on the perimeter of vessels with the CD31.

Results

A positive and significant correlation of gestational age with tongue perimeter and length was found. There was a positive and significant correlation between collagen fibers and gestational age, as well as between gestational age and the perimeter of blood vessels. Between collagen fibers and fetal weight, a positive and significant increase was observed. Regarding the correlation between the perimeter of blood vessels and the fetal weight, an increase was observed.

Conclusion

As gestational age advances, there is an increase in tongue perimeter and length, in the percentage of collagen fibers, and in vascular perimeter, demonstrating that tongue formation is directly related to tongue growth and development.

Keywords:
Gestational age
Stillborn
Autopsy
Resumo
Objetivos

Analisar, por meio do método morfométrico, o perímetro e o comprimento da língua, as fibras de colágeno, o perímetro dos vasos sanguíneos, em idades gestacionais e de acordo com o peso fetal.

Materiais e métodos

Línguas (n=55) de natimortos autopsiados com 23-40 semanas de idade gestacional foram analisadas macroscopicamente, medidas em comprimento e perímetro; 55 fragmentos das línguas foram coletados por meio de uma secção longitudinal na região que acompanha o sulco lingual médio e processados histologicamente. As lâminas foram coloridas com picrosirius e imunomarcadas com o anticorpo CD31. A quantificação foi feita em fibras de colágeno examinadas com microscópio de luz polarizada e o perímetro dos vasos com o CD31.

Resultados

Foi encontrada uma correlação positiva e significativa da idade gestacional com o perímetro e o comprimento da língua. Houve uma correlação positiva e significativa entre as fibras de colágeno e a idade gestacional; bem como entre a idade gestacional e o perímetro dos vasos sanguíneos; e houve um aumento positivo e significativo entre as fibras de colágeno e o peso fetal. No que diz respeito à correlação entre o perímetro dos vasos sanguíneos e o peso fetal, houve um aumento.

Conclusão

Conforme a idade gestacional avança, há um aumento no perímetro e no comprimento da língua, um aumento no percentual de fibras de colágeno e um aumento no perímetro vascular, demonstra que a formação da língua está diretamente relacionada ao crescimento e ao desenvolvimento da língua.

Palavras-chave:
Idade gestacional
Natimortos
Autópsia
Full Text
Introduction

Pediatric autopsy is an important study of the structural and functional differences of the organs according to the time of fetal development. In the autopsy, the estimation of the gestational age (GA) is important to identify whether fetal development was occurring normally, to determine the death time in relation to the birth, to ascertain the diagnosis of the diseases that are specific to that developmental stage, and to detect those children classified as risk in the neonatal period.1

During examination, the evaluation of the tongue provides a variety of information, as it is a special organ of reception, chewing, swallowing, speaking, and tasting. Evidences from mammalian studies suggests that it is composed of muscle cells that have different arrangements in origin and insertion, and different histochemical properties in comparison with other skeletal muscles.2,3

The development of the tongue is described as a relatively rapid process, which begins between the fourth and fifth week of intrauterine life. This process has a remarkable effect on the oral cavity4; therefore, it is extremely important for the development of the stomatognathic system that the tongue develops correctly.5 There appears to be a synchrony in the formation of the orofacial complex since, from the 14th week onwards, the muscles of the oropharyngeal region are sufficiently advanced to move the tongue, coinciding with peaks in the growth of the head circumference that occur between the 15th and 17th week.6,7

Collagen is expressed in the tongue in the early stages of development, and is detectable in the mesenchyme derived from cranial neural crest cells (CNCC), adjacent to the tongue epithelium8 and in tendons of the extrinsic muscles, which connect the tongue to the mandible.9 The connective tissue and the vascular system of the tongue are derived from the CNCC, while most of its muscles originate from myoblasts that migrated from the occipital somites.10

Endothelial cells play a key role in the control of coagulation, thrombosis, vascular tone, permeability, inflammation, tissue repair, and angiogenesis.11 They constitute a heterogeneous population of cells in the human body. Functions and molecular characteristics of endothelial cells vary along the vascular tree and in the same organ between different vessels, as for example, phenotypic variations can occur in the expression of the CD31 molecule in these cells.12–14

