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Adding Expansile Duraplasty to Posterior Fossa Decompression May Restore Cervical Range of Motion in Grade 3 Chiari Malformation Type 1 Patients
Original Article
Adding Expansile Duraplasty to Posterior Fossa Decompression May Restore Cervical Range of Motion in Grade 3 Chiari Malformation Type 1 Patients Adem Yilmaz, Kamran Urgun, Salah G. Aoun, Ibrahim Colak, Ilhan Yilmaz, Kadir Altas, Murat Musluman
BACKGROUND: Few studies have assessed the effect of Chiari malformation type 1 (CM-1) surgical decompression on cervical lordosis and range of motion (ROM). We aimed to assess the effect of expansile duraplasty on postoperative cervical mobility and spinal stability.
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MATERIALS AND METHODS: This was a single-center retrospective review of prospectively collected data. Patients were included if they underwent surgical treatment for symptomatic CM-1 between the years 1999 and 2009. Cervical ROM and lordosis were assessed before and after surgery in all patients. Collected data also included clinical improvement, as well as surgical complications after the procedure. Patients were divided into 2 groups. The first group underwent a posterior fossa bony decompression alone, while the second group additionally received an expansile duraplasty. Patients were further subdivided into 3 subgroups on the basis of the severity of tonsillar herniation.
CONCLUSION: Adding an expansile duraplasty to craniovertebral decompression in CM-1 patients with severe tonsillar herniation may restore cervical ROM while preserving stability and alignment. This may relieve postoperative pain and improve clinical prognosis.
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RESULTS: A total of 76 patients fit our selection criteria. Fifty-five patients belonged to the duraplasty group. Twenty-one patients underwent bony decompression alone. The 2 groups were statistically demographically and clinically similar. There was no difference in clinical outcome or in ROM and cervical lordosis between the groups except for patients with severe tonsillar herniation (CM-I grade 3). These patients had a statistically significant improvement in their postoperative cervical motility without compromising their spinal stability.
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Key words Cervical lordosis - Cervical range of motion - Chiari type 1 malformation - Expansile duraplasty - Surgical outcome -
Abbreviations and Acronyms CM-1: Chiari malformation type 1 CVD: Craniovertebral decompression JOA: Japanese Orthopedic Association MRI: Magnetic resonance imaging ROM: Range of motion
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BACKGROUND
T
he treatment of Chiari malformation type 1 (CM-1) disease has been the subject of much controversy during the past 50 years.1-7 While some criteria are generally agreed upon as strong indications for a surgical intervention, such as the presence of a syrinx, or worsening neurologic deficits, most symptoms of the disease are still subject to debate as they frequently involve pain.6 The optimal choice of the surgical intervention itself is even more controversial, as it can range from craniovertebral decompression (CVD) alone to posterior fossa decompression with patch duraplasty and cerebellar tonsillar resection.8-11 To add to the complexity of this disease, CM-1 could potentially restrict cervical range of motion (ROM) and experts have questioned if and how surgery with CVD could affect cervical ROM, as well as cervical spine alignment and lordosis.6,7,12 Few studies have assessed the effect of CM-1 surgery on cervical ROM and lordosis, with most showing preservation of both preoperative ROM and alignment after decompression.6,7 However, the severity of tonsillar herniation in some cases and the fact that the dura is often found to be restrictive intraoperatively question the impact of expansile duraplasty on cervical and occipitocervical mechanics, especially as they often relate to postoperative pain. We aimed to study the effects of CM-1 decompression with or
From the Department of Neurological Surgery, University of Texas Southwestern Medical Center, Dallas, Texas, USA To whom correspondence should be addressed: Kamran Urgun, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017) 98:98-103. http://dx.doi.org/10.1016/j.wneu.2016.10.127 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE ADEM YILMAZ ET AL.
RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
without duraplasty on cervical ROM and cervical lordosis, stratified over different grades of tonsillar herniation. MATERIAL AND METHODS This study was a retrospective review of prospectively collected cases of CM-1 patients who underwent surgical treatment between 1999 and 2009 at a single institution. Ethical review board approval was obtained at our institution for the de-identified retrospective collection of patient data. All patients were adults older than 18 years of age. CM-1 was diagnosed using magnetic resonance imaging (MRI) in all cases. CM-1 grading was defined on the basis of previously validated methods in the literature.5,6,13,14 Briefly, in grade 1 the tonsils descended 5 mm below the level of the foramen magnum but did not reach the arch of C1. Grade 2 was defined by the tonsils reaching the arch of C1, and grade 3 by a descent under the arch (Figure 1). Cases with assimilated vertebrae and laminar hypoplasia were excluded. Patients were divided in a CVD-only group and a CVD with duraplasty group. Selection of the surgical treatment was at the discretion of the treating physician. Each group was further subdivided according to the preoperative CM-1 grade into the 3 subgroups described earlier. Surgical indications included severe symptoms such as pressure and Valsalva-type headaches, drop attacks, cranial or peripheral nerve dysfunction, and dysphagia. The presence of a syrinx was also an indication for surgery when coupled with signs of neurologic compromise or uncontrollable headaches. CVD was always done with an attempt to preserve the rectus capitis posterior major, semispinalis, and inferior oblique muscles at their insertion on the C2 arch. A C1 laminectomy was performed in most cases. When duraplasty was deemed necessary, we used a dural Y incision with various grafting material at the discretion of the operator, which included cadaveric dura, bovine pericardium, fascia lata, or autologous pericranium. Cervical ROM and lordosis measurements were obtained for all patients on preoperative and 12-month follow-up imaging. Measurements were made using a computer drafting software (Autocad 2008, Autodesk, Inc., Mill Valley, California, USA). They were done using hyperflexion and hyperextension cervical plain films according to the method previously validated by Ranawat et al.7 and Ono et al.6,15,16 Briefly, the angle between the occiput and C1 was measured at the intersection between a line drawn at the base of the skull and a line connecting the centers of the anterior and posterior C1 arches. The angle at C1eC2 was measured at the intersection between the C1 line and a line drawn parallel to the inferior end plate of the C2 vertebral body. The angle at OceC2 was measured at the intersection between the line drawn on the base of the skull and a line drawn parallel to the inferior end plate of the C2 vertebral body. Because a laminectomy was performed at C1, and therefore the line could not be measured at C1, only the angle at OceC2 was measured after surgery. The angle at C2e3 or below was measured using a line drawn parallel to the inferior end plate of each vertebral body. The lordosis angle at C2e7 was measured at the intersection between the C2 and C7 lines as described earlier on a lateral x-ray view of the cervical spine in neutral position (Figure 2). An example of these measurements is illustrated in Figure 2.
