Download as pdf or txt
Download as pdf or txt
You are on page 1of 5

European Spine Journal

https://doi.org/10.1007/s00586-020-06656-5

ORIGINAL ARTICLE

The Haleem–Botchu classification: a novel CT‑based classification


for lumbar foraminal stenosis
S. Haleem1 · M. Malik2 · V. Guduri1 · C. Azzopardi1 · S. James1 · R. Botchu1

Received: 21 September 2020 / Revised: 21 October 2020 / Accepted: 1 November 2020


© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Purpose No clinical CT-based classification system is currently in use for lumbar foraminal stenosis. MRI scanners are not
easily available, are expensive and may be contraindicated in an increasing number of patients. This study aimed to propose
and evaluate the reproducibility of a novel CT-based classification for lumbar foraminal stenosis.
Materials and methods The grading was developed as four grades: normal foramen—Grade 0, anteroposterior (AP)/supero-
inferior (SI) (single plane) fat compression—Grade 1, both AP/SI compression (two planes) without distortion of nerve
root—Grade 2 and Grade 2 with distortion of nerve root—Grade 3.
A total of 800 lumbar foramen of a cohort of 100 random patients over the age of 60 who had undergone both CT and MRI
scans were reviewed by two radiologists independently to assess agreement of the novel CT classification against the MRI-
based grading system of Lee et al. Interobserver(n = 400) and intraobserver agreement(n = 160) was also evaluated. Agree-
ment analysis was performed using the weighted kappa statistic.
Results A total of 100 patients (M:F = 45:55) with a mean age of 68.5 years (range 60–83 years were included in the study.
The duration between CT and MRI scans was 98 days (range 0–540, SD—108). There was good correlation between CT
and MRI with kappa scores (k = 0.81) and intraobserver kappa of 0.89 and 0.98 for the two readers.
Conclusion The novel CT-based classification correlates well with the MRI grading system and can safely and accurately
replace it where required.

Keywords Lumbar foraminal stenosis · Novel classification system · Computed tomography · Magnetic resonance
imaging · Interobserver agreement · Intraobserver agreement

Introduction using either a partially quantitative system looking at fat


obliteration or a combination of various parameters (types
Lumbar foraminal stenosis (LFS) is an important cause for of stenosis, amount of fat obliteration and nerve root com-
radiculopathy of the lower limb (8–11%) with the foraminal pression) correlated with clinical findings [9–11]. To the
zone lying beneath the lamina and facet joints [1–4] (Fig. 1 authors’ knowledge, no computed tomography (CT)-based
Diagrammatic representation of classification showing anat- classification system is currently in clinical use.
omy of spinal unit and lumbar foramen). First described in While MRI is now available in many urban centres,
1927, it is recognised as the leading cause of failed back sur- it is still relatively scarce in rural areas and generally
gery (up to 60%) mostly because it is not recognised [5–8]. worldwide [12–17]. Data from the World Health Organi-
Various attempts have been made to classify LFS radiologi- sation (WHO) and Global Health Observatory (GHO)
cally mostly based on magnetic resonance imaging (MRI) show that MRI scanners are globally available but at only
0.00000–0.07000 units per million population in most areas
* S. Haleem while the minimum requirement to fully satisfy a popula-
shahnawaz.haleem@gmail.com tions needs are 12–15 units per million population [18–20].
It was felt therefore that there was a clinical need to develop
1
Royal Orthopaedic Hospital, The Woodlands, Bristol Road a CT-based classification system to overcome these hurdles,
South, Birmingham B31 2AP, UK
providing a common language linked to an easily available
2
Division of Medical Education, University of Brighton, resource and thus improve patient care. Furthermore, the
Brighton, UK

13
Vol.:(0123456789)
European Spine Journal

Fig. 2  CT and MRI (a and b) examples of Grade 0—L3 and L4


foramina, Grade 3—L5 foramen

Fig. 1  Diagrammatic representation of classification showing anat-


omy of spinal unit and lumbar foramen

classification system is of value when MRI is contraindi-


cated in patients with ferromagnetic foreign bodies such
as certain types of stents, pacemakers, implantable cardi-
overter-defibrillators(ICDs), nerve stimulators, intrauterine
contraceptive devices (IUCDs), cochlear implants, contact
lens and insulin pumps [21, 22].