Ultrasound examinations have indicated a highly significant correlation between fetal tongue circumference and gestational age (14 to 26 weeks).15 This data may be useful in the prenatal diagnosis of suspected congenital syndromes that include, among its manifestations, tongue growth disorders and GA estimation.12

The autopsy material is very rich for research, since through macro- and microscopic analyses it is possible to make feasible research studies with clinical diagnoses and detection of structural abnormalities. The autopsy is considered an important diagnostic method for the physician, since it allows documenting and comparing clinical and pathological cases.1 In pediatric autopsies, the hallux-calcaneus length (HCL) is a reliable parameter to establish GA in fetuses and stillbirths. The GA obtained by HCL is taken by measuring the length of the foot, from the heel to the tip of the hallux.16

The aim of this study was to analyze, through the morphometric method, the perimeter and length of the tongue, the collagen fibers, the perimeter of the blood vessels, at different GAs and in relation to the fetal weight. It can contribute as a new method to estimate GA through the tongue development.

Material and methods

This was a retrospective study, approved by the Ethics Committee of the Federal University of Triângulo Mineiro, under protocol No. 1158.

Of the 152 pediatric autopsy reports analyzed, those of 55 stillborns autopsied by the General Pathology Discipline at the Clinical Hospital of the Federal University of Triângulo Mineiro (HC/UFTM), Uberaba, State of Minas Gerais, from 1994 to 2015 were selected. The anatomopathological examination was performed by two pathologists, and the information obtained from the autopsy reports was GA, determined using the HCL method (hallux-calcaneus length), and fetal weight.

Inclusion criteria were GA between 23 and 40 weeks, those with data of gender and fetal weight, and those in which the tongue was in good preservation condition. The exclusion criteria were stillborn infants with malformations and lack of data in reports such as GA, fetal weight and gender. Moreover, any cases with intrauterine growth restriction or another alteration were excluded.

Measurement of tongue length and perimeter

The 55 tongues analyzed were arranged on the macroscopy laboratory bench and identified individually, with the respective autopsy number, along with a ruler for later calibration in the ImageJ® Software (National Institutes of Health, USA). All photographs were taken from the same distance (30cm) using a Canon Rebel® camera (Canon, Tokyo, Japan). Morphometric analyses were performed measuring the length from the glossoepiglottic fold to the apex of the tongue; to obtain the perimeter of the tongue, the contour was measured throughout the macroscopic extension.

Sample collection and histopathological processing

Fifty-five tongue fragments from autopsied stillborns recovered in the archive of biological material of the discipline of General Pathology (UFTM) were used. Fragments were removed through a longitudinal section in the region that accompanies the median lingual sulcus, with a thickness of approximately 0.5cm. Serial cuts of 4μm in thickness were then performed. Slides were stained with Picrosirius (PS; saturated aqueous solution of picric acid added with 0.1g% Sirius red F3B) (Bayer, Leverkusen, Germany) with counterstaining by hematoxylin, and a slide was used for immunohistochemistry.

Morphometric analysis of collagen fibers

The PS-stained slide was analyzed for quantification of collagen fibers. The number of fields for evaluation and quantification of collagen fibers of the longitudinal section of the tongue, at different GAs, was defined as four quadrants and ten fields per quadrant of the histological section were analyzed. The area of collagen fibers under polarized light presented a birefringent appearance, ranging from orange to red (Fig. 1). Collagen fibers were marked by the observer to obtain the percentage of collagen per field analyzed. Thus, the field image was digitized using a camera coupled to a microscope with a Leica Qwin Plus® image analyzer (Leica Microsystems Inc, IL, USA). Morphometry was performed with Leica Qwin Plus® software image analyzer system (Leica Microsystems Inc, IL, USA), with a 10× objective lens (final magnification of 320×).

Figure 1.
(1.2MB).

Micrographs of stillborn tongue fragments examined under polarized light, showing the birefringent collagen fibers (arrows) (Picrosirius – 10×–320× final magnification) at different gestational ages (GA).

(A) GA: 23 weeks; (B) GA: 28 weeks; (C) GA: 34 weeks; (D) GA: 37 weeks; (E) GA: 39 weeks, and (F) GA: 40 weeks.