WORLD NEUROSURGERY 98: 98-103, FEBRUARY 2017
Figure 1. Sagittal magnetic resonance images of the craniocervical junction showing the differences among grade I, II, and III Chiari type 1 malformations. Yellow arrows designate the cerebellar tonsils, and red arrows designate the arch of C1.
An MRI was obtained in all cases within 3e5 days after surgery and at least 1 more time during a follow-up consultation, which was usually 3e6 months later, to evaluate the decompression, tonsillar herniation, and evolution of any existing
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RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
Figure 2. Example of angle measurement at different cervical levels and during assessment of cervical lordosis.
Table 1. Clinical, Demographic, and Radiologic Data of Our Study Population CVD D Duraplasty CVD Alone (n [ 55) (n [ 21) P Value Female/Male ratio
32/23
10/11
0.9 0.6
Age
39.4 10.99
31.23 8.72
Presence of a syrinx before surgery
42 (76.36%)
17 (80.95%)
Postoperative resolution of the syrinx at last follow-up
41 (74.54%)
15 (71.42%)
JOA score before surgery
14.18 2.23
14.76 2.44
0.72
JOA score after surgery
15.78 2.24
16.19 2.15
0.65
Clinical improvement at last follow-up
42 (76.36%)
19 (90.47%)
syrinx. Clinical symptoms before and after surgery were assessed using the modified Japanese Orthopedic Association scale before surgery and during the final follow-up evaluation.17-19 Statistical analysis was performed using the SPSS software version 10.0.7 (SPSS, Inc., Chicago, Illinois, USA) and included Student’s t-test, analysis of variance, and multivariate regression analyses. A probability or “P” value <0.05 was considered to be statistically significant. RESULTS Seventy-six patients were identified to fit our selection criteria. Two patients with assimilated vertebrae and 1 patient with laminar hypoplasia were excluded from the analysis. A total of 55 patients underwent CVD with duraplasty while 21 patients underwent CVD
Table 2. Signs and Symptoms Linked to Tonsillar Herniation in Chiari Type 1 Malformation and Prompting Surgery Symptom and Sign
Postoperative complications
CTD CTD CTD Grade 1 Grade 2 Grade 3
2
1
Headache
29
23
13
Infection
1
1
Cervicalgia
22
21
10
Cerebrospinal fluid leak
3
Dysphagia
1
2
2
Bacterial meningitis
1
Impaired gag reflex
0
2
3
6
10
5
17
11
5
Neurologic deficit
Need for additional surgery
2 (3.6%)
2 (9.5%)
Lower extremity paresthesia/hyperesthesia
Grade of Chiari malformation
Dizziness
1
24 (43.6%)
10 (47.6%)
0.53
Tinnitus
4
3
2
2
20 (36.3)
7 (33.3%)
0.54
Upper extremity weakness
3
5
6
3
11 (20%)
4 (19%)
0.45
Lower extremity Weakness or unsteady gait
0
1
3
CVD, craniovertebral decompression; JOA, Japanese Orthopedic Association.
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CTD, cerebellar tonsillar descent.
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Angle Measurement of Flexion-Extension Range of Motion in Degrees
OceC2 ( )
C2e3 ( )
C3e4 ( )
C4e5 ( )
C5e6 ( )
C6e7 ( )
C2e7 ( )
OceC7 ( )
Lordosis Angle at C2e7 ( )
Grade 1
17.89 6.5
7.62 3.37
9.25 2.89
14.23 3.83
13.3 4.46
8.62 3.09
52,28 9,18
70.17 12.87
24.62 8.75
Grade 2
20.21 8.21
8.41 3.2
10.21 4.2
14.01 4.9
11.35 5.51
7.97 3.61
49.39 13.82
71.60 10.83
24.77 9.37
68.52 12.01*
OceC1 ( )
C1eC2 ( )
ADEM YILMAZ ET AL.