Materials and methods

After discussions between senior authors, a novel CT-based


classification system was established after consensus was Fig. 3  CT and MRI (a and b) examples of Grade 1—L5 foramen
reached on clarity and appropriateness of a simplified clas-
sification. The grading was developed as four grades on
CT sagittal images as follows: normal foramen—Grade 0,
anteroposterior (AP)/superoinferior (SI) fat compression—
Grade 1, both AP/SI compression with no distortion of nerve
root—Grade 2, Grade 2 with additional distortion of nerve
root—Grade 3 (Fig. 2 CT and MRI (a & b) examples of
Grade 0—L3 and L4 foramina, Grade 3—L5 foramen, Fig. 3
CT and MRI (a & b) examples of Grade 1—L5 foramen
and Fig. 4 CT and MRI (a and b) examples of Grade 2—
L4 foramen). CT was performed on a 64 slice Somatom
AS, (Siemens, Germany) and MRI was on a 3 T Magnetom
Skyra (Seimens, Germany) MR and CT was analysed by two
experienced musculoskeletal radiologists. The foramen was
analysed on bone and soft tissue windows. The foramen on
MRI were assessed using the T1 and T2 weighted sagittal
sequences.
This novel CT classification was then assessed against the
MRI grading system proposed by Lee et al. and validated by Fig. 4  CT and MRI (a and b) examples of Grade 2—L4 foramen

13
European Spine Journal

Park et al. [10, 11]. A total of 800 foramen of the lumbar Table 2  Interobserver agreement for CT classification between
spine (Right and Left L2 to L5) of a cohort of a 100 random Reader 1 and Reader 2
patients referred for back and leg pain were independently Level of foramen Interobserver (k)
assessed by two fellowship trained radiologists to assess n = 400
correlation. This cohort of patients was above the age of
Right L2 0.79
60 years, and they had undergone both CT and MRI scans.
Right L3 0.63
Both readers analysed the CT and MRI scans and repeated
Right L4 0.43
the same after an interval of one week.
Right L5 0.66
Local research committee approval was obtained
Left L2 1.00
in the form of service evaluation (Project reference
Left L3 0.54
number—20–037).
Left L4 0.45
Left L5 0.59
Statistical analysis
All levels 0.58

Weighted kappa (k) statistic applying linear weighting was k weighted kappa value; n total number of foramina analysed
used to assess agreement. Agreement was analysed between
the CT and MRI scores for each Reader separately and
across both Readers combined. Interobserver agreement for near-perfect agreement for both Reader 1 (k = 0.89) and
each Reader of their first and second readings of the CT Reader 2 (k = 0.98) (Table 3).
studies (50 patients = 400 foramen) and intraobserver agree-
ment between the two readers for both CT and MRI were
also analysed (20 patients = 160 foramen). A kappa value Discussion
of ≤ 0 indicated no agreement, 0.01–0.20 indicated slight
agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate The lumbar foramen described as an oval, round or inverted
agreement; 0.61–0.80, substantial agreement; and 0.81 or teardrop-shaped “window” is also known as the “hid-
greater, nearly perfect agreement [23, 24]. Social Sciences den zone” [26, 27]. The intervertebral disc anteriorly, the
for Windows (version 24, SPSS) was used for statistical facet joint and articular process posteriorly, superior pedi-
analyses [25]. cle (roof) and inferior pedicle (floor) form the borders of
Results—100 patients (M:F = 45:55) with a mean age of the foramen [28]. Stenosis can occur in all of these direc-
68.5 years (range 60–83 years) were included in the study. tions causing neural compression. The concept of LFS was
The duration between CT and MRI scans was 98 days (range known previously as lateral spinal stenosis [29]. Realising
0–540, SD—108). the importance of not addressing LFS adequately subsequent
Kappa scores for both readers combined (k = 0.81) authors have attempted to quantify it numerically by using
revealed a near-perfect agreement (Table 1). Kappa scores MRI-based studies with Lee et al. proposing an MRI LFS
for interobserver analysis revealed moderate agreement grading system [10, 30–32].
(k = 0.58) (Table 2) and intraobserver analysis revealed

