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ROZWÓJ GAŁKI OCZNEJ I OCZODOŁU CZŁOWIEKA W ŻYCIU PŁODOWYM

1 Katedra i Zakład Anatomii Prawidłowej Pomorskiej Akademii Medycznej al. Powstańców Wlkp. 72, 70-111 Szczecin

Head: Prof. Florian Czerwiński M.D., D.M.Sc. Habil.

2 Katedra i Klinika Okulistyki Pomorskiej Akademii Medycznej al. Powstańców Wlkp. 72, 70-111 Szczecin Head: Prof. Danuta Karczewicz M.D., D.M.Sc. Habil.

3 Katedra i Zakład Mikrobiologii i Immunologii Pomorskiej Akademii Medycznej al. Powstańców Wlkp. 72, 70-111 Szczecin

Head: Prof. Stefania Giedrys-Kalemba M.D., D.M.Sc. Habil.

streszczenie

Wstęp: Celem pracy było dokonanie oceny rozwoju gałki ocznej i oczodołu człowieka w życiu płodowym.

Materiał i metody: Przebadano 18 martwych płodów ludzkich (36 oczu i 36 oczodołów) w wieku od 17 do 28 tygodnia ciąży. Badane płody zmarły w pierwszych go-dzinach życia z powodu wcześniactwa. Nie wykazywały żadnych widocznych wad rozwojowych. Mierzono u nich długość osiową i średnicę równikową gałek ocznych oraz głębokość i szerokość oczodołów. Dane opracowano staty-stycznie testem t-Studenta oraz współczynnikami korelacji Pearsona.

Wyniki: Wykazano, że wraz z wiekiem rośnie długość osiowa (p < 0,005) i średnica równikowa (p < 0,001) gałki ocznej (ryc. 1). Stwierdzono, że wraz z wiekiem rośnie głę-bokość (p < 0,001) i szerokość (p < 0,001) oczodołu (ryc. 2).

Zaobserwowano również, że wraz ze wzrostem długości osiowej oka zwiększa się głębokość oczodołu (p < 0,001), a wraz ze wzrostem średnicy równikowej gałki ocznej rośnie szerokość oczodołu (p < 0,001) (ryc. 3). W pracy wykazano, że w życiu płodowym człowieka wzrost gałki ocznej koreluje ze wzrostem oczodołu.

H a s ł a: płód – gałka oczna – oczodół – rozwój.

summary

Purpose: The aim of this paper was to describe the development of the human eyeball and orbit during fetal life.

Material and methods: Eighteen human fetuses (36 eyes and 36 orbits) with gestational age ranging from 17 to 28 weeks were examined. Fetuses died in the first hours of life due to immaturity and did not reveal any developmental anomalies. The axial and equatorial dia-meters of the eyeballs as well as the depth and width of the orbits were measured. The data was analyzed stati-stically with Student’s t-test and Pearson’s correlation coefficients.

Results: It was found that the axial length (p < 0.005) and equatorial diameter (p < 0.001) of the eyeballs, as well as the depth (p < 0.001) and width (p < 0.001) of the orbit increase with age. Furthermore, growth of the axial length of the eye is paralleled by increase in orbital depth (p < 0.001) while growth of the equatorial diameter coincides with increasing orbital width (p < 0.001). It was ascertained that growth of the human eye during fetal life is correlated with growth of the orbit.

K e y w o r d s: fetus – eyeball – orbit − development.

38 EWA TOMASIK, DAMIAN CZEPITA, MARIA ŻEJMO, FLORIAN CZERWIŃSKI

introduction

Based on clinical and experimental investigations it can be assumed that orbital development depends on growth of the eye [1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20]. However, it has not been established how growth of the eyeball affects the development of the orbit. Due to ethical reasons, experimental studies cannot be performed on human fetuses. Therefore, all observations bringing us closer to elucidation of the problem are scientifically impor-tant. We have therefore decided to study the development of the human eye and orbit during fetal life.

material and methods

Eighteen human fetuses (36 eyeballs and 36 orbits) aged from 17 to 28 weeks, without any signs of develop-mental anomalies, were examined. All fetuses died in the first hours of life due to immaturity. Fetuses were placed in 10% formalin prior to the study.

Fetal age was calculated on the basis of the crown-rump length (CRL), crown-heel length (CHL), and body mass [21, 22]. Clinical data was also considered in determining the age of the fetuses. The bodies did not display any symptoms of maceration or postmortem autolysis.

Eyeballs followed by orbits were dissected from the fetal body and transferred to 0.9% saline for a few days prior to measurements. The axial and equatorial diameters of the eyes as well as the depth and width of the orbits were measured using vernier calipers.

The axial length was taken as the distance between the peak of the cornea and the peak of the posterior segment of the eyeball. The equatorial diameter was regarded as the width of the eye at the equator. The depth of the orbit was taken as the distance from the supraorbital margin to the optic canal. The width of the orbit was equal to the distance from the frontozygomatic suture to the frontomaxillary suture.