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Table 3. Angles of Range of Motion and Angles of Cervical Lordosis at Each Occipitocervical Level Before and After Surgery
PFD with Duraplasty Before Surgery
16.49 4.39
7.59 3.66
8.86 2.69
15.32 3.33
13.94 5.74
10.38 3.82
52.02 8.82
18.45 6.88
7.9 3.33
9.5 3.38
14.3 4.12
12.7 5.14
8.7 3.48
51.1 10.9
Grade 1
16.55 6.64
7.07 5.53
9.88 2.47
13.92 3.65
13.00 4.89
8.85 3.13
51.23 9.86
68.78 13.23
24.86 7.56
Grade 2
18.34 6.15
6.72 3.00
12.92 4.10
14.26 4.84
12.02 5.54
7.33 5.16
51.53 15.66
71.88 13.88
23.23 6.56
Grade 3
17.51 4.77
6.36 2.18
12.14 3.42
15.75 2.54
16.08 6.5
9.00 4.51
56.56 10.28
74.07 13.28*
21.80 4.62
Mean
17.39 6.0
6.8 3.07
11.4 3.56
14.4 3.95
13.2 5.57
8.3 4.23
52.4 12.3
8 3.76
8.56 2.73
14.34 3.55
12.9 2.62
9.75 4.2
53.35 6.65
69.55 9.67
24.45 8.61
Grade 3 Mean
8.9 5.0
9.6 3.8
21.73 6.50 24.09 8.53
After Surgery
23.6 6.7
PFD Alone Before Surgery 16.2 9.42
Grade 2
15.67 6.02
10.16 4.96
16.77 5.5
14.09 2.61
10.8 8.54
57.87 11.87
73.54 14.66
23.88 8.70
Grade 3
20.81 5.34
9.1 2.68
11.45 4.13
13.23 2.44
12.92 2.99
8.51 4.84
54.91 24.51
75.73 5.45
25.79 5.83
16.9 7.6
9.1 4.5
10.5 3.4
15.9 4.01
14.1 2.57
10.05 5.79
52.35 13.32
19.55 6.29
7.78 2.05
11.44 2.72
15.45 4.3
14.58 6.04
8.49 4.57
55.27 5.34
Mean
8.2 5.0
8.8 3.8
8.79 6.5
24.51 7.8
After Surgery 74.83 7.82
25.71 8.69
Grade 2
12.69 4.91
8.63 4.94
7.89 4,45
10.96 4.16
11.11 5.16
9.16 8.74
52.84 13.29
65.53 17.69
24.71 6.66
Grade 3
20.08 5.02
7.89 2.27
11.9 2.96
13.1 2.17
12.53 2.59
8.35 4.58
54.19 25.04
74.28 4.12
25.46 5.44
Mean
17.36 6.3
8.27 3.2
10.7 3.96
13.9 4.33
13.4 5.3
8.68 5.97
52.35 13.32
Bolded values were found to be statistically significant. *P < 0.05.
25.33 7.2
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Grade 1
RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
Grade 1
ORIGINAL ARTICLE ADEM YILMAZ ET AL.
RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
alone. Patient clinical, demographic, and radiologic data are summarized in Table 1. Fifteen patients had a grade 3 Chiari malformation. Eleven underwent CVD with duraplasty, while 5 underwent CVD alone. The majority of patient in both groups had an increase in their JOA score and clinically improved after their surgery. There was no statistically significant difference between the demographic characteristics of the group that underwent a posterior fossa decompression alone and those who received additional duraplasty or in their postoperative improvement when it related to the degree of clinical improvement or the increase in JOA score, as displayed in Table 1. Table 2 summarizes the signs and symptoms related to the tonsillar herniation and prompting for surgery in all cases. The ROMs and angles of cervical lordosis for each occipitocervical level were measured in all patients as described earlier and are displayed in detail in Table 3. There was no statistically significant difference in the ROM and the range of cervical lordosis when comparing preoperative and postoperative findings or when comparing the group of patients who had received a CVD alone with those who also underwent an duraplasty, with the singular exception of grade 3 Chiari malformation patients, who had benefited from a decompression with a patch duraplasty. The cervical ROM actually improved after surgery in this subpopulation in a statistically significant fashion (P ¼ 0.044). DISCUSSION Assessing the causal relationship between CM-1 and ROM restriction at the occipitocervical region is difficult because of the paucity of large prospective cohorts and lack of conformity in the patient population that undergoes CVD. Previous landmark studies had revealed a tendency in CM-1 patients to have a reduced OceC2 ROM compared with the general population.6,20,21 A frequently cited study by Ono et al6 involved 1 of the larger consecutive groups of cases to date and assessed the effect on CVD without expansile duraplasty on the cervical ROM and on postoperative cervical stability and lordosis. Two theories were being questioned: 1) Does CM-1 limit cervical ROM, and would CVD offer a corrective option? 2) Does CVD reduce cervical stability and thus affect the cervical angle of lordosis because of iatrogenic injury to posterior cervical muscles? At the conclusion of their analysis, the authors deduced that CVD does not compromise cervical alignment if done with care to preserve the muscular attachments at the arch of C2. However, perhaps due to the small number of patients in their series, they could not
REFERENCES 1. Dyste GN, Menezes AH, VanGilder JC. Symptomatic Chiari malformations. An analysis of presentation, management, and long-term outcome. J Neurosurg. 1989;71:159-168. 2. Dure LS, Percy AK, Cheek WR, Laurent JP. Chiari type i malformation in children. J Pediatr. 1989;115: 573-576. 3. Bertrand SL, Drvaric DM, Roberts JM. Scoliosis in syringomyelia. Orthopedics. 1989;12:335-337.
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correlate the degree of tonsillar herniation to the ROM reduction at OceC2. Our current study confirms these findings. Tonsillar herniation was not correlated to the restriction of occipitocervical ROM, and cervical lordosis was preserved after CVD. Most of our patients also improved clinically after surgery. However, the larger arm of our population involved expansile duraplasty; in the subgroup of patients with grade 3 herniation, expansile duraplasty appeared to improve cervical ROM after surgery without compromising cervical stability or alignment. This may be due to the fact that in more severe cases of tonsillar herniation, where medullary compression is pronounced and cerebrospinal fluid impinged, occipitocervical ROM is more affected than in milder cases and is prone to more significant correction after surgical decompression.6,12 Given the fact that increased cervical ROM has been associated with decreased postoperative pain,22,23 this finding may provide an argument toward adding an expansile duraplasty to CVD in cases of severe tonsillar herniation. Unfortunately, and likely because of the statistically small number of patients in our series, although it is one of the larger reported in the literature, we believe that our study was underpowered to detect a statistically significant difference in the postoperative JOA score increase and the clinical improvement between the 2 groups. Limitations of our study include its retrospective nature and the relatively small size of our study population, although it is one of the larger published to date. It appears greater numbers may be necessary to unmask a possible correlation between the degree of tonsillar herniation and a causal limitation in cervical ROM. Finally, using cerebrospinal fluid flow studies may shed additional light on the mechanics involved in increasing cervical ROM limitation with worsening tonsillar herniation and could explain why expansile duraplasty appears to have a larger benefit in grade 3 patients.
