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The Spine Journal 17 (2017) 390–400

Clinical Study

Preoperative estimation of disc herniation recurrence after


microdiscectomy: predictive value of a multivariate model based on
radiographic parameters
Evgenii Belykh, MDa,b,c,1, Alexander V. Krutko, MD, PhDd,1, Evgenii S. Baykov, MD, PhDd,
Morgan B. Giers, PhDa,b, Mark C. Preul, MDa,b, Vadim A. Byvaltsev, MD, PhDa,c,e,*
a
Irkutsk Scientific Center of Surgery and Traumatology, Bortsov Revolyutsii str., 1, Irkutsk, 664003, Russia
b
Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W. Thomas Rd, Phoenix, AZ 85013, USA
c
Department of Neurosurgery, Irkutsk State Medical University, Krasnogo vosstaniya str., 1, Irkutsk, 664003, Russia
d
Neurosurgery Department No. 2, Novosibirsk Scientific Research Institute of Traumatology and Orthopedics, Frunze str., 17, Novosibirsk, 630091, Russia
e
Neurosurgery Department, Irkutsk Railway Clinical Hospital, Botkina str, 10, Irkutsk, 664005, Russia
Received 14 July 2016; revised 27 September 2016; accepted 12 October 2016

Abstract BACKGROUND CONTEXT: Recurrence of lumbar disc herniation (rLDH) is one of the unfa-
vorable outcomes after microdiscectomy. Prediction of the patient population with increased risk of
rLDH is important because patients may benefit from preventive measures or other surgical options.
PURPOSE: The study assessed preoperative factors associated with rLDH after microdiscectomy
and created a mathematical model for estimation of chances for rLDH.
STUDY DESIGN/SETTING: This is a retrospective case-control study.
PATIENT SAMPLE: The study includes patients who underwent microdiscectomy for LDH.
OUTCOME MEASURES: Lumbar disc herniation recurrence was determined using magnetic res-
onance imaging.
METHODS: The study included 350 patients with LDH and a minimum of 3 years of follow-up.
Patients underwent microdiscectomy for LDH at the L4–L5 and L5–S1 levels from 2008 to 2012.
Patients were divided into two groups to identify predictors of recurrence: those who developed rLDH
(n=50) within 3 years and those who did not develop rLDH (n=300) within the same follow-up period.
Multivariate analysis was performed using patient baseline clinical and radiography data. Non-
linear, multivariate, logistic regression analysis was used to build a predictive model.
RESULTS: Recurrence of LDH occurred within 1 to 48 months after microdiscectomy. Preopera-
tively, patients who developed rLDH were smokers (70% vs. 27%, p<.01; odds ratio [OR]=6.31, 95%
confidence interval [CI]: 3.27–12.16) and had higher body mass index (29.0±6.1 vs. 27.0±4.3, p=.03;
OR=1.09 per 0.01 unit change). Radiological parameters that were associated with rLDH were higher
disc height index (0.35±0.007 vs. 0.26±0.002, p<.001), higher segmental range of motion (9.8±0.28°
vs. 7.6±0.11°, p<.001; OR=0.53 per 0.01 unit change), and lower central angle of lumbar lordosis
(33.4±0.81° vs. 47.1±0.47°, p<.001; OR=0.53 per 0.01 unit change). Additionally, Pfirrmann grade

FDA device/drug status: Not applicable. Russian Science Foundation (F, Paid to the institution), pertaining to sub-
Author disclosures: EB: Grant: Russian Science Foundation (F, Paid to mitted manuscript.
the institution), pertaining to submitted manuscript. AVK: Grant: Russian The disclosure key can be found on the Table of Contents and at
Science Foundation (F, Paid to the institution), pertaining to submitted manu- www.TheSpineJournalOnline.com.
script. ESB: Grant: Russian Science Foundation (F, Paid to the institution), The authors have no relevant financial interests.
pertaining to submitted manuscript. MBG: Grant: Russian Science Foun- The study was performed with financial support from the Russian Science
dation (F, Paid to the institution), pertaining to submitted manuscript. MCP: Foundation, Grant No 15-15-30037.
Grant: Russian Science Foundation (F, Paid to the institution), pertaining * Corresponding author. Barrow Neurological Institute, St. Joseph’s
to submitted manuscript; Other: Barrow Neurological Foundation (F, Paid Hospital and Medical Center, c/o Neuroscience Publications, 350 W. Thomas
to the institution), Women’s Board of the Barrow Neurological Institute (E, Rd, Phoenix, AZ 85013, USA. Tel.: (602) 406-3593; fax: (602) 406-4104.
Paid to the institution), Newsome Family Endowment in Neurosurgery (E, E-mail address: Neuropub@dignityhealth.org (V.A. Byvaltsev)
1
Paid to the institution), pertaining to submitted manuscript. VAB: Grant: These authors contributed equally to this work.