Immunohistochemical analysis

Immunohistochemistry was performed to identify anti-CD31 positivity. The number of fields for evaluation and quantification of the CD31 marker in the longitudinal section of the tongue, at different GAs, was defined as four quadrants and tend fields per quadrant of the histological section were analyzed. Measurements were taken using a video camera coupled to a light microscope, and these to a computer with the image analyzer system Axiovision SE64 Rel. 4.9.1® software. The perimeter of blood vessels was measured using ImageJ® Software (National Institutes of Health, USA), with an objective lens 100× (final magnification 3250×; Fig. 2).

Figure 2.
(0.6MB).

Micrographs of stillborn tongue fragments examined under light microscopy, showing the increase in anti-CD31 immunolabeled blood vessels (arrows) (objective 100×–3250× final magnification) at different gestational ages (GA).

(A) GA: 23 weeks; (B) GA: 28 weeks; (C) GA: 34 weeks; (D) GA: 37 weeks; (E) GA: 39 weeks, and (F) GA: 40 weeks.

Statistical analysis

For the statistical analysis, a spreadsheet of the program Microsoft Excel® was elaborated. The information was analyzed using the electronic program GraphPad Prism® version 5.0 (GraphPad Software, Inc, CA, USA). To verify the type of distribution of the variables the statistical test of Shapiro–Wilk was applied. For correlation, the Spearman correlation coefficient (rS) was used for non-normal distribution. The differences were considered statistically significant when p was less than 5% (p<0.05).

Results

Of the 152 reports of pediatric autopsies analyzed, 55 were selected for evaluation, with a median GA of 33 weeks, ranging from 23 to 40 weeks. Regarding gender, 34 (60.71%) were male and 22 (39.28%) were female. The analyzed data were presented in Table 1.

Table 1.

Constitutional and morphometric data of the 55 stillborns autopsied by the discipline of General Pathology at the Clinical Hospital of the Federal University of Triângulo Mineiro (HC/UFTM), Uberaba, State of Minas Gerais, Brazil, from 1994 to 2015.