CONCLUSION We assessed the effect of CVD with or without expansile duraplasty in patients with CM-1 disease on occipitocervical ROM and cervical stability and lordosis. Our results converge with those of previous studies in proving that CVD with or without duraplasty is a low-risk procedure that is protective of the biomechanics of the cervical spine. More interestingly, our study shows that in severe cases of tonsillar herniation such as grade 3 CM-1, expansile duraplasty may provide some degree of restoration to the ROM while preserving cervical alignment and stability. This could relieve postoperative pain and may improve clinical prognosis.
4. Bondurant CP, Oro JJ. Spinal cord injury without radiographic abnormality and chiari malformation. J Neurosurg. 1993;79:833-838. 5. Elster AD, Chen MY. Chiari I malformations: Clinical and radiologic reappraisal. Radiology. 1992;183:347-353. 6. Ono A, Suetsuna F, Ueyama K, Yokoyama T, Aburakawa S, Takeuchi K, et al. Cervical spinal motion before and after surgery in patients with Chiari malformation type I associated with syringomyelia. J Neurosurg Spine. 2007;7:473-477.
7. Ranawat CS, O’Leary P, Pellicci P, Tsairis P, Marchisello P, Dorr L. Cervical spine fusion in rheumatoid arthritis. J Bone Joint Surg Am. 1979;61: 1003-1010. 8. Munshi I, Frim D, Stine-Reyes R, Weir BK, Hekmatpanah J, Brown F. Effects of posterior fossa decompression with and without duraplasty on chiari malformation-associated hydromyelia. Neurosurgery. 2000;46:1384-1389 [discussion: 1389-1390]. 9. Yundt KD, Park TS, Tantuwaya VS, Kaufman BA. Posterior fossa decompression without duraplasty in infants and young children for treatment of
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RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
Chiari malformation and achondroplasia. Pediatr Neurosurg. 1996;25:221-226.
studied by cine phase-contrast MRI. Neurology. 1995;45:1746-1753.
20. Penning L. Normal movements of the cervical spine. AJR Am J Roentgenol. 1978;130:317-326.
10. Sindou M, Chavez-Machuca J, Hashish H. Craniocervical decompression for chiari type I-malformation, adding extreme lateral foramen magnum opening and expansile duroplasty with arachnoid preservation. Technique and long-term functional results in 44 consecutive adult cases—comparison with literature data. Acta Neurochir (Wien). 2002; 144:1005-1019.
15. Ono A, Suetsuna F, Ueyama K, Yokoyama T, Aburakawa S, Numasawa T, et al. Surgical outcomes in adult patients with syringomyelia associated with chiari malformation type i: The relationship between scoliosis and neurological findings. J Neurosurg Spine. 2007;6:216-221.
21. White AA 3rd, Panjabi MM. The basic kinematics of the human spine. A review of past and current knowledge. Spine (Phila Pa 1976). 1978;3: 12-20.
11. Guyotat J, Bret P, Jouanneau E, Ricci AC, Lapras C. Syringomyelia associated with type I Chiari malformation. A 21-year retrospective study on 75 cases treated by foramen magnum decompression with a special emphasis on the value of tonsils resection. Acta Neurochir (Wien). 1998;140: 745-754. 12. Takeuchi K, Yokoyama T, Ito J, Wada K, Itabashi T, Toh S. Tonsillar herniation and the cervical spine: a morphometric study of 172 patients. J Orthop Sci. 2007;12:55-60. 13. Armonda RA, Citrin CM, Foley KT, Ellenbogen RG. Quantitative cine-mode magnetic resonance imaging of chiari I malformations: an analysis of cerebrospinal fluid dynamics. Neurosurgery. 1994;35:214-223 [discussion: 223-224]. 14. Pujol J, Roig C, Capdevila A, Pou A, MartiVilalta JL, Kulisevsky J, et al. Motion of the cerebellar tonsils in Chiari type I malformation
16. Ono A, Ueyama K, Okada A, Echigoya N, Yokoyama T, Harata S. Adult scoliosis in syringomyelia associated with Chiari I malformation. Spine (Phila Pa 1976). 2002;27:E23-E28. 17. Benzel EC, Lancon J, Kesterson L, Hadden T. Cervical laminectomy and dentate ligament section for cervical spondylotic myelopathy. J Spinal Disord. 1991;4:286-295. 18. Yonenobu K, Abumi K, Nagata K, Taketomi E, Ueyama K. Interobserver and intraobserver reliability of the Japanese orthopaedic association scoring system for evaluation of cervical compression myelopathy. Spine (Phila Pa 1976). 2001;26:1890-1894 [discussion: 1895]. 19. Hirabayashi K, Miyakawa J, Satomi K, Maruyama T, Wakano K. Operative results and postoperative progression of ossification among patients with ossification of cervical posterior longitudinal ligament. Spine (Phila Pa 1976). 1981;6: 354-364.
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22. Hou CR, Tsai LC, Cheng KF, Chung KC, Hong CZ. Immediate effects of various physical therapeutic modalities on cervical myofascial pain and trigger-point sensitivity. Arch Phys Med Rehabil. 2002;83:1406-1414. 23. Cassidy JD, Lopes AA, Yong-Hing K. The immediate effect of manipulation versus mobilization on pain and range of motion in the cervical spine: a randomized controlled trial. J Manipulative Physiol Ther. 1992;15:570-575.
