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Sonographic cerebral sulcal development in premature newborns
Sonographic Cerebral Sulcal Development in Premature Newborns Chao-Ching Huang, MD
Cranial ultrasound examinations with 5.0 and 7.5 mHZ transducers during the first 3 days of life on 60 appropriate-fordate newborns with gestational age 24-36 wks were performed to determine the sulcal development of cerebral cortex in utero. The sulci appeared and developed in sequence. All the calcarine fissure and most of the anterior part of cingulate sulcus began to appear before 28 wks. At 28-31 wks all the whole cingulate sulcus and postrolandic sulcus, and most of the inferior tempC!ral sulcus and covering of insula were ready to be observed. All of the insular sulci and tertiary sulci, and most of the secondary sulci from cingulate sulcus appeared after 31 wks. As cortical organization advanced, the discrepancy in the age of sulcal appearance between neuroanatomic and ultrasonic studies became less striking by the last trimester. Ultrasonic examination of the cortical sulci provides a noninvasive and convenient means to stage the normal cerebral maturation, and can be helpful in the detection of pathology in sulcal formations. Key words: Cerebral ultrasound, sulcal development, prematurity. Huang C-c. Sonographic cerebral sulcal development in premature newborns. BrainDev 1991;13:27-31
Cranial ultrasound through the anterior fontanelle has been widely used as an effective diagnostic tool for the detection of intracranial pathology in newborn infants. Besides abnormal fmdings, normal anatomy of the brain delineated by ultrasound has also been studied by several investigators [1-8]. Their studies have demonstrated sonographic anatomy of basal ganglia [3,4]' cerebellum [5, 6], and occipital lobe [7, 8]. Cortical sulcal development demonstrated by ultrasound has not been reported in detail. Only the cingulate sulcus development in preterm infants was described and correlated with gestational parameters [9, 10]. Since the sequential developmental changes of the fissures, sulci and gyri of the cerebral hemispheres throughout the gestational period has been tabulated by neuropathologists [11, 12]. It is the purpose of this study to evaluate the appearance and maturation of different cerebral sulci by sonography at various gestational ages ranging from 24-36 wks.
From the Department of Pediatrics, National Cheng Kung University Hospital, Tainan, Taiwan. Received for pUblication: March 19, 1990. Accepted for publication: February I, 1991. Correspondence address: Dr. Chao-Ching Huang, Department of Pediatrics, National Cheng Kung University Hospital, 138, Shen-Li Rd, Tainan, 70428 Taiwan, Republic of China.
MATERIALS AND METHODS All the newborns studied were born to mothers with regular menstrual cycles. The gestational age was estimated from the first day of last normal menstrual period and confirmed by at least one second trimester prenatal sonographic examination. Only the appropriate-for-date newborns were included for study and cerebral sonographic examinations were taken within 3 days of life. Sonographic evaluations were performed through anterior fontanelle using Aloka SSD 630 sector scanner with 5.0 and 7.5 mHZ transducers. Images were taken in coronal, sagittal, parasagittal and tangential planes, and then photographed. Prospectively, the presence and maturation of the following selected sulci were recorded in each newborn: parieto-occipital fissure, calcarine fissure, cingulate sulcus, postrolandic sulcus, covering of insula, inferior temporal sulcus, insular sulci, and secondary and tertiary sulci from cingulate sulcus. Covering of insula was detected by 5.0 mHZ transducer in coronal ,dew at the plane of frontal horns oflateral ventricles. Inferior temporal sulcus and insular sulci were scanned by 5.0 mHZ transducer in parasagittal views. Postrolandic sulcus was found by 5.0 mHZ or 7.5 mHZ transducer in tangential views. Parietooccipital fissure and calcarine fissure, cingulate sulcus and its secondary and tertiary sulci were detected by 5.0 mHZ and 7.5 mHZ transducers respectively in sagittal views. Newborns with severe intraventricular hemorrhage and congenital malformation were excluded.