Cases  Tongue length (cm)  Tongue perimeter (cm)  Collagen (%)
X±SD 
Vessels perimeter (μm)
X±SD 
Gestational age (weeks)  Fetal weight (kg) 
N4210  3.314  8.227  2.084±0.305  16.86±1.343  23  0.54 
N4156  3.287  9.065  13.231±1.036  23.37±2.147  23  0.7 
N4301  3.295  8.161  2.881±0.526  70.09±7.397  23  0.545 
N4051  3.901  10.182  2.572±0.564  121.3±15.25  24  1.3 
N4162  3.542  8.861  4.987±0.658  80.48±10.23  24  0.64 
N4238  3.891  10.172  20.588±1.511  19.20±1.555  24  1.08 
N4279  3.622  9.572  2.319±0.563  70.74±6.36  24  0.620 
N4149  4.135  11.021  1.493±0.315  71.18±15.62  25  0.57 
N4313  4.378  11.46  2.527±0.372  80.27±9.780  26  1.04 
N4265  2.951  7.354  7.383±0.634  86.48±12.30  26  0.985 
N4269  3.994  10.333  11.299±0.812  84.02±12.44  26  0.8 
N4090  3.344  9.422  2.833±0.266  24.64±2.078  27  0.85 
N4199  3.237  8.339  3.737±0.569  66.40±4.911  27  0.9 
N4159  4. 327  11.856  6.139±0.791  15.62±1.075  27  2.25 
N3935  4.423  11.43  8.013±1.430  18.38±2.382  28  1.09 
N4086  3.746  10.379  12.202±0.747  25.90±7.057  28  1.25 
N4134  3.755  9.872  1.745±0.218  89.27±8.840  28  1.02 
N4108  3.751  10.033  2.419±0.638  54.88±4.987  28  1.2 
N4174  3.482  9.813  1.327±0.199  70.18±7.454  28  1.08 
N4275  3.324  8.864  4.142±0.401  105.1±7.451  28 
N4239  4.423  11.213  1.837±0.305  21.89±1.765  29  1.24 
N3976  4.902  11.618  6.757±1.049  20.22±1.582  29  2.77 
N4125  4.493  11.031  9.542±0.941  96.22±8.743  30  1.7 
N4295  3.785  9.065  0.7795±0.294  117.5±10.20  30  0.780 
N4325  4.134  11.322  4.25±0.4896  73.24±5.928  31  1.65 
N4284  4.209  11.585  1.699±0.1744  56.87±4.441  31  1.85 
N4145  4.026  11.131  0.993±0.1784  124.0±11.56  31  1.42 
N3901  4.071  11.122  0.888±0.139  28.68±2.396  33  1.9 
N4011  3.357  8.832  10.116±0.551  47.02±3.687  33  1.63 
N4115  4.293  11.784  9.551±1.126  75.32±4.602  33  1.92 
N4136  4.122  10.528  22.634±1.795  22.12±2.462  33  1.02 
N4276  4.491  11.467  2.556±0.448  65.22±7.612  33  1.46 
N4230  3.748  10.117  3.551±0.322  59.95±6.142  34  3.5 
N3913  4.247  11.092  1.444±0.233  30.04±3.152  34  1.96 
N3986  4.449  10.919  9.536±1.255  50.56±5.330  35  1.4 
N4113  3.189  9.173  7.149±1.022  75.35±7.662  35  1.3 
N4119  4.445  11.221  10.357±1.056  22.57±2.067  35  2.34 
N4257  3.682  10.251  3.048±0.472  51.36±4.841  35  2.2 
N4260  40.2  10.34  1.8±0.305  47.83±4.937  35  2.15 
N4083A  4.848  11.893  2.255±0.154  22.41±1.893  35  2.25 
N4232  4.138  11.905  16.117±1.874  18.75±1.413  36  2.66 
N4147  4.07  10.951  2.863±0.475  76.22±6.190  36  3.88 
N4111  3.914  11.641  20.782±1.296  105.5±8.113  37  4.23 
N4150  3.986  10.208  11.147±1.029  22.62±3.218  37  2.16 
N4297  4.313  11.555  5.233±0.524  109.1±9.913  37  1.4 
N3989  4.879  13.47  12.774±1.047  110.4±9.032  38  3.55 
N4019  5.865  14.985  10.028±0.908  76.11±10.24  38  3.44 
N4204  4.851  11.971  6.958±0.589  74.43±8.284  39  2.8 
N3894  3.623  11.214  3.701±0.452  112.5±9.923  40  3.56 
N4100  3.353  8.512  1.889±0.240  26.86±2.116  40  0.9 
N4107  3.592  11.174  12.609±1.94  124.1±9.532  40  0.9 
N4126  5.13  13.431  17.911±3.24  33.13±2.671  40  1.7 
N4140  4.5  11.866  8±0.917  24.90±2.074  40  1.35 
N4158  4.535  12.504  10.003±0.755  18.18±1.370  40  2.93 
N4176  3.395  9.463  4.078±0.327  64.04±6.370  40  1.28 

The tongue perimeter presented a positive and significant correlation with GA (rS=0.528; p<0.001; Fig. 3).

Figure 3.
(0.42MB).

Graphs showing the association of GA with tongue perimeter (A), tongue length (B), collagen fibers (C), and vessel perimeter (E). Fetal weight was associated with the collagen fibers (D) and the perimeter of the vessels (F).

The correlation of GA and tongue length was also positive and significant (rS=0.527; p<0.001; Fig. 3).

A positive and significant increase was observed in the correlation of the GA with collagen fibers (rS=−0.071; p=0.001; Fig. 3).

Considering the relationship between collagen fibers and fetal weight, a positive and significant correlation was observed (rS=0.143; p<0.001; Fig. 3).

The correlation between the GA and the perimeter of the blood vessels was positive and significant (rS=0.093; p<0.001; Fig. 3).

A correlation was observed between the perimeter of blood vessels and the fetal weight: there was an increase in the perimeter of the vessels, in tendency significant (rS=0.028; p=0.076; Fig. 3).