Conflict of interest statement: The authors have no personal conflicts of interests to disclose. Received 2 September 2016; accepted 25 October 2016 Citation: World Neurosurg. (2017) 98:98-103. http://dx.doi.org/10.1016/j.wneu.2016.10.127 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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Adding Expansile Duraplasty to Posterior Fossa Decompression May Restore Cervical Range of Motion in Grade 3 Chiari Malformation Type 1 Patients Adem Yilmaz, Kamran Urgun, Salah G. Aoun, Ibrahim Colak, Ilhan Yilmaz, Kadir Altas, Murat Musluman
BACKGROUND: Few studies have assessed the effect of Chiari malformation type 1 (CM-1) surgical decompression on cervical lordosis and range of motion (ROM). We aimed to assess the effect of expansile duraplasty on postoperative cervical mobility and spinal stability.
-
MATERIALS AND METHODS: This was a single-center retrospective review of prospectively collected data. Patients were included if they underwent surgical treatment for symptomatic CM-1 between the years 1999 and 2009. Cervical ROM and lordosis were assessed before and after surgery in all patients. Collected data also included clinical improvement, as well as surgical complications after the procedure. Patients were divided into 2 groups. The first group underwent a posterior fossa bony decompression alone, while the second group additionally received an expansile duraplasty. Patients were further subdivided into 3 subgroups on the basis of the severity of tonsillar herniation.
CONCLUSION: Adding an expansile duraplasty to craniovertebral decompression in CM-1 patients with severe tonsillar herniation may restore cervical ROM while preserving stability and alignment. This may relieve postoperative pain and improve clinical prognosis.
-
-
RESULTS: A total of 76 patients fit our selection criteria. Fifty-five patients belonged to the duraplasty group. Twenty-one patients underwent bony decompression alone. The 2 groups were statistically demographically and clinically similar. There was no difference in clinical outcome or in ROM and cervical lordosis between the groups except for patients with severe tonsillar herniation (CM-I grade 3). These patients had a statistically significant improvement in their postoperative cervical motility without compromising their spinal stability.
-
Key words Cervical lordosis - Cervical range of motion - Chiari type 1 malformation - Expansile duraplasty - Surgical outcome -
Abbreviations and Acronyms CM-1: Chiari malformation type 1 CVD: Craniovertebral decompression JOA: Japanese Orthopedic Association MRI: Magnetic resonance imaging ROM: Range of motion
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BACKGROUND
T
he treatment of Chiari malformation type 1 (CM-1) disease has been the subject of much controversy during the past 50 years.1-7 While some criteria are generally agreed upon as strong indications for a surgical intervention, such as the presence of a syrinx, or worsening neurologic deficits, most symptoms of the disease are still subject to debate as they frequently involve pain.6 The optimal choice of the surgical intervention itself is even more controversial, as it can range from craniovertebral decompression (CVD) alone to posterior fossa decompression with patch duraplasty and cerebellar tonsillar resection.8-11 To add to the complexity of this disease, CM-1 could potentially restrict cervical range of motion (ROM) and experts have questioned if and how surgery with CVD could affect cervical ROM, as well as cervical spine alignment and lordosis.6,7,12 Few studies have assessed the effect of CM-1 surgery on cervical ROM and lordosis, with most showing preservation of both preoperative ROM and alignment after decompression.6,7 However, the severity of tonsillar herniation in some cases and the fact that the dura is often found to be restrictive intraoperatively question the impact of expansile duraplasty on cervical and occipitocervical mechanics, especially as they often relate to postoperative pain. We aimed to study the effects of CM-1 decompression with or
From the Department of Neurological Surgery, University of Texas Southwestern Medical Center, Dallas, Texas, USA To whom correspondence should be addressed: Kamran Urgun, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017) 98:98-103. http://dx.doi.org/10.1016/j.wneu.2016.10.127 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE ADEM YILMAZ ET AL.
RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
without duraplasty on cervical ROM and cervical lordosis, stratified over different grades of tonsillar herniation. MATERIAL AND METHODS This study was a retrospective review of prospectively collected cases of CM-1 patients who underwent surgical treatment between 1999 and 2009 at a single institution. Ethical review board approval was obtained at our institution for the de-identified retrospective collection of patient data. All patients were adults older than 18 years of age. CM-1 was diagnosed using magnetic resonance imaging (MRI) in all cases. CM-1 grading was defined on the basis of previously validated methods in the literature.5,6,13,14 Briefly, in grade 1 the tonsils descended 5 mm below the level of the foramen magnum but did not reach the arch of C1. Grade 2 was defined by the tonsils reaching the arch of C1, and grade 3 by a descent under the arch (Figure 1). Cases with assimilated vertebrae and laminar hypoplasia were excluded. Patients were divided in a CVD-only group and a CVD with duraplasty group. Selection of the surgical treatment was at the discretion of the treating physician. Each group was further subdivided according to the preoperative CM-1 grade into the 3 subgroups described earlier. Surgical indications included severe symptoms such as pressure and Valsalva-type headaches, drop attacks, cranial or peripheral nerve dysfunction, and dysphagia. The presence of a syrinx was also an indication for surgery when coupled with signs of neurologic compromise or uncontrollable headaches. CVD was always done with an attempt to preserve the rectus capitis posterior major, semispinalis, and inferior oblique muscles at their insertion on the C2 arch. A C1 laminectomy was performed in most cases. When duraplasty was deemed necessary, we used a dural Y incision with various grafting material at the discretion of the operator, which included cadaveric dura, bovine pericardium, fascia lata, or autologous pericranium. Cervical ROM and lordosis measurements were obtained for all patients on preoperative and 12-month follow-up imaging. Measurements were made using a computer drafting software (Autocad 2008, Autodesk, Inc., Mill Valley, California, USA). They were done using hyperflexion and hyperextension cervical plain films according to the method previously validated by Ranawat et al.7 and Ono et al.6,15,16 Briefly, the angle between the occiput and C1 was measured at the intersection between a line drawn at the base of the skull and a line connecting the centers of the anterior and posterior C1 arches. The angle at C1eC2 was measured at the intersection between the C1 line and a line drawn parallel to the inferior end plate of the C2 vertebral body. The angle at OceC2 was measured at the intersection between the line drawn on the base of the skull and a line drawn parallel to the inferior end plate of the C2 vertebral body. Because a laminectomy was performed at C1, and therefore the line could not be measured at C1, only the angle at OceC2 was measured after surgery. The angle at C2e3 or below was measured using a line drawn parallel to the inferior end plate of each vertebral body. The lordosis angle at C2e7 was measured at the intersection between the C2 and C7 lines as described earlier on a lateral x-ray view of the cervical spine in neutral position (Figure 2). An example of these measurements is illustrated in Figure 2.
