The Craniofacial Skeleton in Anencephalic Human Fetuses Ill. FACIAL SKELETON LOUIS METZNER, JAMES D. GAROL, HENRY W. FIELDS, JR. VINCENT G . KOKICH Department of Orthodontics, School Seattle, Washington 98195

of

AND

Dentistry, University of Washington,

ABSTRACT

A sample of 12 anencephalic fetuses with gestational ages ranging from 26 to 40 weeks and exhibiting varying degrees of severity of the dorsal cranial defect was compared to three normal fetuses of comparable gestational ages with regard to the morphology and positional relationships of the maxillofacial skeletal complex. Gross dissection, alizarin red S staining, radiographs, cephalometric tracings, and histologic techniques were utilized. It was found that some facial bones were severely affected in morphology, size, spatial and angular relationships. The manner in which these were altered suggests that their morphogenesis is an adaptation to the primary defect of the neurocranium.

Few studies on anencephaly include a cephalometric analysis of the facial skeleton. However, this congenital defect provides a good opportunity to examine the degree to which the facial skeleton is influenced by a specific, severe disturbance in cranial development. Articles preceding this one have already described the cranial floor (Fields et al., '78) and calvarium (Garol et al., '78). The reader should refer to these for descriptions of the primary defects in anencephaly. MATERIALS AND METHODS

A sample of 12 anencephalic fetuses with gestational ages ranging from 26 to 40 weeks (table 2) was subdivided according to the extent of the dorsal cranial defect as follows: meroacrania, a cranial defect not involving the foramen magnum; holoacrania, a cranial defect involving foramen magnum; and holoacrania with rachischisis, a cranial defect involving the foramen magnum and extending to the vertebral column. Various techniques were utilized including dissection, alizarin red S preparation of whole and half heads, impregnation of halved heads with 0.5% silver nitrate for radiographs, and histologic processing. For control specimens three normal fetuses of comparable gestational ages were processed by the same techniques. For a complete description of the sample and processing techniques see the initial article in the series (Fields et al., '78). TERATOLOGY (1978) 17: 76-82.

A plane Cartesian co-ordinate system was constructed on tracings made from lateral radiographs of each anencephalic specimen (fig. lc). The X axis was represented by the palatal plane and the Y axis by a perpendicular line through midpoint sella (S). Mandibular condyles lying anterior to the Y axis were measured as positive abscissae and condyles posterior to the Y axis were measured as negative abscissae. These measurements are represented by A in figure lc and listed in table 1. Mandibular length was defined as a straight line measurement from condylion (C) to gnathion (Gn) (fig. lc). Maxillary length (MxL) was measured from anterior nasal spine (ANSI to posterior nasal spine (PNS). The ratio of mandibular length (MnL) to maxillary length (MnL/MxL) was computed for each of the anencephalic specimens and for the normal controls (table 1).The shape of the mandible was determined by measuring the body length (B) and the ramus length (R) and expressing these as the ratio B/R (fig. 2a and table 1). The gonial angle, the inside angle between line R and B, was measured (fig. 2a and table l),and the symphyseal height of each mandible was expressed as a ratio to the mandibular length (MnL/Symph) (table 1). The anteroposterior relationship of the mandible to maxilla was determined by constructing an arc of radius C-Gn with center a t Received June I, '11. Accepted Oct. 18, '11.

75

76

L. METZNER, J. D. GAROL, H. W. FIELDS, JR., AND V. G. KOKICH Abbreviations A, Anteroposterior position of the mandibular condyle ANS, Anterior nasal spine B, Body length of the mandible Ba, Basion C, Condylion F, Frontal bone Gn, Gnathion

Mn, Mandible Mx, Maxilla N, Nasion P, Relative prognathism of the mandible PNS, Posterior nasal spine R, Ramus length of mandible S, Sella turcica Z, Zygomatic bone

a Fig. 1a.b Tracings made from lateral head films supplemented by additional information derived from alizarin stained preparations of the same specimens, (a) normal (b) anencephalic (holoacrania).A comparison of figures a and b shows that in the anencephalic the frontal and zygomatic bones are severly affected with respect to morphology, size, and spatial orientation. c A midline tracing of a representative anencephalic specimen with a plane Cartesian co-ordinate system with X axis through palatal plane and Y axis, a perpendicular line through sella turcica. The mandible is related to the maxilla by the projected arc of radius C-Gn and the relative prognathism is measured by the horizontal distance “P.” The mean for this measurement indicates that the mandible is prognathic in anencephalics. The position of the mandibular condyle in relation to sella turcica is described by the horizontal distance A. In anencephalics this greater distance indicates that a more forward position of the mandible may contribute to the degree of prognathism.