Data was analyzed statistically with Student’s t-test and Pearson’s correlation (PC) coefficients. P values smaller than 0.05 were considered to be statistically significant.

Statistica 99 PL Software was used for analysis.

The study protocol was approved by the Bioethics Committee of the Pomeranian Medical University.

results

We found that the axial length (PC = 0.509, p < 0.005, Fig. 1A) and equatorial diameter (PC = 0.557, p < 0.001, Fig. 1B) of the eyeball increase with age.

As a result of ageing, the depth (PC = 0.458, p < 0.001, Fig. 2A) and width (PC = 0.536, p < 0.001, Fig. 2B) of the orbit increase.

The axial length of the eye and the orbital depth in-crease in parallel (PC = 0.805, p < 0.001, Fig. 3A). The

equatorial diameter of the eyeball increased concurrently with orbital width (PC = 0.864, p < 0.001, Fig. 3B).

discussion

The results indicate that the axial length and equatorial diameter of the eye as well as the depth and width of the orbit increase with age. The increase in axial length of the eyeball is associated with increase in the orbital depth, while the increase in equatorial diameter of the eye is as-sociated with the increase in orbital width.

It is widely accepted that the normal shape and size of the orbit result from a balance between a number of genetic and epigenetic factors which may function on a systemic, regional or local scale. The development of the orbital cavity is related to the development of the nasal cavity, parana-sal sinuses, temporal fossa and cranial cavity. However, growth of the eyeball in relation to the orbit is not fully understood. Moreover, the role of the nerves, vessels, fat and glands taking part in the orbital development has not been decisively established [2, 5, 19].

In postnatal experiments conducted on animals (frogs, newts, chicks, rabbits, cats, dogs, pigs, sheep, and primates) it was observed that evisceration, enucleation or

exentera-Fig. 1. Changes in axial length (A) and equatorial diameter (B) of the eyeball depending on age of the fetus

Ryc. 1. Zachowanie się długości osiowej (A) i średnicy równikowej gałki ocznej (B) w zależności od wieku płodu

A

B

16 18 20 22 24 26 28 30

Age (weeks) / Wiek (tygodnie) 6

7 8 9 10 11 12 13

6 7 8 9 10 11 12 13

16 18 20 22 24 26 28 30

Axiallenght/Długośćosiowa(mm)Equatorialdiameter/Średnicarównikowa(mm)

Age (weeks) / Wiek (tygodnie)

39

DEVELOPMENT OF THE HUMAN EYEBALL AND ORBIT DURING THE FETAL LIFE

tion of the orbit leads to a reduction and shallowness of the orbit [1, 2, 3, 4, 7, 8, 9, 11, 12, 13, 19]. On the other hand, enlargement of the eye causes an increase in the dimensions and volume of the orbit [2, 6, 7, 8, 9, 10].

It was observed in unilaterally microphthalmic chick embryos that the calvaria, facial skeleton, and orbit on the side of the operation are small. It thus appears that the eyeball as well as other structures play an important role in controlling the growth of the orbit [14, 15, 16, 17, 18, 19, 20].

In clinical observations performed on humans it was observed that anophthalmia and microphthalmia are as-sociated with smaller orbits and lessened growth of the orbit, depending on the age when the problem arose. It was described that enucleation of one eye before the age of five years could lead to a persisting deficiency of bone growth in the orbital margin by as much as 15 percent on the enucle-ated side as compared with the other side. Enucleation at 9 years of age and after did not lead to appreciable alteration.

It was also observed that removal of orbital contents by the age of two does not result in deceleration of orbital growth [2, 3, 4, 5, 7, 9, 19].

These findings prove that the eyeball as well as the orbital elements play an important role in orbital develop-ment. Our present study has shown a simultaneous increase

in dimensions of the eye and orbit occurs during fetal life in humans.

references

1. Apt L., Isenberg S.: Changes in orbital dimensions following enucle-ation. Arch. Ophthalmol. 1973, 90, 393.

2. Hoyte D. A. N.: Growth of the orbit. In: Fundamentals of craniofacial growth. Eds. A. D. Dixon, D. A. N. Hoyte, O. Rőnning. CRC Press, New York 1997, p. 225−255.

3. Kennedy R. E.: The effect of early enucleation on the orbit in animals and humans. Am. J. Ophthalmol. 1965, 60, 277.

4. Kennedy R. E.: The effect of early enucleation on the orbit in animals and humans. Trans. Am. Ophth. Soc. 1964, 62, 459.

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10. Sarnat B. G., Shanedling P. D.: Increased orbital volume after periodic intrabulbar injection of silicone in growing rabbits. Am. J. Anat. 1974, 140, 523.

