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An Osteometric Evaluation of the Foramen Spinosum and Venosum/ Una Evaluacion Osteometrica de los Foramenes Espinoso y Venoso.

INTRODUCTION

The greater wing of the sphenoid bone is marked by numerous foramina which transmit vital neural and vascular structures (Dogan et al., 2014). These foramina are characteristically situated along the medial aspect of the floor of the middle cranial fossa. Many variants have been described in the anatomic and radiologic literature which is not only important to understand the complex regional neurovascular anatomy but also to distinguish the normal from the potentially abnormal structures (Curtin et al., 1984; Pandolfa et al., 1987).

One such foramen is the Foramen Spinosum (FS) which is located in close proximity postero-lateral to Foramen ovale (FO) and transmits the middle meningeal vessels, the meningeal branch of mandibular nerve and the nervous spinosus (Dogan et al.; Srimani et al., 2014). The transmission of these neurovascular structures allows for communication between the middle cranial and the infratemporal fossae (Kwathai et al., 2012; Srimani et al.).

In addition, the foramen venosum (Foramen of Vesalius) (FV) is occasionally present within the greater wing of the sphenoid bone (Wood-Jones, 1931; Chaisuksunt et al., 2011). The FV is also known as the sphenoid emissary foramen, foramen venosum and canaliculus sphenoidalis and usually opens into the scaphoid fossa infero-laterally (Bergman et al., 2006; Shaik et al., 2012). Although the relatively small FV is unique to humans due to its inconsistency, it is generally situated antero-medial to the FO (Wood-Jones; Chaisuksunt et al.; Shaik et al.). The name of FV is derived from the structure it transmits intracranially, the small emissary vein or " Vein of Vesalius", through which the pterygoid plexus and cavernous sinus communicate in the parapharyngeal space (Henderson, 1966; Gupta et al., 2005; Chaisuksunt et al.; Shaik et al.). Henderson stated that occasionally this emissary vein may be a venous sinus which exits through the anterior aspect of FO when FV is absent; thus non-visualization is a known anatomic variation. Additionally, Fisher (1913) reported entry of the meningeal branch of ascending pharyngeal artery into FV; while Lang (1983) and Gupta et al. described a small nerve, the "nervoulus sphenoidalis lateralis", passing through this foramen to the cavernous sinus.

As the FO is regarded as an easily accessible portal to the mandibular division of the trigeminal nerve during percutaneous trigeminal rhizotomy and neural blockade anesthesia, the proximity of the FS to the FO may render the middle meningeal vessels vulnerable to iatrogenic injury, thereby increasing the risk of extradural hematomas (Shaik et al.; Srimani et al.). Since the emissary vein connects the intracranial venous sinuses with the extracranial veins, the FV presents a passage along which a diseased thrombus may pass from the exterior into the interior of the cranium (Gupta et al.; Chaisuksunt et al.; Shaik et al.). The FV is also considered to be one of the most pathologically affected foramina as tumors of nasopharyngeal origin often tend to invade the middle portion of the skull base (Lanzieri et al., 1988).

In view of the surgical and anesthetic explorative maneuvers involving the skull-base, an accurate osteometric evaluation of the FS and FV including their relative incidences, shapes, morphometric details, respective relations to the FO and/or presence of any anomalies bears much significance. Therefore, this study aimed to document the morphology and morphometry of the FS and FV.

MATERIAL AND METHOD

Osteometric investigations were performed on 100 randomly selected dry human skulls which were obtained from the existing osteological bank at the Department of Clinical Anatomy, University of KwaZulu-Natal. Metric as well as non-metric parameters were analyzed and a database was created (n = 200). A total of 213 foramina were identified (106 right, 107 left). Measurements were recorded with a digital caliper (Wilson Wolpert 110-15DAB, Netherlands). The shape, mean width, distance of FV and its relation to FO were calculated as a percentage of the total number of foramina on each side. Statistical analysis was conducted using a paired T-Test and significant parameters were values whose reality level was [less than or equal to] 0.05. These results were compared with those available in the literature.

RESULTS

All foramina were described as separate entities. There was no confluence of FS with FV or FO or vice versa. No statistically significant differences between sides were observed.