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Figure 1. Sagittal magnetic resonance images of the craniocervical junction showing the differences among grade I, II, and III Chiari type 1 malformations. Yellow arrows designate the cerebellar tonsils, and red arrows designate the arch of C1.
An MRI was obtained in all cases within 3e5 days after surgery and at least 1 more time during a follow-up consultation, which was usually 3e6 months later, to evaluate the decompression, tonsillar herniation, and evolution of any existing
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Figure 2. Example of angle measurement at different cervical levels and during assessment of cervical lordosis.
Table 1. Clinical, Demographic, and Radiologic Data of Our Study Population CVD D Duraplasty CVD Alone (n [ 55) (n [ 21) P Value Female/Male ratio
32/23
10/11
0.9 0.6
Age
39.4 10.99
31.23 8.72
Presence of a syrinx before surgery
42 (76.36%)
17 (80.95%)
Postoperative resolution of the syrinx at last follow-up
41 (74.54%)
15 (71.42%)
JOA score before surgery
14.18 2.23
14.76 2.44
0.72
JOA score after surgery
15.78 2.24
16.19 2.15
0.65
Clinical improvement at last follow-up
42 (76.36%)
19 (90.47%)
syrinx. Clinical symptoms before and after surgery were assessed using the modified Japanese Orthopedic Association scale before surgery and during the final follow-up evaluation.17-19 Statistical analysis was performed using the SPSS software version 10.0.7 (SPSS, Inc., Chicago, Illinois, USA) and included Student’s t-test, analysis of variance, and multivariate regression analyses. A probability or “P” value <0.05 was considered to be statistically significant. RESULTS Seventy-six patients were identified to fit our selection criteria. Two patients with assimilated vertebrae and 1 patient with laminar hypoplasia were excluded from the analysis. A total of 55 patients underwent CVD with duraplasty while 21 patients underwent CVD
Table 2. Signs and Symptoms Linked to Tonsillar Herniation in Chiari Type 1 Malformation and Prompting Surgery Symptom and Sign
Postoperative complications
CTD CTD CTD Grade 1 Grade 2 Grade 3
2
1
Headache
29
23
13
Infection
1
1
Cervicalgia
22
21
10
Cerebrospinal fluid leak
3
Dysphagia
1
2
2
Bacterial meningitis
1
Impaired gag reflex
0
2
3
6
10
5
17
11
5
Neurologic deficit
Need for additional surgery
2 (3.6%)
2 (9.5%)
Lower extremity paresthesia/hyperesthesia
Grade of Chiari malformation
Dizziness
1
24 (43.6%)
10 (47.6%)
0.53
Tinnitus
4
3
2
2
20 (36.3)
7 (33.3%)
0.54
Upper extremity weakness
3
5
6
3
11 (20%)
4 (19%)
0.45
Lower extremity Weakness or unsteady gait
0
1
3
CVD, craniovertebral decompression; JOA, Japanese Orthopedic Association.
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CTD, cerebellar tonsillar descent.
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Angle Measurement of Flexion-Extension Range of Motion in Degrees
OceC2 ( )
C2e3 ( )
C3e4 ( )
C4e5 ( )
C5e6 ( )
C6e7 ( )
C2e7 ( )
OceC7 ( )
Lordosis Angle at C2e7 ( )
Grade 1
17.89 6.5
7.62 3.37
9.25 2.89
14.23 3.83
13.3 4.46
8.62 3.09
52,28 9,18
70.17 12.87
24.62 8.75
Grade 2
20.21 8.21
8.41 3.2
10.21 4.2
14.01 4.9
11.35 5.51
7.97 3.61
49.39 13.82
71.60 10.83
24.77 9.37
68.52 12.01*
OceC1 ( )
C1eC2 ( )
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Table 3. Angles of Range of Motion and Angles of Cervical Lordosis at Each Occipitocervical Level Before and After Surgery
PFD with Duraplasty Before Surgery
16.49 4.39
7.59 3.66
8.86 2.69
15.32 3.33
13.94 5.74
10.38 3.82
52.02 8.82
18.45 6.88
7.9 3.33
9.5 3.38
14.3 4.12
12.7 5.14
8.7 3.48
51.1 10.9
Grade 1
16.55 6.64
7.07 5.53
9.88 2.47
13.92 3.65
13.00 4.89
8.85 3.13
51.23 9.86
68.78 13.23
24.86 7.56
Grade 2
18.34 6.15
6.72 3.00
12.92 4.10
14.26 4.84
12.02 5.54
7.33 5.16
51.53 15.66
71.88 13.88
23.23 6.56
Grade 3
17.51 4.77
6.36 2.18
12.14 3.42
15.75 2.54
16.08 6.5
9.00 4.51
56.56 10.28
74.07 13.28*
21.80 4.62
Mean
17.39 6.0
6.8 3.07
11.4 3.56
14.4 3.95
13.2 5.57
8.3 4.23
52.4 12.3
8 3.76
8.56 2.73
14.34 3.55
12.9 2.62
9.75 4.2
53.35 6.65
69.55 9.67
24.45 8.61
Grade 3 Mean
8.9 5.0
9.6 3.8
21.73 6.50 24.09 8.53
After Surgery
23.6 6.7
PFD Alone Before Surgery 16.2 9.42
Grade 2
15.67 6.02
10.16 4.96
16.77 5.5
14.09 2.61
10.8 8.54
57.87 11.87
73.54 14.66
23.88 8.70
Grade 3
20.81 5.34
9.1 2.68
11.45 4.13
13.23 2.44
12.92 2.99
8.51 4.84
54.91 24.51
75.73 5.45
25.79 5.83
16.9 7.6
9.1 4.5
10.5 3.4
15.9 4.01
14.1 2.57
10.05 5.79
52.35 13.32
19.55 6.29
7.78 2.05
11.44 2.72
15.45 4.3
14.58 6.04
8.49 4.57
55.27 5.34
Mean
8.2 5.0
8.8 3.8
8.79 6.5
24.51 7.8
After Surgery 74.83 7.82
25.71 8.69
Grade 2
12.69 4.91
8.63 4.94
7.89 4,45
10.96 4.16
11.11 5.16
9.16 8.74
52.84 13.29
65.53 17.69
24.71 6.66
Grade 3
20.08 5.02
7.89 2.27
11.9 2.96
13.1 2.17
12.53 2.59
8.35 4.58
54.19 25.04
74.28 4.12
25.46 5.44
Mean
17.36 6.3
8.27 3.2
10.7 3.96
13.9 4.33
13.4 5.3
8.68 5.97
52.35 13.32
Bolded values were found to be statistically significant. *P < 0.05.
25.33 7.2
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ORIGINAL ARTICLE ADEM YILMAZ ET AL.
RESTORING CERVICAL ROM IN GRADE 3 CM-I PATIENTS