http://dx.doi.org/10.1016/j.spinee.2016.10.011
1529-9430/© 2016 Elsevier Inc. All rights reserved.
E. Belykh et al. / The Spine Journal 17 (2017) 390–400 391

3 (OR=16.62, 95% CI: 8.10–34.11), protrusion type of LDH (OR=5.90, 95% CI: 3.06–11.36), and
Grogan sclerosis grades 3 and 4 (OR=4.81, 95% CI: 2.50–9.22) were also associated with rLDH.
Multivariate non-linear modeling allowed for more accurate prediction of rLDH (90% correct prediction
of rLDH; 99% correct prediction of no rLDH) than other univariate logit models.
CONCLUSIONS: Preoperative radiographic parameters in patients with LDH can be used to assess
the risk of recurrence after microdiscectomy. The multifactorial non-linear model provided more ac-
curate rLDH probability estimation than the univariate analyses. The software developed from this
model may be implemented during patient counseling or decision making when choosing the type
of primary surgery for LDH. © 2016 Elsevier Inc. All rights reserved.

Keywords: Complications; Intervertebral disc degeneration; Intervertebral disc displacement; Prevention; Radiography;
Statistics; Surgery

Introduction sible association with recurrence include developmental


abnormalities, extensive physical exercise, weight, smoking
Removal of lumbar disc herniation (LDH) is one of the [14], gender, age less than 35 years [15], stage of interver-
most frequent elective surgical procedures performed for de- tebral disc degeneration, segmental instability, herniation type,
generative lumbar spine lesions. However, because of the subligamentous disc herniation [15], intervertebral disc height,
constant presence of unsatisfying outcomes of open diabetes [14], disc protrusion [14], and others [16–18]. None-
discectomies, neither surgeons nor patients are truly satis- theless, some studies resulted in opposing conclusions
fied. Studies with long postoperative follow-up have shown concerning these risk factors. There is a relative paucity of
that almost 20% of patients develop postdiscectomy com- studies that assess preoperative radiological predictors of rLDH,
plications requiring at least one additional surgery [1–3]. The and no work, to our knowledge, that presents a predictive
10-year results of the Maine Lumbar Spine Study showed that
system that includes multiple radiological characteristics.
25% of patients required reoperation within a median time
Knowledge of the preoperative predictors of recurrence would
of 24 months after discectomy [4]. The spectrum of possi-
be of significant value in clinical decision making. In this study,
ble unfavorable outcomes includes the formation of epidural
we assessed the preoperative magnetic resonance imaging
fibrosis presenting with recurring radicular pain, postopera-
(MRI) and radiographic parameters and investigated their in-
tive instability of the spinal motion segment, reherniation in
fluence on LDH recurrence after discectomy. Furthermore,
the early postoperative period, and recurrence of LDH [5–7].
we created a calculator for estimating the probability of LDH
Reherniation is defined as a repeated LDH occurring within
recurrence.
the first 6 months after discectomy, whereas recurrence is
defined as occurring more than 6 months after discectomy
[8]. Recurrent disc herniation and reherniations are the most Materials and methods
common reasons for secondary surgery during the first 2 years
Study design
after discectomy, and the rate of reoperations is 15% to 25%
[9,10]. Moreover, revision surgery is usually more compli- The institutional ethics committee approved the study.
cated than the initial operation due to postoperative adhesions. We conducted a retrospective case-control study and ob-
The percentage of successful outcomes compared with primary tained information about the patients who underwent
surgery also decreases [11]. The 10-year results of the Maine discectomy from January 2008 to July 2012. Patients who
Lumbar Spine Study showed that only half (26 out of 51, 51%) developed rLDH that required reoperation within 3 years of
of the patients who underwent subsequent surgery were sat- follow-up after the primary surgery composed Group 1. We
isfied with their current state [4]. Additionally, after subsequent then randomly selected 300 patients (Group 2, control) who
surgeries, patients were less satisfied [12] and had worse dis- underwent discectomy during the same period and did not
ability and work outcomes [4]. Moreover, after the first develop rLDH within 3 years of follow-up. The control
reoperation, patients had a considerable 25% cumulative risk cohort was matched by the level of herniation (150 patients
for further spinal surgery [3]. Reherniation and LDH recur- with L4–L5 and 150 patients with L5–S1 LDHs) and pre-
rence are the most frequent conditions causing pain recurrence operative diagnosis.
and requiring subsequent surgical reoperation. The inclusion criteria for both groups were the follow-
Since the mid-1990s, research has primarily been focused ing: LDH at the L4–L5 or L5–S1 level, and single-level
on the detection of correlations between individual factors primary discectomy. The exclusion criteria for both groups
and recurrence of lumbar disc herniation (rLDH) after primary were the following: a combination of LDH with degenera-
surgical treatment. Investigation has shown that intraopera- tive stenosis of the spinal canal, degenerative or isthmic
tive findings and the degree of annular competence after spondylolisthesis, and traumatic lesions of the lumbar spine.
discectomy have a predictive value for reherniation and Patients with recurrence of pain due to stenosis of the spinal
reoperation [13]. Other factors that have been studied for pos- canal, segmental instability without reherniation, peridural fi-
392 E. Belykh et al. / The Spine Journal 17 (2017) 390–400