Table 1  Agreement between CT vs MRI classifications for Reader 1, Table 3  Intraobserver agreement for CT classifications at two differ-
Reader 2 and Combined ent time points for Reader 1 and Reader 2
Level of foramen Reader 1 (k) Reader 2 (k) Combined* (k) Level of foramen Reader 1 (k) Reader 2 (k)
n = 800 n = 400 n = 1200 n = 160 n = 160

Right L2 0.92 0.79 0.88 Right L2 0.84 1.00


Right L3 0.77 0.77 0.78 Right L3 0.78 1.00
Right L4 0.77 0.78 0.78 Right L4 0.72 1.00
Right L5 0.80 0.85 0.82 Right L5 0.96 1.00
Left L2 0.66 1.00 0.72 Left L2 1.00 0.66
Left L3 0.81 0.84 0.82 Left L3 0.77 0.82
Left L4 0.69 0.90 0.77 Left L4 0.96 1.00
Left L5 0.79 0.85 0.81 Left L5 0.85 1.00
All levels 0.80 0.85 0.81 All levels 0.89 0.98

k weighted kappa value; n total number of foramina analysed k weighted kappa value; n total number of foramina analysed

13
European Spine Journal

Our CT-based classification showed near-perfect agree- Author contributions SH contributed to original concept, discussed
ment when compared to the MRI grading system [23, 24]. framework, analysed data, wrote and critically reviewed article for
final acceptance. MM discussed framework, analysed data, critically
This implies that it can provide a reliable replacement for reviewed article for final acceptance. VG discussed framework and
reporting LFS. This aspect is important for a number of critically reviewed article for final acceptance. CA analysed scans and
reasons. data and critically reviewed article for final acceptance. SJ analysed
There are currently only approximately 50,000 MRI scan- scans and data, critically reviewed article for final acceptance. RB dis-
cussed framework, analysed data, wrote and critically reviewed article
ners in use worldwide with 5000 sold every year with most for final acceptance.
scanners being situated in urban centres of developed coun-
tries [20]. MRI scanners are limited by cost, lack of expertise Funding No funding was received in relation to this article.
and infrastructure in most developing nations. As an exam-
ple, the whole of Western Africa has only 84 MRI scanners Compliance with ethical standards
serving a population of 372 million, whereas Nigeria by
itself has 183 CT scanners [33, 34]. A CT-based grading Conflict of interest The authors declare no conflict of interest in rela-
would simplify reporting and allow a common language to tion to this article.
be utilised which would benefit patient care in these areas
of need.
Other drawbacks of MRI are the amount of time taken
per examination which would preclude it’s use in the trauma References
situation whereas the presence of CT-based classification for
1. Orita S, Inage K, Eguchi Y et al (2016) Lumbar foraminal steno-
LFS would obviate the need for further imaging to diagnose sis, the hidden stenosis including at L5/S1. Eur J OrthopSurgTrau-
any spinal cause for leg pain. 4% to 30% of patients report matol 26:685–693. https​://doi.org/10.1007/s0059​0-016-1806-7
anxiety related reactions with 3% to 15% of scans unable to 2. Porter RW, Hibbert CEC (1984) The natural history of root entrap-
ment syndrome. Spine 9:418–421 ((Phila Pa 1976))
be completed for the same reason [35–39]. The prevalence
3. Kunogi JHM (1991) Diagnosis and operative treatment of intra-