C (fig. l c ) and measuring the horizontal distance (P) between the most anteroinferior point of the maxillary alveolus and a point on the arc parallel to palatal plane. A negative measurement indicated that the arc extended posterior to the maxillary point and a positive measurement indicated that it was located anteriorly. Table 2 arranges the sample into comparable age levels according to foot length (FL). The absolute linear sizes of the maxillae and

mandibles are listed as well as their ratios. The linear distance from sella (S) to PNS is also recorded. From lateral head radiographs, cephalometric tracings were made as illustrated in figure 2a. The tangents to the nasal bone and frontal bone were drawn to meet at nasion (N). The cranial base was described by lines connecting S to N (SN) and S to basion (Ba) (SBa). Since the orbit was abnormally shaped and porion difficult to identify, the anthropo-

77

FACIAL SKELETON IN ANENCEPHALY

’\

Fig. 2a Cephalometric polygon derived from mean measurements of normal controls. b-d Superimpositionof polygons on palatal plane with registration on anterior nasal spine. Solid lines represent means for normal specimens and dashed lines represent means for meroacrania (b), holoacrania (c), and holoacrania with rachischisis (d). Note the relative positional and angular changes of the cranial base and facial bones between normals and abnormals.

metric reference plane of Frankfort was not used. Instead the palatal plane, as identified in lateral radiographs, was utilized. Palatal plane was represented by the line ANS-PNS. The mandibular morphology was collectively described as the ratio of ramus to body length in addition to the gonial angle measurement. The following cephalometric angles were measured: the angle formed by the anterior extensions of the lines tangent to nasal bone and palatal plane (N-PP); the angle between the tangents to the frontal bone and nasal bone (F-N); the angle between the frontal bone tangent and SN line (F-SN);the ventral angle between SN and SBa (SXBa); and lastly the gonial angle. The mean (X)values and standard deviations (9) for these cephalometric

measurements are listed in table 1. Ninetyeight percent confidence intervals for means of all measurements were calculated (table 1). The arithmetic means of these measurements were used to construct polygons which graphically illustrate the differences between the maxillofacial morphology of the anencephalic and normal fetuses (figs. 2b-d). These polygons were superimposed on the palatal plane and registered so that the anterior nasal spines coincided. RESULTS

Since the sample consisted of specimens with varying degrees of severity of the dorsal cranial defect, it was subdivided accordingly: five anencephalic fetuses with meroacrania,

2.47 1.00

-3.8 -4.0

Pmm5

19

3.60

50 5.00 122.3 14.20 118.3 10.40 143.3 5.80

4.5-33.5 29.7-70.1 65.2-179.4 76.4-160.2 120.1-166.5

1.32-1.56

-13.7-6.1 -8.2-0.2

2.73-4.83

90-167.8 1.03-3.21

(Lc-UC) '5

7.9

162 -2.4 108

26 30.8

1.76

6.1 13.3

3.32 3.90 8.7

0.08

4.9 3.5

-0.4 7.8

0.40

0.38

3.46

142 2.05

s

147.4-176.6 - 12.6-7.8 85.7-130.3

20.4-31.6 24.3-37.3

1.63-1.89

-8.25-8.18 1.93-13.7

2.79-4.13

128.7-155.3 1.41-2.69

(Lc-UC)

Memacrania n = 5 x

'

I

Gonial angle. Body length of mandiblehamus length of mandible. Height of mandibular symphysis expressed as a ratio to MnL. ' Distance of condyle from Y axis (fig. 1). Relative prognathism of mandible (fig. 1). Mandibular length = C-Gn (fig. 1). Maxillary length = ANS-PNS (fig. 2). Linear distance from sella to posterior nasal spine.