Table 1
Classification of Pfirrmann grade from magnetic resonance imaging [19]
Grade 1 Bright white, clearly defined nucleus pulposus, normal height
Grade 2 Bright with bands, clearly defined nucleus pulposus, normal
Context height
Grade 3 Gray, nucleus pulposus is not clearly defined, normal or
Recurrent disc herniation following treatment for lumbar minimally decreased height
radiculopathy is a known issue. At present, risk factors for Grade 4 Gray/black, no nucleus pulposus, normal to moderately
the development of this condition are not well under- decreased height
stood. The authors evaluated this using data from 350 Grade 5 Black, no nucleus pulposus visible, severely decreased height
patients treated at their center.
Contribution
Radiographic variables
Fifty patients were found to have a recurrent disc hernia-
tion. A multivariable model used by the authors identified Lumbar radiography (Definium 8000, General Electric
a number of significant predictors including smoking status, Medical Systems, Waukesha, WI, USA) was performed in the
Pfirrmann grade and BMI among others. neutral anteroposterior and neutral lateral planes with the
patient standing. Additionally, functional lumbar radio-
Implications
graphs were obtained at the maximal forward bending position
The findings should be interpreted in light of a low number
and maximal extension position. Disc height index (DHI), sag-
of recurrences and a statistical model that is likely overfit
ittal segmental range of motion (sROM), and the central angle
as a result. By standard convention, co-variates in a sta-
of lumbar lordosis were also assessed on plain lateral radio-
tistical model can be supported by every 20 patients with
graphs. Disc height index was defined as the quotient of the
the outcome of interest. At best then, given the low number
disc height to the height of the overlying vertebral body. Sag-
of recurrences in the authors’ cohort, only 2-3 variables
ittal segmental range of motion was defined as the difference
could really be supported in a multivariable model. The
between the segmental angles on lateral flexion and exten-
number of co-variates included may lead to spurious results
sion radiographs. The segmental angle was measured on plain
unique to the patients and significant only by chance. This
lateral radiographs as the angle between the adjacent end plates
directly impairs the translational capacity of these find-
of the diseased spinal level. The central angle of lumbar lor-
ings. The study design cannot account for patients lost to
dosis was measured on plain lateral radiographs using the Cobb
the system who may have sought care elsewhere for a re-
method [23] as the angle between the lines parallel to the su-
currence, nor can selection bias or preferential nonoperative
perior end plates of the L1 and S1 vertebrae. The presence
care be addressed. The evidence presented should be viewed
of retrolisthesis and lumbarization or sacralization of the lower
as Level IV as a result.
vertebrae was also recorded and assessed.
—The Editors
Statistical analysis