alone. Patient clinical, demographic, and radiologic data are summarized in Table 1. Fifteen patients had a grade 3 Chiari malformation. Eleven underwent CVD with duraplasty, while 5 underwent CVD alone. The majority of patient in both groups had an increase in their JOA score and clinically improved after their surgery. There was no statistically significant difference between the demographic characteristics of the group that underwent a posterior fossa decompression alone and those who received additional duraplasty or in their postoperative improvement when it related to the degree of clinical improvement or the increase in JOA score, as displayed in Table 1. Table 2 summarizes the signs and symptoms related to the tonsillar herniation and prompting for surgery in all cases. The ROMs and angles of cervical lordosis for each occipitocervical level were measured in all patients as described earlier and are displayed in detail in Table 3. There was no statistically significant difference in the ROM and the range of cervical lordosis when comparing preoperative and postoperative findings or when comparing the group of patients who had received a CVD alone with those who also underwent an duraplasty, with the singular exception of grade 3 Chiari malformation patients, who had benefited from a decompression with a patch duraplasty. The cervical ROM actually improved after surgery in this subpopulation in a statistically significant fashion (P ¼ 0.044). DISCUSSION Assessing the causal relationship between CM-1 and ROM restriction at the occipitocervical region is difficult because of the paucity of large prospective cohorts and lack of conformity in the patient population that undergoes CVD. Previous landmark studies had revealed a tendency in CM-1 patients to have a reduced OceC2 ROM compared with the general population.6,20,21 A frequently cited study by Ono et al6 involved 1 of the larger consecutive groups of cases to date and assessed the effect on CVD without expansile duraplasty on the cervical ROM and on postoperative cervical stability and lordosis. Two theories were being questioned: 1) Does CM-1 limit cervical ROM, and would CVD offer a corrective option? 2) Does CVD reduce cervical stability and thus affect the cervical angle of lordosis because of iatrogenic injury to posterior cervical muscles? At the conclusion of their analysis, the authors deduced that CVD does not compromise cervical alignment if done with care to preserve the muscular attachments at the arch of C2. However, perhaps due to the small number of patients in their series, they could not
REFERENCES 1. Dyste GN, Menezes AH, VanGilder JC. Symptomatic Chiari malformations. An analysis of presentation, management, and long-term outcome. J Neurosurg. 1989;71:159-168. 2. Dure LS, Percy AK, Cheek WR, Laurent JP. Chiari type i malformation in children. J Pediatr. 1989;115: 573-576. 3. Bertrand SL, Drvaric DM, Roberts JM. Scoliosis in syringomyelia. Orthopedics. 1989;12:335-337.
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correlate the degree of tonsillar herniation to the ROM reduction at OceC2. Our current study confirms these findings. Tonsillar herniation was not correlated to the restriction of occipitocervical ROM, and cervical lordosis was preserved after CVD. Most of our patients also improved clinically after surgery. However, the larger arm of our population involved expansile duraplasty; in the subgroup of patients with grade 3 herniation, expansile duraplasty appeared to improve cervical ROM after surgery without compromising cervical stability or alignment. This may be due to the fact that in more severe cases of tonsillar herniation, where medullary compression is pronounced and cerebrospinal fluid impinged, occipitocervical ROM is more affected than in milder cases and is prone to more significant correction after surgical decompression.6,12 Given the fact that increased cervical ROM has been associated with decreased postoperative pain,22,23 this finding may provide an argument toward adding an expansile duraplasty to CVD in cases of severe tonsillar herniation. Unfortunately, and likely because of the statistically small number of patients in our series, although it is one of the larger reported in the literature, we believe that our study was underpowered to detect a statistically significant difference in the postoperative JOA score increase and the clinical improvement between the 2 groups. Limitations of our study include its retrospective nature and the relatively small size of our study population, although it is one of the larger published to date. It appears greater numbers may be necessary to unmask a possible correlation between the degree of tonsillar herniation and a causal limitation in cervical ROM. Finally, using cerebrospinal fluid flow studies may shed additional light on the mechanics involved in increasing cervical ROM limitation with worsening tonsillar herniation and could explain why expansile duraplasty appears to have a larger benefit in grade 3 patients.