N-S-Ba""

F-SNO

F-NO"

N-PP"

S-PNSmma

MnL MxL

SPP Amm'

0.03

0.26

3.78

MnL -

1.44

9.64 0.27

129.0 2.12

B/R 2

GO I

81'

Normal n = 3

X"

-

3.2 4.0 0.6 10.8

1.15

0.03

3.2 1.3

0.41

6.9 0.40

8

~~

17.7-26.7 13.8-39.6 182.9-215.1 -2.1-2.7 60.2-147.2

1.61-1.85

0.6-11.0

-8.2-17.8

1.60-3.63

120.1-175.8 0.1-3.36

(Lc-UC)

125

192 10

27.8 32.3

1.73

1.5 3.9

3.57

143.8 2.07

K

7.5 7.7 20.1

4.5 9.3

0.06

3.5 0.63

0.53

0.44

10.2

s

79.4-170.6

- 7.5-27.5

175-209

17.5-37.97 11.2-53.4

1.59-1.87

-6.5-9.5 2.5-5.3

2.37-4.77

120.6-167.0 1.07-3.07

(Lc-UCI

Holmcrania with rachiwhisis n = 4

181.3 2.4 112.6

25.1 30.3

1.75

1.5 6.0

3.54

144.1 2.0

x

-

18.6 7.9 16.9

3.6 6.0

0.06

4.3 2.8

0.41

8.1 0.49

s

22.3-27.9 25.6-34.0 166.7-195.9 -3.8-8.6 99.3-125.9

1.70-1.80

3.8-8.2

- 1.9-4.9

3.22-3.85

EX

x

0

137.7-150.5 4 1.62-2.38 P

(Lc-UC)

Total abnormals n = 12

Angle between extension of nasal bone to palatal plane. Angle between tangent to frontal bone and nasal bone. " Angle between frontal bone and sella to nasion plane. l 2 Cranial base angle-inner angle between sella-naaion and sella-basion. l 3 Mean. I' Standard deviation of sample. Is Lower confidence limit-upper confidence limit a t 98% confidence level. lo

22.3 26.7 199 0.3 103.7

1.73

4.7 5.8

3.62

148 1.76

x

Holmcrania n = 3

Cephalometric comparisons between normal controls, meroacrania, holoacrania, holoacrania with rachischisis and total abnormals

TABLE 1

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FACIAL SKELETON IN ANENCEPHALY TABLE 2

Cephalometric comparisons between normal and anencephalic specimens in three age clusters baaed on foot length FLmm'

-

xa

Normal Abnormal Normal Abnormal Normal Abnormal

n=ls

n=6 n=l n=2 n=l n=4

ANS-PNS mm '

8'

58 58.323.7 77 75.520.71 85 87.3+.2.2

x

C-Gn mm

x

s

22 22.72 1.6 32 27.0k 0 31 29.8e 0.5

s

31 39.2k 2.5 41 47.02 1.4 45 52.8-t 2.5

MnL/MxL'

S - P N S mm -

T t s

1.41 1.742 0.05 1.47 1.73520.05 1.45 1.782 0.09

x

s

15 22.32 1.0 20 26.5k 4.9 22 28.5k 2.4

' Foot length. Maxillary length = anterior nasal spine to posterior nasal spine. Mandibular length = condylion to gnathion. ' Ratio of mandibular length to maxillary length. Linear distance from sefia to posterior nasalspine. Mean. ' Standard deviation of sample. Number of sample.

three with holoacrania and four with holoacrania and rachischisis. The interrelationships of the bones of the facial skeleton can be described with reference to the positions of the sutural articulations. The frontonasal suture was generally in a more posterior position in the abnormal with reference to the most anterior part of the zygomaticomaxillary suture (compare figs. l a and lb). In the normals it was either in the same plane or located more anteriorly. The nasal bone was angularly affected with an angulation of 30.6 26' to PP in anencephalic fetuses. There was no significant difference with respect to the degree of severity of the defect. The nasal bone in normals was 50 f 5.0' to PP. The frontal bone is severely affected in anencephaly. In the normal fetus the frontal bone forms an angle of 122.3 f 14.2' to the nasal bone. There was a marked increase in this angulation in the anencephalic since the frontal bone has no eminence. In the anencephalics with meroacrania the glabellar portion of the frontal bone formed an angle of 162 8.7" with the nasal bone and then almost immediately lay down flat with an angle of 210 f 9.8" to the naeal bone (fig. 2b). Specimens exhibiting holoacrania and holoacrania with rachischisis showed angles of 199 f 4' and 192 f 7.5" respectively, for the glabellar portion of the frontal bone, and in both groups the frontal eminence was absent. The superior orbital rim was directed posterolaterally with a lateral obliquity which makes a n acute angle with the sagittal plane whereas it normally forms a right angle. In most specimens no orbital plate of the frontal