Morphological features of the FS and FV were recorded as follows:

i) Incidence (n= 200): single (FS: 95%; FV: 5%); duplicate (FS: 2.5%; FV: 0%); triplicate (FS: 0.5%; FV: 0%); absent (FS: 2%; FV: 0%) (Figs. 1-4, Table I);

ii) Shape (n= 213): oval (FS: 43.5%; FV: 4.5%); round (FS: 58%; FV: 0.5%) (Table I);

iii) Relation to FO: postero-lateral (FS: 93%; FV: 0%); posterior (FS: 1.9%; FV: 0%); postero-medial (FS: 0.5%; FV: 0%); anterior (FS: 0%; FV: 0.5%); antero-medial (FS: 0%; FV: 4.5%) (Table I).

Mean morphometric parameters pertaining to the FS and FV and their relation to FO were documented:

i) Internal diameter (FS: 2.53+0.76 mm; FV: 1.93 [+ or -] 0.46 mm) (Table I);

ii) External diameter (FS: 2.50+0.74 mm; FV: 2.81 [+ or -] 1.53 mm) (Table I);

iii) Distance to FO (FS: 3.45+1.29 mm; FV: 2.63 [+ or -] 1.24 mm) (Table I).

DISCUSSION

The FS is typically located postero-lateral to FO (93% in this study), along the posteromedial aspect of the greater wing of the sphenoid bone and is usually round or oval in shape (Ginsberg et al, 1994). This study also describes posterior and postero-medial locations of the FS in relation to the FO (Table I).

The FS was absent in 2% of cases in our study (Tables I and II). It is postulated that in the absence of a FS, the middle meningeal artery enters the cranial cavity through the FO (Reymond et al., 2005). Ginsberg et al. provide an additional explanation of the absence of a FS in the case of an aberrant middle meningeal artery which arises from the stapedial branch of the internal carotid artery or the ophthalmic artery (Lindblom, 1936; Paullus, 1977). Fisher (1914) and Greig (1929) have explained the embryologic development of the middle meningeal artery. The stapedial artery originates as a dorsal branch of the second aortic arch and is part of the carotid arterial system (Fisher; Greig). In the 15mm embryo, the infraorbital and mandibular branches of the stapedial artery fuse with the external carotid artery and are destined to become the internal maxillary artery (Fisher; Greig). The main trunk of the stapedial artery atrophies and its origin from the internal carotid disappears (Fisher; Greig). The usual distribution of the stapedial artery is then replaced by branches from the external carotid artery (Fisher; Greig). If the connection with the external carotid artery fails to occur, the superior or supraorbital branch of the ophthalmic artery becomes the middle meningeal artery (Fisher; Greig). In this case the middle meningeal artery enters the skull through the superior orbital fissure. Lindblom reported this variation in 0.4% of cases. However, the stapedial artery may also persist. This vessel has also been associated with an aberrant internal carotid artery. The persistent stapedial artery courses through the tympanic cavity, between the crura of the stapes and enters the facial canal distal to the geniculate ganglion. It enters the middle cranial fossa by the facial hiatus and becomes the middle meningeal artery. In both of these cases of a variant middle meningeal artery, the FS will be tiny or absent (Ginsberg et al.).

In this study single FS appeared in 95% of cases which corroborated the findings of previous studies (Table II). Duplicate FS were observed in 2.5% of cases vs. 0.8% recorded by Ginsberg et al. (Table II). Duplication can be explained by early division of the middle meningeal artery into a posterior and anterior division resulting in a duplicate FS (Lindblom; Sondheimer, 1971; Reymond et al.). The literature reviewed remains silent on the course of the meningeal branch of the mandibular nerve in the absence or duplication of a FS.

FS was observed at a distance of 3.45+1.29 mm to FO which compared favorably to that reported by Paullus et al. and Aslan et al. (1998) (Table III).

The internal and external diameters of FS varied from side to side but did not usually exceed 3 mm (Table I). Table IV describes diameters of FS culled from the literature. According to Sondheimer, in the instance of the diameter exceeding 5 mm, the patient should be immediately evaluated for middle meningeal artery abnormality.