brosis, LDH at a different level, or contralateral rLDH were The statistical analysis was performed using SPSS 15.0
excluded from the analysis. (IBM Corp, Armonk, NY, USA) and Statistica 8.0 (StatSoft
The preoperative MRI and radiographic parameters of pa- Inc, Tulsa, OK, USA) software. Quantitative data are pre-
tients were assessed using data from the radiological archive sented as means and standard deviations. The non-
by two independent physicians who were blinded to the parametric Mann-Whitney U test and chi-square test were
outcome (recurrent LDH). Any disagreement in the grading used to perform comparisons between the groups. The
was discussed until a consensus was achieved. threshold level of statistical significance was set at p<.05.
Correlations among the variables were assessed using the
MRI variables Spearman coefficient (r). Multiple logistic regression anal-
ysis with the binomial (yes or no) dependent variable of
The stage of intervertebral disc degeneration was as- rLDH within 3 years was conducted using Statistica 13.0
sessed on preoperative T2-weighted MRIs (1.5T MRI, Hitachi (Dell Software, Aliso Viejo, CA, USA). All variables deter-
Ltd, Tokyo, Japan) using the Pfirrmann grading system mined to be significant by the Mann-Whitney U test and
(Table 1) [19]. Lumbar disc herniations were classified into chi-square test were used as variables in the model. The
three types—protrusions, extrusions, or sequestrations—as de- Wald statistic and p value for each variable were then used
scribed by Fardon and Milette [20]. Modic changes of vertebral as tests of significance of the regression coefficients in the
end plates and bone marrow of adjacent vertebrae were also model. All insignificant variables were removed. This was
assessed on T1-weighted and T2-weighted MRI scans [21]. done to ensure the model was not overparameterized. Finally,
Degeneration of the facet joint cartilage and the degree of sub- we developed a simple calculator in Microsoft Excel
chondral sclerosis of the facet joints were assessed as described (Redmond, WA, USA) that estimates LDH recurrence prob-
by Grogan et al. [22]. ability based on the defined preoperative variables.
E. Belykh et al. / The Spine Journal 17 (2017) 390–400 393

the 50 patients who developed rLDH composed Group 1. Re-


currence of lumbar disc herniation occurred from 1 to 48
(12.6±12.0) months after the primary surgery. Another 28 pa-
tients were excluded from the analysis: 6 patients developed
contralateral rLDH, 7 patients had postoperative instability
and peridural fibrosis, and 15 patients developed postoper-
ative stenosis at the level of surgery. The distribution of
reherniation according to the time after discectomy showed
several peaks, the first during the first 3 months, after 6 to
12 months, and then at about 20 months after the initial surgery
(Fig. 1). Comparative analysis of the subgroup of patients who
developed rLDH within 6 months after surgery and the sub-
group of patients who developed rLDH more than 6 months
after surgery showed no significant differences in all studied
variables (Supplementary Appendix S2). Three hundred pa-
tients from the pool of 1,290 who had 3 years of follow-up
Fig. 1. Timing of recurrent disc herniation in Group 1 patients (n=50). (The
figure is used with permission from Barrow Neurological Institute, Phoenix, without rLDH and who did not have exclusion criteria com-
Arizona.) posed the control group (Group 2).
The female-to-male ratio and mean age were compara-
ble in the groups of patients with and without rLDH. Patients
Results with rLDH had a significantly higher body mass index (BMI)
(p=.026). When the data on preoperative symptoms were com-
Patient characteristics
pared, we found significantly lower preoperative back (p<.001)
There were 1,368 discectomies performed at the L4–L5 and leg pain (p=.002) in the group of patients with rLDH,
and L5–S1 levels for patients with nerve root compression although this difference may not be clinically significant
caused by LDH from January 2008 through October 2012. (Table 2). Patients with rLDH had a mean preoperative
All patients had planned surgery for LDH with a history of Oswestry disability score of 51.8±17 comparable with the
at least 6 weeks of ineffective conservative treatment. Op- mean preoperative score of those without rLDH, 48.3±15.8,
erations were performed at the L4–L5 level in 57.7% (n=790) p=.09. The proportion of smokers was more than 2.5 times
and the L5–S1 level in 42.3% (n=578) of cases. Lumbar disc greater in the group of patients who developed rLDH (70%,
herniation removal was performed according to the Caspar 35 out of 50) compared with that in the non-recurrent group
open microdiscectomy technique described previously [24]. (27%, 81 out of 300) (p<.01), and the correlation with the
All operations were performed by neurosurgeons specializ- recurrence was r=.32 (p<.05). The average BMI was signifi-
ing in spinal surgery with significant experience in the cantly higher in the rLDH group (29.0±6.1 vs. 27.0±4.3,
technique. We identified 78 patients who required revision p=.03), but the correlation with recurrence was weak, r=.12,
surgery within the follow-up period of up to 3 years. Of these, p<.05. Of the patients’ preoperative parameters, smoking status