*

bone could be identified, but when it existed, it extended only a short distance laterally from the midline (Fields et al., '78). In anencephaly the bony roof of the eye was incomplete due to the posterolateral inclination of the frontal bone (fig. lb). The posterior portion of the eye was roofed by that portion of the frontal bone which normally constituted the frontal eminence and not by the orbital plate of the frontal bone. In the anencephalic fetus, the superior orbital rim was curved with an anterior concavity while in the normals there was an anterior convexity. Morphologically, the zygomatic bone was the most affected facial bone. In the lateral view it generally had a rhomboid shape (fig. shape. lb), while in the normal it had a "I" The frontal process of the zygomatic bone had a posterosuperior inclination while in the normal it was directed superiorly. Therefore, the frontozygomatic suture was located more posteriorly than normal (figs. la,b). The temporal process of the zygomatic bone was parallel to the palatal plane as in the normal fetus. Consequently the angle between the frontal and the temporal processes of the zygomatic bone was acute (approximately 45'1, while in the normal it was approximately a right angle. In the lateral view the frontozygomatic suture was located posterior to the zygomaticotemporal suture in the anencephalic fetuses. In addition, the zygomaticotemporal suture was generally closer to the body of the zygoma due to a less well-developed temporal process of the zygomatic bone. The suture extended from anterosuperior to posteroinferior as in the normal fetus, but i t had a "C" shape with the concavity of the "C" posteriorly. The normal zygo-

80

L. METZNER, J. D. GAROL, H. W. FIELDS, JR., AND V. G. KOKICH

maticotemporal suture extended in a straight line from anterosuperior to posteroinferior. The lateral rim of the orbit in the anencephalic fetus formed a 180" angle between the frontal process of the zygomatic bone and the lateral portion of the inferior orbital rim (fig. lb). Normally this relationship was nearly a right angle. The anencephalic zygomaticomaxillary suture was in a normal position and had a normal direction but was slightly longer than normal. The morphology and spatial relationship of the maxilla was similar to that seen normally in the lateral view. The palatomaxillary suture and the horizontal plate of the palatine bone appeared normal in sagittal histologic sections. The vomer was directed superiorly at its cranial end as it approximated the body of the sphenoid in the anencephalics. The mandibles in the anencephalics were prognathic without exception with the mean 6.0 f 2.8 mm (fig. lc and table of P being 11, while the normals were retrognathic without exception a t - 4.0 ? 1.0 mm. The relationship between the most posterior portion of the mandibular condyle and sella was measured (A in fig. l c ) and is recorded in table l. The normal condyles were located posterior to sella with a mean of - 3.8 f 2.5 mm and the abnormals were anterior to sella a t + 1.5 +4.3mm. There were some differences with respect to the three subdivisions: meroacrania averaged - 0.4 f 4.9 mm, holoacrania 4.7 & 3.2 mm, and holoacrania with rachischisis + 1.5 f 3.5mm. The relationship of mandibular length to maxillary length (MnL/MxL) was 1.44 f 0.03 for normals and 1.75 f 0.06 for the anencephalics. The relative shape of the mandible was documented by comparing the gonial angle, the ratio of body length to ramus length, and the ratio of mandibular length to symphyseal height, respectively, in both normals and anencephalics. The gonial angle was slightly more obtuse in the anencephalic mandibles (144f 8.1")than in the normal mandible (129 5 9.6'). The ratio of body length to ramus length (B/R) was 2.12+- 0.27 and 1.99f 0.4, and the ratio of mandibular length to synphyseal height was 3.54 2 0.41 and 3.78 f 0.26for abnormals and normals respectively. The cranial base has been described in the foregoing article by Fields e t al. ('78). Its angular relationship is included here to relate the midline facial structures to the cranial base and to complete the polygons described in