Table 1 Case numbers of sonographic visualization of the selected sulci at each gestational age group Vis ualized sulci
24-25 wks
26-27 wks
28-29 wks
30-31 wks
32-33 wks
34-35 wks
36 wks
Total
Parieto-occipital Calcarine Cingulate anterior whole Postrolandic Covering of insula Inferior temporal Secondary Insular partial whole Tertiary
8 6
12 12
12 12
11 11
7
6 6
4 4
60 58
2 0 0 0 0 0
10 1 5 0 0 0
12 10 12 3 2 0
11
7
10 10 3
7
6 6 6 6 6 6
4 4 4 4 4 4
52 39 45 30 29 20
0 0 0
0 0 0
0 0 0
0 0 0
4 0 0
6 4
4 4 2
14 8 3
Total
8
12
12
11
7
6
4
60
Fig 1 From a 24 weeks gestation neonate. A : Coronal view shows the widely· opened lateral sulcus (arrow). B: Sagittal view shows
the parieto·occipital fissure (arrow) and cingulate sulcus is absent.
7
11
7
11
7
7 7
Fig 2 Sagittal views. A : The calcarine fissure (arrow) begins to separate from the parieto-occipital fissure at 25 weeks gestation. B: The parieto-occipital fissure and calcarine rlSsure (arrow) are now Y-shaped in a 29 weeks neonate.
RESULTS Sixty infants were studied with a gestational age ranging from 24 to 36 wks. The sonographic findings of the sulci in each gestational age group are presented in Table 1. Lateral sulcus was widely opened in each case below 28 wks of gestation (Fig lA) and was closed with covering of the insula in all except one case above 29 wks. Parietooccipital fissure was already present in all cases, even by 24 wks (Fig 1B). Calcarine fissure branched and developed from parieto-occipital fissure in 6 of 8 cases at 24-25 wks (Fig 2A) and was present in all cases above 25 wks (Fig 2B). Postrolandic sulcus appeared in 5 of the 12 cases at 26-27 wks and was present in all cases above 27 wks (Fig 3A). Inferior temporal sulcus appeared in only 2 of the 12 cases at 28-29 wks, but could be demonstrated in all except one case by 30-31 wks (Fig 3B). Anterior
28 Brain & Development, Vol 13, No 1, 1991
Fig 3 A: In tangential view, the postrolandic sulcus (arrow) appears in a 28 weeks newborn. B: In parasagittal View, the inferior temporal sulcus (arrow) develops in a 30 weeks newborn.
Fig 4 Sagittal views. A: Anterior part of cingulate sulcus (arrow) develops in a 26 weeks neonate. B: Development of a whole straight cingulate sulcus (arrow) in a 28 weeks neonate.
Fig 5 Sagittal views. A :Notice the curvy cingulate sulcus (arrow) in a 30 weeks neonate. B: Secondary sulci (arrowhead) begin to bud from the cingulate sulcus in a 31 weeks neonate.
Fig 6 Sagittal views. A: More secondary sulci (arrow) develop from cingulate sulcus in a 34 weeks neonate. B : The tertiary sulci (arrowhead) from cingulate sulcus in a 36 weeks neonate.
Fig 7 Parasagittal views. A : Insular sulci (arrow) begin to develop in a 34 weeks neonate. B: Complete mature insular sulci (arrow) develop in a 36 weeks neonate.
cingulate sulcus (Fig 4A) first appeared in only 2 of the 8 cases at 24-25 wks, but was present in 10 of the 12 cases at 26-27 wks and in all the cases above 27 wks. The cingulate sulcus developed and extended posteriorly in only 1 of the 12 cases at 26-27 wks gestation, but the whole cingulate sulcus was present in 10 of the 12 cases at 28-29 wks (Fig 4B). Thereafter, the cingulate sulcus became curvy (Fig 5A) and secondary sulci began to branch from it in 3 of the 11 cases at 30-31 wks (Fig 5B). By 32-33 wks, secondary sulci from cingulate sulcus became present in all the cases. Further development and branching of the secondary sulci into tertiary sulci was noted in only 1 of the 6 cases at 34-35 wks and in 2 of the 4 cases at 36 wks (Figs 6A, 6B). Partial insular sulci appeared in 4 of the 7 cases at 32-33 wks and the whole insular sulci were present in 4 of the 6 cases at 34-35 wks while appearing in all cases at 36 wks (Figs 7 A, 7B). Anterior cingulate sulcus appeared in 52 cases and 50 (96%) of them were above 25 wks of gestation. Whole
cingulate sulcus was present in 39 cases and 38 (97%) of them were above 27 wks. There were 45 cases with postrolandic sulcus and 40 (89%) of them were above 27 wks. In 30 cases with covering of the insula, 27 (90%) of them were above 29 wks. In all, 29 cases had inferior temporal sulcus, 27 (93%) of them being above 29 wks. Partial insular sulci appeared in 14 cases all of which were above 31 wks. Secondary sulci were present in 20 cases and 17 (85%) of them were above 31 wks. Whole insular sulci were detected in 8 cases and all of them (100%) were above 33 wks. Tertiary sulci were present in 3 cases and 2 (67%) of them were above 35 wks.