Table 2
Preoperative patient characteristics according to recurrence of lumbar disc herniation
Group 1 Group 2
All patients Recurrent disc herniation Without recurrent disc herniation p Value r Value†
No. of patients 350 50 300
Age (years) 42.6±11.8 (17–77) 43.6±7.9 (30–61) 42.5±12.3 (17–77) .34 .05
Gender ratio (M:F) 161:189 (46%:54%) 22:28 (44%:56%) 139:161 (46%:54%) .76 −.02
BMI (kg/m2) 27.3±4.7 (17.9–45.8) 29.0±6.1 (18.3–45.8) 27.0±4.3 (17.9–42.5) .03 .12*
Preoperative VAS score in back 3.8±1.2 (1–7) 3.1±1.1 (1–5) 3.9±1.2 (1–7) <.01 −.19*
Preoperative VAS score in leg 6.0±1.5 (3–9) 5.4±1.4 (3–8) 6.1±1.5 (3–9) <.01 −.16*
Patients with preoperative neurologic deficit 286 (82%) 40 (80%) 246 (82%) .73 −.02
Duration of pain before surgery (mo) 4.2±4.6 (1–60) 3.5±6.1 (1–11) 4.4±4.9 (1–60) .66 −.02
Patients with right-sided radicular symptoms 169 (48%) 20 (40%) 149 (49.6%) .20 −.07
Preoperative Oswestry score (points) 48.8±15.9 (12–96) 51.8±17 (12–96) 48.3±15.8 (24–88) .09 .09
Smoking (yes/no) 116 (33%) 35 (70%) 81 (27%) <.01 .34*
BMI, body mass index; SD, standard deviation; VAS, visual analog scale.
The data are presented as means±SD (range), n (%), or as absolute value (%) for binomial variables. p Values are calculated using the Mann-Whitney U
test and χ2 criteria for binomial variables.
* p<.05 for the corresponding r.

r=Spearman correlation coefficient of a variable with lumbar disc herniation recurrence.
394 E. Belykh et al. / The Spine Journal 17 (2017) 390–400

Table 3
Correlation of radiological parameters with rLDH by group
Group 1 Group 2
Recurrent disc herniation Without recurrent disc herniation p-Value r-Value†
Level of LDH .60 .02
L4–L5 23 150 (50%)
L5–S1 27 150 (50%)
DHI, mm (mean±SD) 0.35±0.007 0.26±0.002 <.001 .53*
sROM, degrees (mean±SD) 9.8±0.28 7.6±0.11 <.001 .36*
Central angle of lumbar lordosis, degrees (mean±SD) 33.4±0.81 47.1±0.47 <.001 −.53*
Modic changes .10 .09‡
Type 1 31 (62.0%) 37 (12.3%)
Type 2 5 (10.0%) 89 (29.7%)
None 14 (28.0%) 174 (58.0%)
Pfirrmann disc degeneration <.001 .49*
Grade 3 38 (76.0%) 48 (16.0%)
Grade 4 12 (24.0%) 252 (84.0%)
Herniation type <.001 .32*
Protrusion 35 (70.0%) 85 (28.3%)
Extrusion 13 (26.0%) 210 (70.0%)
Sequestration 2 (4.0%) 5 (1.7%)
Grogan subchondral sclerosis <.001 .27*
Grade II 15 (30.0%) 202 (67.3%)
Grade III 33 (66.0%) 92 (30.7%)
Grade IV 2 (4.0%) 6 (2.0%)
Grogan degeneration of joint cartilage <.001 .29*
Grade II 7 (14.0%) 169 (56.3%)
Grade III 33 (66.0%) 103 (34.3%)
Grade IV 10 (20.0%) 28 (9.4%)
Lumbarization 5 (10.0%) 3 (1.0%) <.001 .21*
Retrolisthesis 19 (38.0%) 34 (11.3%) <.001 .26*
DHI, disc height index; rLDH, recurrence of lumbar disc herniation; SD, standard deviation; sROM, sagittal segmental range of motion.
* p<.05 for the corresponding r.

r=Spearman correlation coefficient of a variable with LDH recurrence.