+

+

figures 2b, 2c, and 2d. The absolute linear distance from sella to posterior nasal spine was 19 f 3.6 mm for the normals and 25.1 f 3.6 mm for the anencephalics. The cranial base angle (NSBa) was 143 f 5.8",108 f 13.3', 103.7 f 1l0, and 125 f 20.1' for the normals, meroacrania, holoacrania, and holoacrania with rachischisis, respectively. DISCUSSION

The face in anencephaly has been variously described in the literature. To some investigators (Keen, '62) all structures inferior to the orbits appeared normal. Others have described various anomalies of the face such as broadbased nose (Ballantyne, '05; Lemire et al., '721,palatal fissures and cleftings (Lemire et al., '72),prognathic mandibles (Ballantyne, '05;Abd-El-Malek, '57;Lemire et al., '721,etc. Few studies on anencephaly, however, have described the interrelationships of the facial skeleton through the use of a comprehensive technique. In the present study a cephalometric approach supplemented by various other morphologic techniques was used to examine the relationships of the facial bones and to compare these with normal controls. Andersen et al. ('67) found a relationship between the extent of hypoplasia of the optic ganglion, optic disc, and optic nerve and the degree of severity of the anencephalic fetuses. This was postulated as being secondary to the cerebral malformations. These investigators have also shown that the eyes were grossly of normal shape and size regardless of the degree of severity. The stimulus of the eye as a functional matrix in the development of the orbit should then be unaffected. Our findings have shown that the orbit is much affected. Due to the lateral obliquity of the orbit and the posterior angulation of the frontal process of the zygomatic bone, the eye remains largely uncovered by a bony roof. The extent of the covering that was present was of a heavier plate of bone than in normals. This heavier plate also exhibited a midline metopic suture and articulated laterally with the zygomatic bone. In the specimens with meroacrania this portion of the frontal bone articulated with the right and left parietal bones. I t is interesting that the portion of the frontal bone normally forming the glabella and eminence contribute to the structure of the orbital roof in the abnormal; and therefore the orbital plate of the frontal bone is absent. Van Limborgh ('70) feels that the primordia of head structures,

FACIAL SKELETON IN ANENCEPHALY

i.e., eyes, exert strong effects on the development of the skull, and that adjacent structures can also exert powerful morphogenetic influences. Is the shape of the malformed orbit in anencephaly an expression of the contribution of the eye primordium only since it is normal; and is the difference between the shape of the orbit in anencephaly and normal equal to the morphogenetic influence of a normally developing brain? The zygomatic bone was severely and similarly affected regardless of the degree of severity of anencephaly. The posterosuperior angulation of the frontal process and the relative position of the frontozygomatic suture suggests an adaptation to the severely affected frontal bone. The failure of normal development of the cerebrum may have caused the frontal bone to develop toward a horizontal and lateral position and the angular changes seen in the zygomatic bone would be consistent with this maldevelopment. The zygomaticomaxillary suture was in a normal position and relationship with the adjacent skeletal structures. In lateral view the maxilla appeared normal. The vomer (Fields e t al., '78) angulated superiorly as it made its articulation with the body of the sphenoid, however, its articulation with the maxilla was normal. There appears to be a gradient; i.e., as the distance from the defect increases, the relative changes from normal decrease. The vomer and zygomatic bone, which can be considered as struts connecting the facial skeleton to the cranial base and cranial vault respectively, were more affected than the maxilla. All anencephalics studied exhibited prognathism of the mandible relative to the maxilla. Since the ratio of mandibular length to maxillary length was significantly different between normals and abnormals, a relative prognathism could be due to three possibilities: (1) in anecephalics the mandibles may be larger than normal; (2) the maxilla may be smaller than normal; or (3) there may be a combination of both of the above. Table 2 shows absolute values grouped in comparable gestational age clusters for both normals and abnormals, and suggests that in anencephaly the mandible is larger and the maxilla is more nearly normal in size. A contributing factor in the degree of prognathism was the more anterior relationship of the mandible in anencephalics. The forward, inward and downward rotation of the petrous