DISCUSSION Developmental maturation is a better indicator of gestational age than simple anthropometric measurements [12]. The sequence of sulcal and gyral development of the brain in newborns at various gestational ages has been
Huang C-C: Sulcal development in prematurity 29
Table 2 Selected gestational age-dependent sulcal-gyral patterns based on cerebral sonographic examinations
24-25 weeks Prominent parieto-occipital fissure Early branching of calcarine fissure 26-27 weeks More maturation of calcarine fissure Appearance of anterior cingulate sulcus 28-29 weeks Development of whole cingulate sulcus Appearance of postrolandic sulcus Closing of lateral sulcus 30-31 weeks Covering of insula Bending and curvature of cingulate sulcus Appearance of inferior temporal sulcus Occasional secondary sulci budding from cingulate sulcus 32-33 weeks Branching of secondary sulci from cingulate sulcus Appearance of partial insular sulci 34-35 weeks Further development of insular sulci More maturation of secondary sulci Occasional tertiary sulci 36 weeks Development of tertiary sulci Maturation of insular sulci
studied, and is a reliable guide to the gestational age [11-13]. No descriptive sonographic data about sequential developments of different sulci has been published. In this study, by using proper transducers and scanning planes, several cerebral sulci were visualized at certain gestational ages. From the smooth contour of the immature brain to multiple convolutions that typify the mature brain, these cerebral sulci emerge in three distinctive gestational age groups: < 28 wks, 28-31 wks and > 31 wks. All calcarine fissure and most of the anterior part of cingulate sulcus begin to appear below 28 wks. At 28-31 wks all the whole cingulate sulcus and postrolandic sulcus, and most of the inferior temporal sulcus and covering of insula are ready to be observed. All of the insular sulci and tertiary sulci, and most of the secondary sulci from cingulate sulcus appear after 31 wks. Selected ultrasonic sulcal patterns in Table 2 represent the regional or hemispheric gyral maturation at various gestational ages. This sonographic sulcal maturation sequence relates with the EEG maturation patterns in preterm infants, which were described by Scher et al and Niedermeyer [13, 14J. The prominent occipital slow wave activity and vertex-central delta brush below 28 wks of gestation correspond to the early developments of occipital lobe (parieto-occipital and calcarine fissures) and
30 Brain & Development, Vol 13, No1, 1991
rolandic area (cingulate and postrolandic sulci) at this gestational age. By 28-31 wks the appearance of delta brush at temporal and occipital areas corresponds to the covering of insula and more development of temporal (inferior temporal sulcus) and occipital lobes (formation of cuneus). And after 31 wks decrease in periods of quiescence in EEG activity and a greater degree of interhemispheric synchrony may be associated with the development of secondary and tertiary sulci and more organization of cerebral cortex. Because of its central location and developmental symmetry, the imaging of the cingulate sulcus in preterm newborns had been used as a qualitative assessment of brain maturation [9]. And Worthern et al [10] were able to show retrospectively good correlation between three sonographic developmental stages of the cingulate sulcus with gestational parameters, such as birth weight, birth length and gestational age by date and by Dubowitz score. In addition to the cingulate sulcus, many other important sulci, as shown in this study, can be readily demonstrated by ultrasound and are also related to maturation. Serial imaging of several distinctive cerebral sulci can be more valuable than the cingulate sulcus alone in qualitative brain development, and the sonographic fmdings can supplement the clinical examination criteria for gestational age assessment [15]. Although the sequence of events demonstrated by ultrasound corresponded well to the sulcal development established from anatomic studies, the anatomic ages of appearance of cerebral sulci [11, 12] were earlier than the ages of appearance by ultrasound. The differences were about 8-9 wks in the age group below 28 wks, which included calcarine fissure and cingulate sulcus. There were only about 1-3 wks difference in the age group at 28-31 wks, which included postrolandic sulcus and inferior temporal sulcus. While there were no differences in age of appearance in the age group