Discussion

The present study corroborates the literature, as a positive and significant increase in perimeter and length of the tongue was reported at different GAs.4,17 Fetal development is extremely important for the evaluation of the newborn, thus GA is an indispensable parameter for evaluation and survival after birth.18 Foot length is an important element for the structural assessment of the fetus at different GAs, because it is a body measurement that is closely related to GA, weight, and length.19

A positive and significant correlation was observed between collagen fibers in the tongue of stillborns and GA (23–40 weeks) and weight. This finding indicate that CNCC initiates and directly potentiates tongue development and gives rise to fibroblasts that promote the development of connective tissue.9,20

In addition, blood vessels perimeter was positively correlated with different GAs. The authors chose to use the perimeter for vessel morphometry using the CD31 marker, which has not yet been described in the literature. As observed in a study on stillborns with 20 to 40 weeks GA, anti-CD31 is a marker of vessels in relation to the development of GA.14,21

The present study corroborates the literature, in which 23 tongues of autopsied stillborns were analyzed, demonstrating that after the seventh week, the vessels (whose walls are beginning to develop) increase progressively. In the posterior region of the tongue, the blood vessels are small and form a very dense capillary network. The anterior vascularization of the tongue is greater, the vessels have smaller calibers, providing the conditions for a rapid supply of energy and nutrients to the myocytes. This capillary network of the tongue has been described in the literature as an important element against diseases.22–24

In turn, the increase of the perimeter of blood vessels correlated with the fetal weight was positive and tendency significant. There is a natural tendency for fetal growth during the different GAs, but some factors may cause changes in fetal weight, since this variable is different in each GA and depends on external factors, such as maternal nutrition. Intrauterine complications resulting in newborns with low birth weight (<2500g) are recognized as risk factors that contribute to the development of vascular diseases in adulthood.25 Fetal weight and GA should be taken into account due to the influence of other characteristics (genetic and socioeconomic factors). The increase in fetal weight may be related to a severe fetal complication, which generates a fetal systemic response characterized by edema, inflammation, and alteration of chemical mediators.26

The precise evaluation for growth in the neonatal period is important to observe if the fetus was subjected to abnormal intrauterine conditions that resulted in delayed growth acceleration.27 However, antenatal ultrasound detection and estimated fetal weight are far from straightforward, because these well-defined parameters are estimated using complex calculations that may give varying results for the same fetus. To further complicate matters, then obtained results can then be plotted on a number of different antenatal reference charts generated from local, national, or international cohorts, some of which are customized for maternal factors, such as parity, height, weight, and ethnicity. These variations contribute to large differences in antenatal detection abnormalities.28,29

Therefore, with the advance of GA, there is an increase in the perimeter and length of the tongue, an increase in the percentage of collagen fibers and an increase in the vascular perimeter, demonstrating that tongue formation is directly linked to fetal growth and development. Therefore, tongue embryogenesis would be a valid parameter to estimate GA in the pediatric autopsy, in conjunction with traditional methods.

Funding

Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Fundação de Ensino e Pesquisa de Uberaba (FUNEPU).

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgments

The present study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Fundação de Ensino e Pesquisa de Uberaba (FUNEPU).