81

portion of the temporal bone, as described in the foregoing article by Fields e t al. ('781, may explain the more anterior position of the glenoid fossa and the mandibular condyle. This forward rotation was not as pronounced in the specimens with meroacrania, which is consistent with the measurements found by this analysis. Therefore, the relative prognathism may be a manifestation of the initial defect transmitted through the spatial alteration of the intervening temporal bone. The mandibular symphyseal heights appeared larger in the anencephalics than in the normals. Although in some fetuses it was actually larger than comparably aged normals it was found that when related to mandibular length as a ratio, the confidence intervals demonstrated complete overlap. Therefore, the relative symphyseal heights were not different than in the normal controls, but since the mandibles were larger in the anencephalics the symphyseal heights were also correspondingly larger. The cranial base angulation in anencephaly has an interesting association with the facial skeleton when compared to normals. This relationship is described by a linear measurement from S to PNS. The polygons in figures 2b, 2c, and 2d show this distance to be increased in the abnormals. This increased dimension between cranial base and facial skeleton may be an adaptive response to the lack of normal cranial base flattening, thereby maintaining an airway space. Marin-Padilla ('70) states that the facial bones depict only anomalous positions (slight posterior rotations) and reductions of their transverse diameters. In the present study the facial bones in anencephaly occupy anomalous positions as an adaptation to the more severely affected chondrocranium and neurocranium but their anomalous shapes are adaptive as well. The temporal bone influences the forward position of the mandible in relation to the maxilla, while the frontal bone influences not only the position of the zygomatic bone but also its anomalous shape. The location of the sphenoid bone to the palatal plane influences the size and shape of the vomer. The anencephalic maxillofacial complex has been studied in detail. In contrast to previous reports, it has been clearly demonstrated that the morphology, size, and spatial relationships of nearly all facial bones and their fibrous articulations have been morphogenetically altered. The results of the present investigation

82

L. METZNER, J. D. GAROL, H. W. FIELDS, JR., AND V. G. KOKICH

indicate that a primary defect in neurocranial development initiates adaptive secondary alterations in the remaining contiguous skeletal components of the craniofacial complex. ACKNOWLEDGMENTS

Grateful acknowledgments are due to Doctor Benjamin C. Moffett for guidance and for assistance in the preparation of the manuscript; Doctors Ronald J. Lemire and J. Bruce Beckwith for making available a large sample of well documented specimens; and to Mrs. Livia Molnar for her technical assistance. This research was supported by Public Health Service Research Grant DE 02931 and the University of Washington Orthodontic Memorial Fund. LITERATURE CITED AM-El-Malek,S. 1957 The anencephalic skull andavascular theory of causation. Egyptian Med. Assw., 40: 216-224.

Andersen, S. R., F. Bro-Rasmussen and I. Tygstrup 1967 Anencephaly related to ocular development and malformation. Am. J. of Ophth., 64: 559-566. Ballantyne. J. W. 1905 Manual of Antenatal Pathology and Hygiene: the Embryo. William Wood and Co., New York, pp. 332-351. Fields, H. W., Jr., L. Metzner, J. D. Garol and V. G. Kokich 1978 The craniofacial skeleton in anencephalic human fetuses. I. Cranial floor. Teratology, 17: 57.66. Garol, J. D.. H. W.Fields, Jr., L. Metzner and V. Kokich 1978 The craniofacial skeleton in anencephalic human fetuses. 11. Calvarium. Teratology, 17: 67-74. Keen, J. A. 1962 The morphology of the skull in human anencephalic monsters. S . Afr. Med. J., 8: 1-9. Lemire, R. J., J . B. Beckwith and T. H. Shepard 1972 Iniencephaly and anencephaly with spinal retroflexion. A comparative study of eight human specimens. Teratology, 6: 27-36.

Limborgh, J. van 1970 A new view on the control of morphogenesis of the skull. Acta Morphol. Need.-Scand., 8: 143-160.

Marin-Padilla, M. 1965 Study of the skull in human cranioschisis. Acta anat., 62: 1-20. 1966 Mesodermal alterations induced by hypervitaminosis A. J. Embryol. Exp. Morph., 15: 261-269. 1970 Morphogenesis of anencephaly and related malformations. Current Topics in Path., 51: 145-174.

The craniofacial skeleton in anencephalic human fetuses. III. Facial skeleton.

The Craniofacial Skeleton in Anencephalic Human Fetuses Ill. FACIAL SKELETON LOUIS METZNER, JAMES D. GAROL, HENRY W. FIELDS, JR. VINCENT G . KOKICH De...
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