above 31 wks, which included secondary and tertiary branches from cingulate sulcus, and insular sulci. The younger the brain the larger the differences in time of sulcal appearance between neuroanatomy and sonography. Although anatomically evident in the immature brain, the shallow indentation of the sulcus could not be demonstrated by ultrasound. The immature sulcus gradually increased in depth over several weeks before well demarcated by ultrasound. The differences might be related to the degree of organization of the cerebral cortex which occurred from the sixth month of gestation to years after birth. The organization included: alignment orientation and layering of cortical neurons; dendritic and axonal ramification; establishment of synaptic contacts and glial proliferation and differentiation. This major development occurred especially in the third trimester which resulted in rapid increase in cortical thickness and brain surface areas [16,17]. By 24 wks of gestation the calcarine fissure and cingulate sulcus in the
less organized immature brain, which could be recognized by neuropathologists, were not deepened enough to be demonstrated by the 5.0 or 7.5 mHZ ultrasonic transducer. After 28 wks, in the more organized mature brain, the newly developed sulci could be readily demonstrated by ultrasound. In conclusion, ultrasound provides a noninvasive and useful method to clarify cortical sulcal structures. The sequential normal appearances and maturations of several fissures and sulci can be mapped by ultrasound and clinically be a morphologic indicator of gestational age. And it can be helpful in the evaluation of congenital abnormalities of sulcal formations, such as lissencephaly, microgyria and macrogyria. Prospective study of sonographic sulcal developments in appropriate-for-date and small-fordate newborns is undertaken to evaluate any temporal differences in maturation sequence. REFERENCES 1. Fisher AQ, Anderson JC, Shumen RM, Stinson W. Pediatric neurosonography: clinical, tomographic, and neuropathologic cOffelates. New York: Wiley Medical Publication, 1985:45106. 2. Mack LA, Alvord EC, Cyr DR, Aitken AGF, Richardson TE. The neonatal brain: nonnal appearances. In: Rumack CM, Johnson ML, eds. Perinatal and infant brain imaging. Chicago: Year Book Medical Publishers, 1984: 39-59. 3. Naidich TP, Gusnard DA, Yousefzadeh DK. Sonography of the internal capsule and basal ganglia in infants: 1. Coronal sections. AJNR 1985;6:909-17. 4. Naidich TP, Yousefzadeh DK, Gusnard DA. Sonographyof the normal neonatal head. Supratentorial structures: state of the art imaging. Neuroradiology 1986;28:408-27.
5. Yousefzadeh DK, Naidich TP. US anatomy of the posterior fossa in children: correlation with brain sections. Radiology 1985; 156: 353-61. 6. Sasaki M, Yoshioka K, Yanagisawa T, et al. Normal sonographic findings of the posterior cranial fossa in infants (in Japanese). No To Hattatsu (Tokyo) 1987; 19:363-70. 7. DiPietro MA, Brody BA, Teele RL. The calcar avis: demonstration with cranial US. Radiology 1985; 156: 363-4. 8. Vade A, Otto R. Cranial sonography of the occipital horns and gyral patterns in the occipital lobes. AJNR 1986; 7: 873-7. 9. Slagle TA, Michael 0, Gross SJ. Cingulate sulcus development in preterm infants. Pediatr Res 1989;26:598-602. 10. Worthen NJ, Gilbertson V, Lau C. Cortical sulcal development seen on sonography: relationship to gestational parameters. J Ultrasound Med 1986;5:153-6. 11. Dorovini-Zis K, Dolman CL. Gestational development of the brain. Arch Pathol Lab Med 1977; 101: 192-5. 12. Chi JG, Dooling EC, Gilles FH. Gyral development of the human brain. Ann Neurol 1977; 1:86-93. 13. Scher MS, Mamdouha AB. Estimation of gestational age by electrographic, clinical, and anatomical criteria. Pediatr NeuroI1987;3:256-62. 14. Niedermeyer E. Maturation of the EEG: Development of waking and sleep patterns. In: Niedermeyer E, Fernando LDS, eds. Electroencephalography: basic principles, clinical applications and related fields. Baltimore· Munich: Urban & Schwarzenberg, 1982: 107-30. 15. Murphy NP, Rennie J, Cooke RWI. Cranial ultrasound assessment of gestational age in low birthweight infants. Arch Dis Child 1988;64:569-72. 16. England MA. Normal development of the central nervous system. In: Levene MI, Bennett MJ, Punt J, eds. Fetal and neonatal neurology and neurosurgery. Edinburgh: Churchill Livingstone, 1988: 1-27. 17. Volpe 11. Neurology of the newborn. 2nd. Philadelphia: WB Saunders Company, 1987: 33-68.