References
[1]
M.C. Cohen, R. Drut
La autopsia en pediatría. Diagnóstico de situación en un hospital de pediatría de referencia
Arch Argent Pediatr, 101 (2003), pp. 166-170
[2]
I. Sato, M. Suzuki, M. Sato, T. Sato, S. Inokuchi
A histochemical study of lingual muscle fibers in rat
Okajimas Folia Anat Jpn, 66 (1990), pp. 405-415
[3]
K.R. Dalrymple, T.I. Prigozy, C.F. Shuler
Embryonic, fetal, and neonatal tongue myoblasts exhibit molecular heterogeneity in vitro
[4]
J.R. Siebert
A morphometric study of normal and abnormal fetal to childhood tongue size
Arch Oral Biol, 30 (1985), pp. 433-440
[5]
S.J. Hong, B.G. Cha, Y.S. Kim, S.K. Lee, J.G. Chi
Tongue growth during prenatal development in Korean fetuses and embryos
J Pathol Transl Med, 49 (2015), pp. 497-510 http://dx.doi.org/10.4132/jptm.2015.09.17
[6]
J.R. Siebert
Prenatal growth of the median face
Am J Med Genet, 25 (1986), pp. 369-379 http://dx.doi.org/10.1002/ajmg.1320250224
[7]
T. Inoue, K. Nakayama, Y. Ihara, S. Tachikawa, S. Nakamura, A. Mochizuki
Coordinated control of the tongue during suckling-like activity and respiration
J Oral Sci, 59 (2017), pp. 183-188 http://dx.doi.org/10.2334/josnusd.16-0850
[8]
R. Hosokawa, K. Oka, T. Yamaza, J. Iwata, M. Urata, X. Xu
TGF-beta mediated FGF10 signaling in cranial neural crest cells controls development of myogenic progenitor cells through tissue-tissue interactions during tongue morphogenesis
[9]
C. Parada, Y. Chay
Mandible and tongue development
Curr Top Dev Biol, 115 (2015), pp. 31-58 http://dx.doi.org/10.1016/bs.ctdb.2015.07.023
[10]
C. Parada, D. Han, Y. Chay
Molecular and cellular regulatory mechanisms of tongue myogenesis
J Dent Res, 91 (2012), pp. 528-535 http://dx.doi.org/10.1177/0022034511434055
[11]
J.E. Deanfield, J.P. Halcox, T.J. Rabelink
Endothelial function and dysfunction: testing and clinical relevance
Circulation, 115 (2007), pp. 1285-1295 http://dx.doi.org/10.1161/CIRCULATIONAHA.106.652859
[12]
K. Naruse, M. Fujieda, E. Miyazaki, Y. Hayashi, M. Toi, T. Fukui
An immunohistochemical study of developing glomeruli in human fetal kidneys
[13]
L.C. Junqueira, J. Carneiro
Histologia básica
O trato digestivo, 11th ed., pp. 284-285
[14]
L. Liu, G.P. Shi
CD31: beyond a marker for endothelial cells
Cardiovasc Res, 94 (2012), pp. 3-5 http://dx.doi.org/10.1093/cvr/cvs108
[15]
R. Achiron, A. Ben Arie, U. Gabbay, S. Mashiach, Z. Rotstein, S. Lipitz
Development of the fetal tongue between 14 and 26 weeks of gestation: in utero ultrasonographic measurements
Ultrasound Obstet Gynecol, 9 (1997), pp. 39-41 http://dx.doi.org/10.1046/j.1469-0705.1997.09010039.x
[16]
A.F. Zago, L.M. Paravidine, L.M. Siqueira, L.M. Balbão, M.A. Reis, E.C. Castro
Estudo comparativo entre o comprimento hálux-calcâneo e outros métodos de avaliação de idade gestacional em recém-nascidos
Pediatr Mod, 36 (2000), pp. 388-391
[17]
M. Bronshtein, E.Z. Zimmer, D. Tzidony, J. Hajos, M. Jaeger, S. Blazer
Transvaginal sonographic measurement of fetal lingual width in early pregnancy
Prenat Diagn, 18 (1998), pp. 577-580
[18]
E.F. Hutchinson, J.A. Kieser, B. Kramer
Morphometric growth relationships of the immature human mandible and tongue
Eur J Oral Sci, 122 (2014), pp. 181-189 http://dx.doi.org/10.1111/eos.12126
[19]
A.K. Salge, E.L. Rocha, M.A. Gaíva, T.C. Castral, J.V. Guimarães, R.M. Xavier
Medida do comprimento hálux-calcâneo de recém-nascidos em gestações de alto e baixo risco
Rev Esc Enferm USP, 51 (2017), pp. e03200 http://dx.doi.org/10.1590/S1980-220X2016016703200
[20]
J. Iwata, A. Suzuki, R.C. Pelikan, T.V. Ho, Y. Chai
Noncanonical transforming growth factor β (TGFβ) signaling in cranial neural crest cells causes tongue muscle developmental defects
J Biol Chem, 288 (2013), pp. 29760-29770 http://dx.doi.org/10.1074/jbc.M113.493551
[21]
M.L. Fonseca Ferraz, A.M. Dos Santos, C.L. Cavellani, R.C. Rossi, R.R. Corrêa, M.A. Dos Reis
Histochemical and immunohistochemical study of the glomerular development in human fetuses
Pediatr Nephrol, 23 (2008), pp. 257-262 http://dx.doi.org/10.1007/s00467-007-0654-4
[22]
R.I. Macleod, J.V. Soames
A morphometric study of age changes in the human lingual artery
Arch Oral Biol, 33 (1988), pp. 455-457
[23]
I. Granberg, B. Lindell, P.O. Eriksson, F. Pedrosa-Domellöf, P. Stål
Capillary supply in relation to myosin heavy chain fibre composition of human intrinsic tongue muscles
Cells Tissues Organs, 192 (2010), pp. 303-313 http://dx.doi.org/10.1159/000318645
[24]
A.R. Mangold, R.R. Torgerson, R.S. Rogers
Diseases of the tongue
[25]
Y. Kandasamy, R. Smith, I.M. Wright, L. Hartley
Relationship between birth weight and retinal microvasculature in newborn infants
J Perinatol, 32 (2012), pp. 443-447 http://dx.doi.org/10.1038/jp.2011.118
[26]
R.R. Corrêa, L.P. Rocha, C.G. Petrini, V.P. Texieira, E.C. Castro
Influência da causa de morte no peso corporal e dos órgãos internos em autópsias perinatais
Rev Bras Ginecol Obstrt, 36 (2014), pp. 23-28
[27]
R. Thawani, P. Dewan, M.M. Faridi, S.K. Arora, R. Kumar
Estimation of gestational age, using neonatal anthropometry: a cross-sectional study in India
J Health Popul Nutr, 31 (2013), pp. 523-530
[28]
J. Gardosi, M. Mongelli, M. Wilcox, A. Chang
An adjustable fetal weight standard
Ultrasound Obstet Gynecol, 6 (1995), pp. 168-174 http://dx.doi.org/10.1046/j.1469-0705.1995.06030168.x
[29]
B. Poljak, U. Agarwal, R. Jackson, Z. Alfirevic, A. Sharp
Diagnostic accuracy of individual antenatal tools for prediction of small-for-gestational age at birth
Ultrasound Obstet Gynecol, 49 (2017), pp. 493-499 http://dx.doi.org/10.1002/uog.17211