of claustrophobia amongst the population is increasingly foraminal and extraforaminal nerve root compression. Spine
necessitating the need for open MRI scanners [35, 38, 39]. 16:1312–1320 ((Phila Pa 1976))
Another important reason is the increasing utilisation of car- 4. Jenis LG, An HS (2000) Spine update: lumbar foraminal stenosis.
Spine 25:389–394 ((Phila Pa 1976))
diac and neural stimulation implants that prevent the use of
5. Putti V (1927) New conceptions in the pathogenesis of sci-
MRI scan in those patients [21, 22]. atic pain. Lancet 210:53–60. https​: //doi.org/10.1016/S0140​
While our study showed near perfect intraobserver agree- -6736(01)30667​-0
ment it revealed a moderate agreement in interobserver anal- 6. Mitchell C (1934) Lumbosacral facetectomy for relief of sciatic
pain. J Bone JtSurg Br 36-B:230–237
ysis [23, 24]. This could be due to user preference for the
7. Burton CV, Kirkaldy-Willis WH, Yong-Hing KHK (1981) Causes
choice of window settings or slice thickness which could of failure of surgery on the lumbar spine. ClinOrthopRelat Res
lead to a possible distortion in assessing foraminal diameters 157:183–187
and can be easily overcome by using standardised depart- 8. Jenis LG, An HSGR (2001) Foraminal stenosis of the lumbar
spine: a review of 65 surgical cases. Am J Orthop (Belle Mead
mental protocols [40].
NJ) 30:205–211
The limitations of our study are the use of the static CT 9. Wildermuth S, Zanetti M, Duewell S, Schmid MR, Romanow-
scan as dynamic changes are known to occur in extension ski B, Benini A, Böni T, Hodler J (1998) Lumbar spine: quan-
[41]. The well documented radiation hazards of CT scans titive and qualitative assessment of positional (upright flex-
ion and extension) MR imaging and myelography. Radiology
(increased incidence of cataracts, glaucoma, leukaemia
207:391–398
and brain tumours, etc.) as compared to MRI may limit its 10. Lee S, Lee JW, Yeom JS, Kim K-J, Kim H-J, SooKyo Chung
repeatability in a patient presenting with persistent/recurrent HSK (2010) A practical MRI grading system for lumbar foraminal
symptoms [42–48]. stenosis. AJR Am J Roentgenol 194:1095–1098
11. Park HJ, Kim SS, Lee SY, Park NH, Rho MH, Hong HP, Kwag
HJ, Kook SH, Choi SH (2012) Clinical correlation of a new MR
imaging method for assessing lumbar foraminal stenosis. Am J
Neuroradiol 33:818–822
Conclusion 12. No authors listed (2017) Geographical distribution of MRI—Fig-
ure 5: distribution of MRI units across Canada in 2017. In: Can.
Med. Imaging Invent. 2017. https:​ //www.cadth.​ ca/canadi​ an-medic​
Our study assessed bony stenosis, fat compression and nerve al-imagi​ng-inven​tory-2017. Accessed 20 Oct 2020
root distortion in grading LFS. There is perfect agreement 13. Matsumoto KS, Kashima S, Awai K (2015) Geographic distribu-
between the novel CT-based classification and the MRI tion of CT, MRI and PET devices in Japan: a longitudinal analysis
based on national census data. PLoS ONE 10:e0126036. https​://
grading system, indicating that it can safely and accurately
doi.org/10.1371/journ​al.pone.01260​36
replace the MRI grading system where required. 14. Khaliq AA, Deyo D, Duszak R Jr (2015) The impact of hospital
characteristics on the availability of radiology services at critical