Huang C-C: Sulcal development in prematurity 31
Cranial ultrasound examinations with 5.0 and 7.5 mHZ transducers during the first 3 days of life on 60 appropriate-fordate newborns with gestational age 24-36 wks were performed to determine the sulcal development of cerebral cortex in utero. The sulci appeared and developed in sequence. All the calcarine fissure and most of the anterior part of cingulate sulcus began to appear before 28 wks. At 28-31 wks all the whole cingulate sulcus and postrolandic sulcus, and most of the inferior tempC!ral sulcus and covering of insula were ready to be observed. All of the insular sulci and tertiary sulci, and most of the secondary sulci from cingulate sulcus appeared after 31 wks. As cortical organization advanced, the discrepancy in the age of sulcal appearance between neuroanatomic and ultrasonic studies became less striking by the last trimester. Ultrasonic examination of the cortical sulci provides a noninvasive and convenient means to stage the normal cerebral maturation, and can be helpful in the detection of pathology in sulcal formations. Key words: Cerebral ultrasound, sulcal development, prematurity. Huang C-c. Sonographic cerebral sulcal development in premature newborns. BrainDev 1991;13:27-31
Cranial ultrasound through the anterior fontanelle has been widely used as an effective diagnostic tool for the detection of intracranial pathology in newborn infants. Besides abnormal fmdings, normal anatomy of the brain delineated by ultrasound has also been studied by several investigators [1-8]. Their studies have demonstrated sonographic anatomy of basal ganglia [3,4]' cerebellum [5, 6], and occipital lobe [7, 8]. Cortical sulcal development demonstrated by ultrasound has not been reported in detail. Only the cingulate sulcus development in preterm infants was described and correlated with gestational parameters [9, 10]. Since the sequential developmental changes of the fissures, sulci and gyri of the cerebral hemispheres throughout the gestational period has been tabulated by neuropathologists [11, 12]. It is the purpose of this study to evaluate the appearance and maturation of different cerebral sulci by sonography at various gestational ages ranging from 24-36 wks.
From the Department of Pediatrics, National Cheng Kung University Hospital, Tainan, Taiwan. Received for pUblication: March 19, 1990. Accepted for publication: February I, 1991. Correspondence address: Dr. Chao-Ching Huang, Department of Pediatrics, National Cheng Kung University Hospital, 138, Shen-Li Rd, Tainan, 70428 Taiwan, Republic of China.
MATERIALS AND METHODS All the newborns studied were born to mothers with regular menstrual cycles. The gestational age was estimated from the first day of last normal menstrual period and confirmed by at least one second trimester prenatal sonographic examination. Only the appropriate-for-date newborns were included for study and cerebral sonographic examinations were taken within 3 days of life. Sonographic evaluations were performed through anterior fontanelle using Aloka SSD 630 sector scanner with 5.0 and 7.5 mHZ transducers. Images were taken in coronal, sagittal, parasagittal and tangential planes, and then photographed. Prospectively, the presence and maturation of the following selected sulci were recorded in each newborn: parieto-occipital fissure, calcarine fissure, cingulate sulcus, postrolandic sulcus, covering of insula, inferior temporal sulcus, insular sulci, and secondary and tertiary sulci from cingulate sulcus. Covering of insula was detected by 5.0 mHZ transducer in coronal ,dew at the plane of frontal horns oflateral ventricles. Inferior temporal sulcus and insular sulci were scanned by 5.0 mHZ transducer in parasagittal views. Postrolandic sulcus was found by 5.0 mHZ or 7.5 mHZ transducer in tangential views. Parietooccipital fissure and calcarine fissure, cingulate sulcus and its secondary and tertiary sulci were detected by 5.0 mHZ and 7.5 mHZ transducers respectively in sagittal views. Newborns with severe intraventricular hemorrhage and congenital malformation were excluded.
Table 1 Case numbers of sonographic visualization of the selected sulci at each gestational age group Vis ualized sulci
24-25 wks
26-27 wks
28-29 wks
30-31 wks
32-33 wks
34-35 wks
36 wks
Total
Parieto-occipital Calcarine Cingulate anterior whole Postrolandic Covering of insula Inferior temporal Secondary Insular partial whole Tertiary
8 6
12 12
12 12
11 11
7
6 6
4 4
60 58
2 0 0 0 0 0
10 1 5 0 0 0
12 10 12 3 2 0
11
7
10 10 3
7
6 6 6 6 6 6
4 4 4 4 4 4
52 39 45 30 29 20
0 0 0
0 0 0
0 0 0
0 0 0
4 0 0
6 4
4 4 2
14 8 3
Total
8
12
12
11
7
6
4
60
Fig 1 From a 24 weeks gestation neonate. A : Coronal view shows the widely· opened lateral sulcus (arrow). B: Sagittal view shows
the parieto·occipital fissure (arrow) and cingulate sulcus is absent.