Fig. 2. Changes in the depth (A) and width (B) of the orbit depending on age of the fetus

Ryc. 2. Zachowanie się głębokości (A) i szerokości (B) oczodołu w zależności od wieku płodu

A

B

10 12 14 16 18 20

16 18 20 22 24 26 28 30

16 18 20 22 24 26 28 30

8 10 12 14 16 18

Depth/Głębokość(mm)Width/Szerokość(mm)

Age (weeks) / Wiek (tygodnie)

Age (weeks) / Wiek (tygodnie)

Fig. 3. Changes in the depth of the orbit depending on the axial length of the eyeball (A) as well as changes in the width of the orbit depending on

the equatorial diameter of the eyeball (B)

Ryc. 3. Zachowanie się głębokości oczodołu w zależności od długości osiowej gałki ocznej (A) oraz zachowanie się szerokości oczodołu

w zależności od średnicy równikowej gałki ocznej (B)

A

B

6 7 8 9 10 11 12 13

10 12 14 16 18 20

6 7 8 9 10 11 12 13

8 10 12 14 16 18

Width/Szerokość(mm)Depth/Głębokość(mm)

Axial lenght / Długość osiowa (mm)

Equatorial diameter / Średnica równikowa (mm)

40 EWA TOMASIK, DAMIAN CZEPITA, MARIA ŻEJMO, FLORIAN CZERWIŃSKI 11. Sarnat B. G., Shanedling P. D.: Orbital growth after evisceration or

enucleation without and with implants. Acta Anat. 1972, 82, 497.

12. Sarnat B. G., Shanedling P. D.: Orbital volume following evisceration, enucleation and exenteration in rabbits. Am. J. Ophthalmol. 1970, 70, 787.

13. Sarnat B. G., Shanedling P. D.: Postnatal growth of the orbit and upper face in rabbits after exenteration of the orbit. Arch. Ophth. 1965, 73, 829.

14. Tonneyck-Müller I.: Das Wachstum von Augen und Augenhöhlen beim Hühnerembryo. VI. Die Entwicklung der Augen und Schädelanlage bei Embryonen von 7−10 Tagen mit künstlich erzeugter einseitiger Mikrophthalmie. Acta Morphol. Neerl-Scand. 1971/72, 9, 235.

15. Tonneyck-Müller I.: Das Wachstum von Augen und Augenhöhlen beim Hühnerembryo. V. Die Entwicklung der Augen und Schädelanlage bei Embryonen mit künstlich erzeugter einseitiger Mikrophthalmie von 3−6 Tagen. Acta Morphol. Neerl-Scand. 1971, 9, 57.

16. Tonneyck-Müller I.: Das Wachstum von Augen und Augenhöhlen beim Hühnerembryo. IV. Die Wachstum des Schädels bei Embryonen von 11−19 Tagen mit künstlich erzeugter einseitiger Mikrophthalmie. Acta Morphol. Neerl-Scand. 1970/71, 8, 303.

17. Tonneyck-Müller I., Van Limborgh J.: Das Wachstum von Augen und Augenhöhlen beim Hühnerembryo. III. Die quantitativen Verhältnisse der Augenhöhlen und des Kreuzschnabels bei Embryonen von 11−19 Tagen mit künstlich erzeugter einseitiger Mikrophthalmie. Acta Mor-phol. Neerl-Scand. 1970/71, 8, 293.

18. Tonneyck-Müller I., Van Limborgh J.: Das Wachstum von Augen und Augenhöhlen beim Hühnerembryo. II. Die Grössenverhältnisse der Au-gen und AuAu-genhöhlen bei Embryonen von 11−19 TaAu-gen mit künstlich erzeugter einseitiger Mikrophthalmie. Acta Morphol. Neerl-Scand.

1970/71, 8, 211.

19. Van Limborgh J.: Factors controlling skeletal morphogenesis. In:

Factors and mechanisms influencing bone growth. Eds. A. D. Dixon, B. G. Sarnat. Alan R. Liss, New York 1982, p. 1−17.

20. Van Limborgh J., Tonneyck-Müller I.: Orbital growth pattern in expe-rimental microphthalmia. Mod. Probl. Ophthal. 1975, 14, 1.

21. Bożiłow W., Sawicki K.: Investigative methods of studying variable human anatomical traits during prenatal and perinatal development (in Polish). Akad. Med., Wrocław 1980.

22. Bożiłow W., Sawicki K.: Methodics of anthropometric investiganions on fetuses (in Polish). Mat. Prac. Antrop. 1972, 83, 185.

An nAles AcAdemiAe medicAe steti nensis, 2005, 51, 41– 47

r o c z n i k i p o m o r s k i e j a k a d e m i i m e d y c z n e j w s z c z e c i n i e AnnAls of tHe PomerAniAn medicAl University, 2005, 51, 41–47

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