13
European Spine Journal

access hospitals. J Am CollRadiol 12:1351–1356. https​://doi. 34. Adejoh T, Onwujekwe EC, Abba M et al (2018) Computed tomog-
org/10.1016/j.jacr.2015.09.008 raphy scanner census and adult head dose in Nigeria. Egypt J
15. Ginde AA, Foianini A, Renner DM et al (2008) Availability and RadiolNucl Med 49:66–70. https ​ : //doi.org/10.1016/j.ejrnm​
quality of computed tomography and magnetic resonance imag- .2017.09.001
ing equipment in U.S. emergency departments. AcadEmerg Med 35. Hricak H, Amparo EG (1984) Body MRI: alleviation of claus-
15:780–783. https​://doi.org/10.1111/j.1553-2712.2008.00192​.x trophobia by prone positioning. Radiology 152:819. https​://doi.
16. No Authors Listed (2011) Pakistan country report. In: org/10.1148/radio​logy.152.3.64632​67
RAD-AID-Pakistan-health-care-radiology-report 36. Quirk ME, Letendre AJ, Ciottone RA, Lingley JF (1989) Anxiety
17. Moser JW (2008) 2007 Survey of radiologists: practice charac- in patients undergoing MR imaging. Med Dosim 14:294. https​://
teristics, ownership, and affiliation with imaging centers. J Am doi.org/10.1016/0958-3947(89)90021​-6
CollRadiol 5:965–971. https​://doi.org/10.1016/j.jacr.2008.03.011 37. Meléndez JC, Mccrank E (1993) Anxiety-related reactions
18. No authors listed (2014) Medical equipment: magnetic resonance associated with magnetic resonance imaging examinations.
imaging (MRI) units per million population. In: World Heal. JAMA J Am Med Assoc 270:745–747. https​://doi.org/10.1001/
Organ. https​://www.who.int/diagn​ostic​_imagi​ng/colla​borat​ion/ jama.1993.03510​06009​1039
mripe​rmill​_14.jpg?ua=1. Accessed 20 Oct 2020 38. Katznelson R, Djaiani GN, Minkovich L et al (2008) Prevalence
19. No authors listed (2016) Global health observatory data reposi- of claustrophobia and magnetic resonance imaging after coronary
tory—Medical equipment—Data by country. In: World Heal. artery bypass graft surgery. Neuropsychiatr Dis Treat 4:487–493.
Organ. https​://apps.who.int/gho/data/node.main.510. Accessed https​://doi.org/10.2147/ndt.s2699​
20 Oct 2020 39. Koh SAS, Lee W, Rahmat R et al (2017) Interethnic variation in
20. Rinck PA (2020) 21–02 How many MRI machines are there?— the prevalence of claustrophobia during MRI at Singapore general
MR imaging: facts and figures. In: Rinck PA (ed) Magnetic reso- hospital: does a wider bore MR scanner help? ProcSingapHealthc
nance in medicine a critical introduction, 12th edn. BoD, Ger- 26:1–5. https​://doi.org/10.1177/20101​05817​69581​9
many, p 432 40. Beers GJ, Carter AP, Leiter BE et al (1985) Interobserver discrep-
21. Dill T (2008) Contraindications to magnetic resonance imaging. ancies in distance measurements from lumbar spine CT scans. Am
Heart 94:943–948. https​://doi.org/10.1136/hrt.2007.12503​9 J Roentgenol 144:395–398. https​://doi.org/10.2214/ajr.144.2.395
22. Shellock FG, Crues JV (2004) MR procedures: biologic effects, 41. Mayoux-Benhamou MA, Revel M, Aaron C et al (1989) A mor-
safety, and patient care. Radiology 232:635–652 phometric study of the lumbar foramen—Influence of flexion-
23. Cohen J (1968) Weighted kappa: nominal scale agreement pro- extension movements and of isolated disc collapse. SurgRadiolA-
vision for scaled disagreement or partial credit. Psychol Bull nat 11:97–102. https​://doi.org/10.1007/BF020​96463​