7
11
7
11
7
7 7
Fig 2 Sagittal views. A : The calcarine fissure (arrow) begins to separate from the parieto-occipital fissure at 25 weeks gestation. B: The parieto-occipital fissure and calcarine rlSsure (arrow) are now Y-shaped in a 29 weeks neonate.
RESULTS Sixty infants were studied with a gestational age ranging from 24 to 36 wks. The sonographic findings of the sulci in each gestational age group are presented in Table 1. Lateral sulcus was widely opened in each case below 28 wks of gestation (Fig lA) and was closed with covering of the insula in all except one case above 29 wks. Parietooccipital fissure was already present in all cases, even by 24 wks (Fig 1B). Calcarine fissure branched and developed from parieto-occipital fissure in 6 of 8 cases at 24-25 wks (Fig 2A) and was present in all cases above 25 wks (Fig 2B). Postrolandic sulcus appeared in 5 of the 12 cases at 26-27 wks and was present in all cases above 27 wks (Fig 3A). Inferior temporal sulcus appeared in only 2 of the 12 cases at 28-29 wks, but could be demonstrated in all except one case by 30-31 wks (Fig 3B). Anterior
28 Brain & Development, Vol 13, No 1, 1991
Fig 3 A: In tangential view, the postrolandic sulcus (arrow) appears in a 28 weeks newborn. B: In parasagittal View, the inferior temporal sulcus (arrow) develops in a 30 weeks newborn.
Fig 4 Sagittal views. A: Anterior part of cingulate sulcus (arrow) develops in a 26 weeks neonate. B: Development of a whole straight cingulate sulcus (arrow) in a 28 weeks neonate.
Fig 5 Sagittal views. A :Notice the curvy cingulate sulcus (arrow) in a 30 weeks neonate. B: Secondary sulci (arrowhead) begin to bud from the cingulate sulcus in a 31 weeks neonate.
Fig 6 Sagittal views. A: More secondary sulci (arrow) develop from cingulate sulcus in a 34 weeks neonate. B : The tertiary sulci (arrowhead) from cingulate sulcus in a 36 weeks neonate.
Fig 7 Parasagittal views. A : Insular sulci (arrow) begin to develop in a 34 weeks neonate. B: Complete mature insular sulci (arrow) develop in a 36 weeks neonate.
cingulate sulcus (Fig 4A) first appeared in only 2 of the 8 cases at 24-25 wks, but was present in 10 of the 12 cases at 26-27 wks and in all the cases above 27 wks. The cingulate sulcus developed and extended posteriorly in only 1 of the 12 cases at 26-27 wks gestation, but the whole cingulate sulcus was present in 10 of the 12 cases at 28-29 wks (Fig 4B). Thereafter, the cingulate sulcus became curvy (Fig 5A) and secondary sulci began to branch from it in 3 of the 11 cases at 30-31 wks (Fig 5B). By 32-33 wks, secondary sulci from cingulate sulcus became present in all the cases. Further development and branching of the secondary sulci into tertiary sulci was noted in only 1 of the 6 cases at 34-35 wks and in 2 of the 4 cases at 36 wks (Figs 6A, 6B). Partial insular sulci appeared in 4 of the 7 cases at 32-33 wks and the whole insular sulci were present in 4 of the 6 cases at 34-35 wks while appearing in all cases at 36 wks (Figs 7 A, 7B). Anterior cingulate sulcus appeared in 52 cases and 50 (96%) of them were above 25 wks of gestation. Whole
cingulate sulcus was present in 39 cases and 38 (97%) of them were above 27 wks. There were 45 cases with postrolandic sulcus and 40 (89%) of them were above 27 wks. In 30 cases with covering of the insula, 27 (90%) of them were above 29 wks. In all, 29 cases had inferior temporal sulcus, 27 (93%) of them being above 29 wks. Partial insular sulci appeared in 14 cases all of which were above 31 wks. Secondary sulci were present in 20 cases and 17 (85%) of them were above 31 wks. Whole insular sulci were detected in 8 cases and all of them (100%) were above 33 wks. Tertiary sulci were present in 3 cases and 2 (67%) of them were above 35 wks.