The FV is regarded as a small opening in the medial aspect of the greater wing of the sphenoid bone antero-medial to FO. In this study FV was located anterior (0.5%) or anteromedial (4.5%) to FO (Table I). Single (5%) and duplicate (0.5%) FV were observed which correlated with the wide range in incidence of this foramen reported in the literature reviewed (0.6-80%) (Table II). In the absence of the FV, the respective emissary vein leaves the skull through the FO (Henderson). It is also postulated that the emissary vein is a dural venous sinus rather than a vein (Henderson). In addition, Lang and Gupta et al. described a small nerve, the nervoulus sphenoidalis lateralis, which may also pass through the FV into the cavernous sinus.

The FV was identified to be situated 2.63 [+ or -] 1.24 mm from the FO, a finding which may be regarded as a unique reference measurement as it has not been reported in previous literature. The internal and external diameters were found to be 1.93 [+ or -] 0.46 mm and 2.81 [+ or -] 1.53 mm, respectively, which were markedly increased in comparison with the values recorded in earlier studies (Table IV). Ozer & Govsa (2014) explained that the FV presenting with a diameter of less than 0.5 mm are most reliable and safe during percutaneous practice as apertures of greater than 0.5 mm pose a major risk on the adjacent FO.

Many authors have claimed that the variations observed in skull-based foramina may be a result of the evolutionary process such that the incidence of a specific previously-observed variant may later be considered to be the variant-normal or constant of a particular geographical population and/or ethnic group (Sharma & Garud, 2011).

CONCLUSION

In this study the evaluation of the FS and FV and their respective relationships to FO may provide a reliable osteometric standardization of the alisphenoid structures in the middle cranial fossa. The recognition and knowledge of the normal and abnormal foramen anatomy may assist in misinterpretation during various imaging procedures. As a connecting passage, the significance of the FV lies in thorough surgical intervention to prevent puncture of the trigeminal cave and cavernous sinus as well as subsequent hemorrhage of the temporal lobe. Therefore, the above information may serve as a guideline to surgeons, radiologists and anesthetists.

REFERENCES

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Berlis, A.; Putz, R. & Schumacher, M. Direct and CT measurements of canals and foramina of the skull base. Br J. Radiol., 65(776): 653-61, 1992.

Chaisuksunt, V.; Kwathai, L.; Namonta, K.; Rungruang, T.; Apinhasmit, W. & Chompoopong, S. Occurrence of the foramen of Vesalius and its morphometry relevant to clinical consideration. ScientficWorld Journal, 2012: 817454, 2012.

Curtin, H. D.; Williams, R. & Johnson, J. CT of perineural tumor extension: pterygopalatine fossa. AJNR Am. J. Roentgenol., 144(1):163-9, 1985.

Dogan, N. U.; Fazhogullari, Z.; Uysal, I. I.; Seker, M. & Karabulut, A. K. Anatomical examination of the foramens of the middle cranial fossa. Int. J. Morphol., 32(1):43-8, 2014.

Fisher, A. G. A Case of Complete Absence of both Internal Carotid Arteries, with a Preliminary Note on the Developmental History ofthe Stapedial Artery. J. Anat.Physiol., 48(Pt. 1):37-46, 1913.

Ginsberg, L. E.; Pruett, S. W.; Chen, M. Y & Elster, A. D. Skull-base foramina of the middle cranial fossa: reassessment of normal variation with high-resolution CT. AJNR Am. J. Roentgenol, 15(2):283-91, 1994.

Greig, D. M. Congenital anomalies ofthe foramen spinosum. Edinb. Med. J, 36:363-71, 1929.

Gupta, N.; Ray, B. & Ghosh, S. Anatomic characteristics of foramen vesalius. Kathmandu Univ. Med. J. (KUMJ), 3(2):155-8, 2005.

Henderson, W. R. A note on the relationship of the human maxillary nerve to the cavernous sinus and to an emissary sinus passing through the foramen ovale. J. Anat., 100(Pt. 41:905-8, 1966.

Kim, D. I. & Kim, H. S. High Resolution CT evaluation on the morphologic characteristics and variations of foramen ovale and adjacent foramina in the skull base. J. Korean Radiol. Soc., 33(1):43-8, 1995.

Kim, H. Y; Chung, E. C.; Suh, J. S., Choi, H. Y; Ko, E. J. & Lee, M. S. Skull-Base Foramina of the Middle Cranial Fossa: Assessment of Normal Variation with High-Resolution CT. J. Korean Radiol. Soc., 36(5):747-52, 1997.