70:213–220. https​://doi.org/10.1037/h0026​256 42. No authors listed (2019) Radiation dose in X-ray and CT exams.
24. McHugh ML (2012) Lessons in biostatistics Interrater reliability: In: RadiologyInfo.org. https​://www.radio​logyi​nfo.org/en/info.
the kappa statistic. BiochemMedica 22:276–282 cfm?pg=safet​y-xray. Accessed 20 Oct 2020
25. SPSS version 24, SPSS Inc, Chicago, Illinois U SPSS version 24 43. de Gonzalez AB, Mahesh M, Kim K-P et al (2009) Projected
26. Stephens M, Evans J, O’Brien J (1991) Lumbar intervertebral cancer risks from computed tomographic scans performed in the
foramens: an in vitro study of their shape in relation to interver- United States in 2007. Arch Intern Med 169:2071–2077. https​://
tebral disc pathology. Spine 16:525–529 ((Phila Pa 1976)) doi.org/10.1016/j.physb​eh.2017.03.040
27. Macnab I (1971) Negative disc exploration: an analysis of the 44. Smith-Bindman R, Lipson J, Marcus R et al (2009) Radiation dose
causes of nerve-root involvement in sixty-eight patients. J Bone associated with common computed tomography examinations and
JtSurg Am 53:891–903 the associated lifetime attributable risk of cancer. Arch Intern Med
28. Mandell JC, Czuczman GJ, Gaviola GC et al (2017) The lumbar 169:2078–2086. https:​ //doi.org/10.1001/archin​ ternm​ ed.2009.427.
neural foramen and transforaminal epidural steroid injections: an Radia​tion
anatomic review with key safety considerations in planning the 45. Pearce MS, Salotti JA, Little MP et al (2012) Radiation exposure
percutaneous approach. Am J Roentgenol 209:W26–W35. https​ from CT scans in childhood and subsequent risk of leukaemia and
://doi.org/10.2214/AJR.16.17471​ brain tumours: a retrospective cohort study. Lancet 380:499–505.
29. Arnoldi CC, Brodsky AE, Cauchoix J et al (1976) Lumbar spi- https​://doi.org/10.1016/S0140​-6736(12)60815​-0
nal stenosis and nerve root entrapment syndromes. Definition 46. Lin EC (2010) Radiation risk from medical imaging. Mayo Clin-
and classification. ClinOrthopRelat Res 115:4–5. https​://doi. Proc 85:1142–1146. https​://doi.org/10.4065/mcp.2010.0260
org/10.1097/00003​086-19760​3000-00002​ 47. Sagerman RH (1993) Radiation-induced cataracts: simple but dif-
30. Hasegawa T, An HS, Haughton VM (1993) Imaging anatomy ficultto quantify. Int J RadiatOncolBiolPhys 26:713–714
of the lateral lumbar spinal canal. Semin Ultrasound, CT, MRI 48. Takeda A, Shigematsu N, Suzuki S et al (1999) Late retinal com-
14:404–413. https​://doi.org/10.1016/S0887​-2171(05)80034​-4 plications of radiation therapy for nasal and paranasal malignan-
31. Aota Y, Niwa T, Yoshikawa K et al (2007) Magnetic resonance cies: relationship between irradiated-dose area and severity. Int J
imaging and magnetic resonance myelography in the presurgical RadiatOncolBiolPhys 44:599–605
diagnosis of lumbar foraminal stenosis. Spine 32:896–903. https:​ //
doi.org/10.1097/01.brs.00002​59809​.75760​.d5 ((Phila Pa 1976)) Publisher’s Note Springer Nature remains neutral with regard to
32. Eguchi Y, Ohtori S, Suzuki M et al (2016) Diagnosis of lumbar jurisdictional claims in published maps and institutional affiliations.
foraminal stenosis using diffusion tensor imaging. Asian Spine J
10:164–169. https​://doi.org/10.4184/asj.2016.10.1.164
33. Ogbole GI, Adeyomoye AO, Badu-Peprah A et al (2018) Survey
of magnetic resonance imaging availability in West Africa. Pan
Afr Med J 30:240

13

You might also like