DISCUSSION Developmental maturation is a better indicator of gestational age than simple anthropometric measurements [12]. The sequence of sulcal and gyral development of the brain in newborns at various gestational ages has been
Huang C-C: Sulcal development in prematurity 29
Table 2 Selected gestational age-dependent sulcal-gyral patterns based on cerebral sonographic examinations
24-25 weeks Prominent parieto-occipital fissure Early branching of calcarine fissure 26-27 weeks More maturation of calcarine fissure Appearance of anterior cingulate sulcus 28-29 weeks Development of whole cingulate sulcus Appearance of postrolandic sulcus Closing of lateral sulcus 30-31 weeks Covering of insula Bending and curvature of cingulate sulcus Appearance of inferior temporal sulcus Occasional secondary sulci budding from cingulate sulcus 32-33 weeks Branching of secondary sulci from cingulate sulcus Appearance of partial insular sulci 34-35 weeks Further development of insular sulci More maturation of secondary sulci Occasional tertiary sulci 36 weeks Development of tertiary sulci Maturation of insular sulci
studied, and is a reliable guide to the gestational age [11-13]. No descriptive sonographic data about sequential developments of different sulci has been published. In this study, by using proper transducers and scanning planes, several cerebral sulci were visualized at certain gestational ages. From the smooth contour of the immature brain to multiple convolutions that typify the mature brain, these cerebral sulci emerge in three distinctive gestational age groups: < 28 wks, 28-31 wks and > 31 wks. All calcarine fissure and most of the anterior part of cingulate sulcus begin to appear below 28 wks. At 28-31 wks all the whole cingulate sulcus and postrolandic sulcus, and most of the inferior temporal sulcus and covering of insula are ready to be observed. All of the insular sulci and tertiary sulci, and most of the secondary sulci from cingulate sulcus appear after 31 wks. Selected ultrasonic sulcal patterns in Table 2 represent the regional or hemispheric gyral maturation at various gestational ages. This sonographic sulcal maturation sequence relates with the EEG maturation patterns in preterm infants, which were described by Scher et al and Niedermeyer [13, 14J. The prominent occipital slow wave activity and vertex-central delta brush below 28 wks of gestation correspond to the early developments of occipital lobe (parieto-occipital and calcarine fissures) and
30 Brain & Development, Vol 13, No1, 1991
rolandic area (cingulate and postrolandic sulci) at this gestational age. By 28-31 wks the appearance of delta brush at temporal and occipital areas corresponds to the covering of insula and more development of temporal (inferior temporal sulcus) and occipital lobes (formation of cuneus). And after 31 wks decrease in periods of quiescence in EEG activity and a greater degree of interhemispheric synchrony may be associated with the development of secondary and tertiary sulci and more organization of cerebral cortex. Because of its central location and developmental symmetry, the imaging of the cingulate sulcus in preterm newborns had been used as a qualitative assessment of brain maturation [9]. And Worthern et al [10] were able to show retrospectively good correlation between three sonographic developmental stages of the cingulate sulcus with gestational parameters, such as birth weight, birth length and gestational age by date and by Dubowitz score. In addition to the cingulate sulcus, many other important sulci, as shown in this study, can be readily demonstrated by ultrasound and are also related to maturation. Serial imaging of several distinctive cerebral sulci can be more valuable than the cingulate sulcus alone in qualitative brain development, and the sonographic fmdings can supplement the clinical examination criteria for gestational age assessment [15]. Although the sequence of events demonstrated by ultrasound corresponded well to the sulcal development established from anatomic studies, the anatomic ages of appearance of cerebral sulci [11, 12] were earlier than the ages of appearance by ultrasound. The differences were about 8-9 wks in the age group below 28 wks, which included calcarine fissure and cingulate sulcus. There were only about 1-3 wks difference in the age group at 28-31 wks, which included postrolandic sulcus and inferior temporal sulcus. While there were no differences in age of appearance in the age group above 31 wks, which