Kodama, K.; Inoue, K.; Nagashima, M.; Matsumura, G.; Watanabe, S. & Kodama, G. Studies on the foramen vesalius in the Japanese juvenile and adult skulls. Hokkaido Igaku Zasshi, 72(6):667-74, 1997.

Kwathai, L.; Namonta, K.; Rungruang, T.; Chaisuksunt, V.; Apinhasmit, W. & Chompoopong, S. Anatomic and morphometric consideration for external landmarks of foramen spinosum in thai dry skulls. Siriraj Med. J., 64(Suppl. 1):S26-9, 2012.

Lang, J. Clinical Anatomy of the head. Neurocranium, orbit and craniocervical region. Berlin, Springer-Verlag, 1983.

Lang, J.; Maier, R. & Schafhauser, O. Postnatal enlargement of the foramina rotundum, ovale et spinosum and their topographical changes. Anat. Anz., 156(5):351-87, 1984.

Lanzieri, C. F.; Duchesneau, P M.; Rosenbloom, S. A.; Smith, A. S. & Rosenbaum, A. E. The significance of asymmetry of the foramen of Vesalius. AJNR Am. J. Neuroradiol., 9(6):1201-4, 1988.

Lindblom, K. Roentgenographic study of vascular channels of skull with special reference to intracranial tumors and arteriovenous aneurysms. Acta Radiol., 30:1-146, 1936.

Ozer, M. A. & Govsa, F. Measurement accuracy of foramen of vesalius for safe percutaneous techniques using computer-assisted three-dimensional landmarks. Surg. Radiol. Anat., 36(2):147-54, 2014.

Paullus, W. S.; Pait, T. G. & Rhoton, A. L. Jr. Microsurgical exposure of the petrous portion of the carotid artery. J. Neurosurg., 47(5):713-26, 1977.

Pandolfo, I.; Gaeta, M.; Blandino, A. & Longo, M. The radiology of the pterygoid canal: normal and pathologic findings. AJNR Am. J. Neuroradiol., 8(3):479-83, 1987.

Reymond, J.; Charuta, A. & Wysocki, J. The morphology and morphometry of the foramina of the greater wing of the human sphenoid bone. FoliaMorphol. (Warsz.), 64(3):188-93, 2005.

Shaik, H. S.; Shepur, M. P.; Desai, S. D.; Thomas, S. T.; Maavishettar, G. F. & Haseena, S. Study of foramen vesalius in South Indian skulls. Indian J. Med. Healthc., 1(1):22-4, 2012.

Sharma, N. A. & Garud, R. S. Morphometric evaluation and a report on the aberrations of the foramina in the intermediate region of the human cranial base: A study of an Indian population. Eur. J. Anat, 15(3):140-9, 2011.

Shinohara, A. L.; de Souza Melo, C. G.; Silveira, E. M.; Lauris, J. R.; Andreo, J. C. & de Castro Rodrigues, A. Incidence, morphology and morphometry of the foramen of Vesalius: complementary study for a safer planning and execution of the trigeminal rhizotomy technique. Surg. Radiol. Anat., 32(2):159-64, 2010.

Sondheimer, F. K. Basal foramina and canals. In: Newton, T. H. & Potts, D. G. (Eds.). Radiology of the skull and brain. St. Louis, Mosby, 1971. pp.305-21.

Srimani, P.; Mukherjee, P.; Sarkar, M.; Roy, H.; Sengupta, S. K.; Sarkar, A. N. & Ray, K. Foramina in alisphenoid--An observational study on their osseous-morphology and morphometry. Int. J. Anat. Radiol. Surg., 3(1):1-6, 2014.

Teul, I.; Czerwin'ski, F.; Gawlikowska, A.; Konstanty-Kurkiewicz, V & Sawin'ski, G. Asymmetry of the ovale and spinous foramina in mediaeval and contemporary skulls in radiological examinations. Folia Morphol. (Warsz.), 61(3):147-52, 2002.

Wood-Jones, F. The Non-metrical Morphological Characters of the Skull as Criteria for Racial Diagnosis: Part I: General Discussion of the Morphological Characters Employed in Racial Diagnosis. J. Anat., 65(Pt. 2):179-95, 1931.