Please cite this article as: Aguiar LS, Juliano GR, Silveira LA, Oliveira MS, Torquato BG, Juliano GR, et al. Tongue development in stillborns autopsied at different gestational ages. J Pediatr (Rio J). 2018;94:616–23.

Study conducted at Universidade Federal do Triângulo Mineiro (UFTM), Instituto de Ciências Biológicas e Naturais, Disciplina de Patologia Geral, Uberaba, MG, Brazil.

Copyright © 2017. Sociedade Brasileira de Pediatria
Idiomas
Jornal de Pediatria (English Edition)

Subscribe to our Newsletter

Article options
Tools
en pt
Taxa de publicaçao Publication fee
Os artigos submetidos a partir de 1º de setembro de 2018, que forem aceitos para publicação no Jornal de Pediatria, estarão sujeitos a uma taxa para que tenham sua publicação garantida. O artigo aceito somente será publicado após a comprovação do pagamento da taxa de publicação. Ao submeterem o manuscrito a este jornal, os autores concordam com esses termos. A submissão dos manuscritos continua gratuita. Para mais informações, contate assessoria@jped.com.br. Articles submitted as of September 1, 2018, which are accepted for publication in the Jornal de Pediatria, will be subject to a fee to have their publication guaranteed. The accepted article will only be published after proof of the publication fee payment. By submitting the manuscript to this journal, the authors agree to these terms. Manuscript submission remains free of charge. For more information, contact assessoria@jped.com.br.
Cookies policy Política de cookies
To improve our services and products, we use "cookies" (own or third parties authorized) to show advertising related to client preferences through the analyses of navigation customer behavior. Continuing navigation will be considered as acceptance of this use. You can change the settings or obtain more information by clicking here. Utilizamos cookies próprios e de terceiros para melhorar nossos serviços e mostrar publicidade relacionada às suas preferências, analisando seus hábitos de navegação. Se continuar a navegar, consideramos que aceita o seu uso. Você pode alterar a configuração ou obter mais informações aqui.