CONCLUSION We assessed the effect of CVD with or without expansile duraplasty in patients with CM-1 disease on occipitocervical ROM and cervical stability and lordosis. Our results converge with those of previous studies in proving that CVD with or without duraplasty is a low-risk procedure that is protective of the biomechanics of the cervical spine. More interestingly, our study shows that in severe cases of tonsillar herniation such as grade 3 CM-1, expansile duraplasty may provide some degree of restoration to the ROM while preserving cervical alignment and stability. This could relieve postoperative pain and may improve clinical prognosis.
4. Bondurant CP, Oro JJ. Spinal cord injury without radiographic abnormality and chiari malformation. J Neurosurg. 1993;79:833-838. 5. Elster AD, Chen MY. Chiari I malformations: Clinical and radiologic reappraisal. Radiology. 1992;183:347-353. 6. Ono A, Suetsuna F, Ueyama K, Yokoyama T, Aburakawa S, Takeuchi K, et al. Cervical spinal motion before and after surgery in patients with Chiari malformation type I associated with syringomyelia. J Neurosurg Spine. 2007;7:473-477.
7. Ranawat CS, O’Leary P, Pellicci P, Tsairis P, Marchisello P, Dorr L. Cervical spine fusion in rheumatoid arthritis. J Bone Joint Surg Am. 1979;61: 1003-1010. 8. Munshi I, Frim D, Stine-Reyes R, Weir BK, Hekmatpanah J, Brown F. Effects of posterior fossa decompression with and without duraplasty on chiari malformation-associated hydromyelia. Neurosurgery. 2000;46:1384-1389 [discussion: 1389-1390]. 9. Yundt KD, Park TS, Tantuwaya VS, Kaufman BA. Posterior fossa decompression without duraplasty in infants and young children for treatment of
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10. Sindou M, Chavez-Machuca J, Hashish H. Craniocervical decompression for chiari type I-malformation, adding extreme lateral foramen magnum opening and expansile duroplasty with arachnoid preservation. Technique and long-term functional results in 44 consecutive adult cases—comparison with literature data. Acta Neurochir (Wien). 2002; 144:1005-1019.
15. Ono A, Suetsuna F, Ueyama K, Yokoyama T, Aburakawa S, Numasawa T, et al. Surgical outcomes in adult patients with syringomyelia associated with chiari malformation type i: The relationship between scoliosis and neurological findings. J Neurosurg Spine. 2007;6:216-221.
21. White AA 3rd, Panjabi MM. The basic kinematics of the human spine. A review of past and current knowledge. Spine (Phila Pa 1976). 1978;3: 12-20.
11. Guyotat J, Bret P, Jouanneau E, Ricci AC, Lapras C. Syringomyelia associated with type I Chiari malformation. A 21-year retrospective study on 75 cases treated by foramen magnum decompression with a special emphasis on the value of tonsils resection. Acta Neurochir (Wien). 1998;140: 745-754. 12. Takeuchi K, Yokoyama T, Ito J, Wada K, Itabashi T, Toh S. Tonsillar herniation and the cervical spine: a morphometric study of 172 patients. J Orthop Sci. 2007;12:55-60. 13. Armonda RA, Citrin CM, Foley KT, Ellenbogen RG. Quantitative cine-mode magnetic resonance imaging of chiari I malformations: an analysis of cerebrospinal fluid dynamics. Neurosurgery. 1994;35:214-223 [discussion: 223-224]. 14. Pujol J, Roig C, Capdevila A, Pou A, MartiVilalta JL, Kulisevsky J, et al. Motion of the cerebellar tonsils in Chiari type I malformation
16. Ono A, Ueyama K, Okada A, Echigoya N, Yokoyama T, Harata S. Adult scoliosis in syringomyelia associated with Chiari I malformation. Spine (Phila Pa 1976). 2002;27:E23-E28. 17. Benzel EC, Lancon J, Kesterson L, Hadden T. Cervical laminectomy and dentate ligament section for cervical spondylotic myelopathy. J Spinal Disord. 1991;4:286-295. 18. Yonenobu K, Abumi K, Nagata K, Taketomi E, Ueyama K. Interobserver and intraobserver reliability of the Japanese orthopaedic association scoring system for evaluation of cervical compression myelopathy. Spine (Phila Pa 1976). 2001;26:1890-1894 [discussion: 1895]. 19. Hirabayashi K, Miyakawa J, Satomi K, Maruyama T, Wakano K. Operative results and postoperative progression of ossification among patients with ossification of cervical posterior longitudinal ligament. Spine (Phila Pa 1976). 1981;6: 354-364.
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22. Hou CR, Tsai LC, Cheng KF, Chung KC, Hong CZ. Immediate effects of various physical therapeutic modalities on cervical myofascial pain and trigger-point sensitivity. Arch Phys Med Rehabil. 2002;83:1406-1414. 23. Cassidy JD, Lopes AA, Yong-Hing K. The immediate effect of manipulation versus mobilization on pain and range of motion in the cervical spine: a randomized controlled trial. J Manipulative Physiol Ther. 1992;15:570-575.
Conflict of interest statement: The authors have no personal conflicts of interests to disclose. Received 2 September 2016; accepted 25 October 2016 Citation: World Neurosurg. (2017) 98:98-103. http://dx.doi.org/10.1016/j.wneu.2016.10.127 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
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