Yanagi, S. Developmental studies on the foramen rotundum, foramen ovale and foramen spinosum of the human sphenoid bone. Hokkaido Igaku Zasshi, 62(3):485-96, 1987.

L. Lazarus *; N. Naidoo * & Satyapal, K. S. *

* Department of Clinical Anatomy, College of Health Sciences, School of Laboratory Medicine & Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.

Corresponding to:

Professor KS Satyapal

Department of Clinical Anatomy

College of Health Sciences

School of Laboratory Medicine & Medical Sciences

University of KwaZulu-Natal

Private Bag X54001

Durban

4001

SOUTH AFRICA

Telephone: + 27 31 260 7195

Email: satyapalk@ukzn.ac.za

Received: 24-06-2014

Accepted: 30-01-2015

Caption: Fig. 1. Superior view of middle cranial fossa demonstrating duplicate FS. Key: A = Anterior; FS = Foramen spinosum; L = Lateral; M = Medial; P = Posterior.

Caption: Fig. 2. Superior view of middle cranial fossa demonstrating duplicate FS and single FV bilaterally. Key: A= Anterior; FS = Foramen spinosum; FV = Foramen Venosum; L = Lateral; M = Medial; P = Posterior.

Caption: Fig. 3. Superior view of middle cranial fossa demonstrating duplicate FS and single FV on the left side and single FS and FV on the right side. Key: A = Anterior; FS = Foramen spinosum; FV = Foramen Venosum; L = Lateral; M = Medial; P = Posterior.

Caption: Fig. 4. Superior view of the middle cranial fossa demonstrating triplicate FS and duplicate FV on the left side. Key: A= Anterior; FS = Foramen spinosum; FV = Foramen Venosum; L = Lateral; M = Medial; P = Posterior.
Table I. Morphology and morphometry of FS and FV.

Parameter                          Foramen Spinosum
Incidence
                           R (n = 100)          L (n = 100)

    Single                   95 (95%)             95 (95%)
    Duplicate                 3 (3%)               2 (2%)
    Triplicate                  --                 1 (1%)
    Absent                    2 (2%)               2 (2%)
* Shape                    R (n = 106)          L (n = 107)
    Oval                    39 (36.8%)           48 (44.9%)
    Round                   62 (58.5%)           54 (50.5%)
* Mean diameter (mm)
    Internal            2.47 [+ or -] 0.73   2.59 [+ or -] 0.78
    External            2.46 [+ or -] 0.72   2.54 [+ or -] 0.76
* Distance to FO (mm)   3.44 [+ or -] 1.32   3.46 [+ or -] 1.26
* Relation to FO
Postero-lateral             99 (93.4%)           99 (92.5%)
Posterior                    2 (1.9%)             2 (1.9%)
Postero-medial                  --                1 (0.9%)
Anterior                        --                   --
Antero-medial                   --                   --

Parameter                Foramen Spinosum     Foramen Venosum
Incidence
                         Total (n = 200)         R(n = 100)

    Single                  190 (95%)              5 (5%)
    Duplicate                5 (2.5%)                --
    Triplicate               1 (0.5%)                --
    Absent                    4 (2%)                 --
* Shape                  Total (n = 213)         R(n = 106)
    Oval                    87 (43.5%)            4 (3.8%)
    Round                   116 (58%)             1 (0.9%)
* Mean diameter (mm)
    Internal            2.53 [+ or -] 0.76   2.06 [+ or -] 0.19
    External            2.50 [+ or -] 0.74   2.83 [+ or -] 1.65
* Distance to FO (mm)   3.45 [+ or -] 1.29   2.83 [+ or -] 1.59
* Relation to FO
Postero-lateral             198 (93%)                --
Posterior                    4 (1.9%)                --
Postero-medial               1 (0.5%)                --
Anterior                        --                1 (0.9%)
Antero-medial                   --                4 (3.8%)

Parameter                           Foramen Venosum
Incidence
                           L (n = 100)        Total (n = 200)