included secondary and tertiary branches from cingulate sulcus, and insular sulci. The younger the brain the larger the differences in time of sulcal appearance between neuroanatomy and sonography. Although anatomically evident in the immature brain, the shallow indentation of the sulcus could not be demonstrated by ultrasound. The immature sulcus gradually increased in depth over several weeks before well demarcated by ultrasound. The differences might be related to the degree of organization of the cerebral cortex which occurred from the sixth month of gestation to years after birth. The organization included: alignment orientation and layering of cortical neurons; dendritic and axonal ramification; establishment of synaptic contacts and glial proliferation and differentiation. This major development occurred especially in the third trimester which resulted in rapid increase in cortical thickness and brain surface areas [16,17]. By 24 wks of gestation the calcarine fissure and cingulate sulcus in the
less organized immature brain, which could be recognized by neuropathologists, were not deepened enough to be demonstrated by the 5.0 or 7.5 mHZ ultrasonic transducer. After 28 wks, in the more organized mature brain, the newly developed sulci could be readily demonstrated by ultrasound. In conclusion, ultrasound provides a noninvasive and useful method to clarify cortical sulcal structures. The sequential normal appearances and maturations of several fissures and sulci can be mapped by ultrasound and clinically be a morphologic indicator of gestational age. And it can be helpful in the evaluation of congenital abnormalities of sulcal formations, such as lissencephaly, microgyria and macrogyria. Prospective study of sonographic sulcal developments in appropriate-for-date and small-fordate newborns is undertaken to evaluate any temporal differences in maturation sequence. REFERENCES 1. Fisher AQ, Anderson JC, Shumen RM, Stinson W. Pediatric neurosonography: clinical, tomographic, and neuropathologic cOffelates. New York: Wiley Medical Publication, 1985:45106. 2. Mack LA, Alvord EC, Cyr DR, Aitken AGF, Richardson TE. The neonatal brain: nonnal appearances. In: Rumack CM, Johnson ML, eds. Perinatal and infant brain imaging. Chicago: Year Book Medical Publishers, 1984: 39-59. 3. Naidich TP, Gusnard DA, Yousefzadeh DK. Sonography of the internal capsule and basal ganglia in infants: 1. Coronal sections. AJNR 1985;6:909-17. 4. Naidich TP, Yousefzadeh DK, Gusnard DA. Sonographyof the normal neonatal head. Supratentorial structures: state of the art imaging. Neuroradiology 1986;28:408-27.
5. Yousefzadeh DK, Naidich TP. US anatomy of the posterior fossa in children: correlation with brain sections. Radiology 1985; 156: 353-61. 6. Sasaki M, Yoshioka K, Yanagisawa T, et al. Normal sonographic findings of the posterior cranial fossa in infants (in Japanese). No To Hattatsu (Tokyo) 1987; 19:363-70. 7. DiPietro MA, Brody BA, Teele RL. The calcar avis: demonstration with cranial US. Radiology 1985; 156: 363-4. 8. Vade A, Otto R. Cranial sonography of the occipital horns and gyral patterns in the occipital lobes. AJNR 1986; 7: 873-7. 9. Slagle TA, Michael 0, Gross SJ. Cingulate sulcus development in preterm infants. Pediatr Res 1989;26:598-602. 10. Worthen NJ, Gilbertson V, Lau C. Cortical sulcal development seen on sonography: relationship to gestational parameters. J Ultrasound Med 1986;5:153-6. 11. Dorovini-Zis K, Dolman CL. Gestational development of the brain. Arch Pathol Lab Med 1977; 101: 192-5. 12. Chi JG, Dooling EC, Gilles FH. Gyral development of the human brain. Ann Neurol 1977; 1:86-93. 13. Scher MS, Mamdouha AB. Estimation of gestational age by electrographic, clinical, and anatomical criteria. Pediatr NeuroI1987;3:256-62. 14. Niedermeyer E. Maturation of the EEG: Development of waking and sleep patterns. In: Niedermeyer E, Fernando LDS, eds. Electroencephalography: basic principles, clinical applications and related fields. Baltimore· Munich: Urban & Schwarzenberg, 1982: 107-30. 15. Murphy NP, Rennie J, Cooke RWI. Cranial ultrasound assessment of gestational age in low birthweight infants. Arch Dis Child 1988;64:569-72. 16. England MA. Normal development of the central nervous system. In: Levene MI, Bennett MJ, Punt J, eds. Fetal and neonatal neurology and neurosurgery. Edinburgh: Churchill Livingstone, 1988: 1-27. 17. Volpe 11. Neurology of the newborn. 2nd. Philadelphia: WB Saunders Company, 1987: 33-68.
Huang C-C: Sulcal development in prematurity 31