    Single                    5 (5%)              10 (5%)
    Duplicate                 1 (1%)              1 (0.5%)
    Triplicate                  --                   --
    Absent                      --                   --
* Shape                    L (n = 107)        Total (n = 213)
    Oval                     5 (4.7%)             9 (4.5%)
    Round                       --                1 (0.5%)
* Mean diameter (mm)
    Internal            1.79 [+ or -] 0.73   1.93 [+ or -] 0.46
    External            2.79 [+ or -] 1.40   2.81 [+ or -] 1.53
* Distance to FO (mm)   2.42 [+ or -] 0.88   2.63 [+ or -] 1.24
* Relation to FO
Postero-lateral                 --                   --
Posterior                       --                   --
Postero-medial                  --                   --
Anterior                        --                1 (0.5%)
Antero-medial                5 (4.7%)             9 (4.5%)

* Shape, Mean length, distance and relation to FO were calculated as a
percentage of the total number of foramina on each side

Table II. Incidence and shape of foramina spinosum and venosum in a
review of literature.

Author (year)                Sample size       Incidence (%)

                                            Spinosum    Venosum

Incidence: Absent
Lindblom (1936)             Not recorded       0.4
Berlis et al. (1992)             60            0.8        64.0
Ginsberg et al. (1994)           123           3.2        20.3
Kim et al. (1997)                163           2.5        45.4
Sharma & Garud (2011)            50            ---        38.0
Chaisuksunt et al. (2012)        754           ---        89.1
Present study                    200           2.0        ---
Incidence: Single
Sondheimer (1971)                50                       15%
Lang (1983)                 Not recorded       ---        40.0
Lanzieri et al. (1988)           54            ---        72.2
Ginsberg et al. (1994)           123           48         80.0
Kim & Kim (1995)                 305           ---        47.5
Kim et al. (1997)                163           ---        51.5
Kodama et al. (1997)             400           ---        21.8
Teul et al. (2002)               187           100        ---
Gupta et al. (2005) (a)          35            ---        42.9
Reymond et al. (2005)            100           100        17.0
Sharma & Garud (2011)            50           100.0       62.0
Chaisuksunt et al. (2012)        754           ---        10.9
Kwathai et al. (2012)            206          52.4        ---
Shaik et al. (2012)              250           ---        36.0
Dogan et al. (2014)              62            ---        32.3
Ozer & Govsa (2014)              344           ---        34.8
Srimani et al. (2014)            80            ---        5.0
Present study                    200          95.0         5
Incidence: Duplicate
Ginsberg et al. (1994)           123           0.8        13.8
Kim et al. (1997)                163           ---        3.1
Ozer & Govsa (2014)              344           ---        0.6
Present study                    200           2.5        0.5
Incidence: Triplicate
Present study                    200           0.5
Shape: Oval
Kwathai et al. (2012)            206          39.3
Srimani et al. (2014)            80            30         ---
Lazarus et al (2014)             213          43.5        4.5
Shape: Round
Kwathai et al. (2012)            26           43.2
Srimani et al. (2014)            80           51.3        ---
Present study                    213           58         0.5

Table III. Distance of foramen spinosum to foramen ovale in a review
of literature.

Author (year)            Distance (mm)    Range (mm)

Paullus et al. (1977)         3.2           1.0-6.0
Asian et al. (1998)           3.7          2.0-11.0
Present study                 3.5           0.9-8.6

Table IV Diameter of foramina spinosum and venosum in a review of
literature.

Author (year)                F. Spinosum (mm)    F. Venosum (mm)

Sondheimer (1971)                1.50-3.0              --
Lang et al. (1984)                  2.1                1.1
Yanagi (1987)                       2.7                --
Berlis et al. (1992)               1 .9                1.0
Aslan et al. (1998)                 --                 --
Sharma & Garud (2011)               2.6                --
Chaisuksunt et al. (2012)           --            15 [+ or -] 0.7
Kwathai et al. (2012)               2.2                --
Dogan et al. (2014)          1.9 [+ or -] 0.4     13 [+ or -] 05
Ozer & Govsa (2014)                 --           0.9 [+ or -] 0.3
Srimani et al. (2014)               --                 --
Present study                       2.5                2.4
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Author:Lazarus, L.; Naidoo, N.; Satyapal K.S.
Publication:International Journal of Morphology
Date:Jun 1, 2015
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