Spearman correlation is not significant; however, if the Modic change equals “none,” it is excluded from the analysis, Spearman r=−.48 and p<.05.

and BMI were included in the multivariate logistic regres- However, we decided to include this variable in the model
sion analysis. because it increased the correct prediction rate of the whole
model for rLDH (Fig. 2). Among the univariate models, the
Radiological parameters model with DHI as a single effect had the highest correct pre-
diction rate: 93.4% (327 out of 350) overall, 60% (30 out of
The results of comparisons of preoperative MRI and ra- 50) for the cases with rLDH, and 99.0% (297 out of 300) for
diographic parameters (LDH level, DHI, sROM, lordosis angle, the cases without rLDH (Fig. 3). The sagittal lumbar lordo-
Modic changes, Pfirrmann grade, herniation type, Grogan sis angle had a significant correlation with the DHI and was
grades, lumbarization, and retrospondylolisthesis) of the lumbar also a significant predictor of rLDH (Fig. 4).
spine are shown in Table 3. Correlation analysis showed that The resultant multiple non-linear logistic regression anal-
nine variables, namely DHI, sROM, the central angle of lumbar ysis yielded a mathematical model for rLDH chance estimation
lordosis, Pfirrmann grade, the type of herniation, Grogan scle- with overall 98% correct prediction rate (Table 5). The model
rosis grade, Grogan degeneration grade, lumbarization, and had the following form:
retrolisthesis, have significant correlations with the rLDH.
Grogan sclerosis and degeneration grades had significantly
high correlation (r=.76, p<.05) between each other. p=
(
exp β0 + ∑ j =1 β j x j
N
)
( )
exp β0 + ∑ j =1 β j x j +1
N

Multiple non-linear logistic regression model


where p is the probability, β0 is the intercept coefficient
For the multiple logistic regression analysis, we selected and β is the variable coefficient, and x is the variable
seven variables: BMI, DHI, sROM, the central angle of lumbar magnitude. Finally, the classification-of-case analysis showed
lordosis, smoking, LDH type, and Pfirrmann grade. The re- that the model was able to predict 45 out of 50 (90%) of re-
gression analysis showed that each variable was a significant currences and 298 out of 300 (99.3%) of cases without rLDH
predictor of rLDH with the exception of sROM (Table 4). correctly. The calculator for patient-specific rLDH probabil-
E. Belykh et al. / The Spine Journal 17 (2017) 390–400 395

Table 4
Estimation of parameters in multiple non-linear logistic regression analysis with modeled probability that recurrence equals either 1 (event occurred) or 0
(event did not occur) (distribution of dependent variable is binomial, linked function is logit)
Effect (x) Level of effect β Standard error Lower 95% CI Upper 95% CI Wald statistic p Value
Intercept – 17.03 (β0) 8.85 −0.32 34.38 3.70 .054
BMI – −0.47 0.16 −0.79 −0.15 8.42 <.01
DHI – −115.75 36.57 −187.43 −44.07 10.02 <.01
sROM – 0.70 0.40 −0.08 1.49 3.09 .079
Central angle of lumbar – 0.61 0.18 0.27 0.96 12.16 <.01
lordosis
Smoking No 2.39 0.84 0.75 4.03 8.16 <.01
LDH type Extrusion 3.57 1.30 1.01 6.12 7.50 <.01
LDH type Protrusion −0.90 0.88 −2.61 0.82 1.05 .306
Pfirrmann Grade 3 −1.82 0.72 −3.22 −0.41 6.42 <.01
BMI, body mass index; DHI, disc height index; sROM, sagittal segmental range of motion; LDH, lumbar disc herniation; CI, confidence interval.

ity was generated using Excel and can be found in patients underwent secondary spinal surgery [3]. After the sec-
Supplementary Appendix S1. ondary surgery, patients had a 25% cumulative risk of further
spinal surgery during the next 10 years [3]. Although our study
Discussion was not designed to study the overall incidence of rLDH, we
identified 50 out of 1,368 patients (3%) who developed LDH
Large population-based studies have demonstrated the risk recurrence at the L4–L5 and L5–S1 levels within the 3-year
of reoperation for LDH to be 10% to 15% [3,4]. A Finnish follow-up period. This rate is lower than the reported 15% to
study of 35,309 discectomy patients has shown that 14% of 20% of rLDH, possibly because we analyzed only cases of

Fig. 2. Graph of logistic regression analysis showing the sagittal, segmental range of motion as the independent variable, and recurrence as the binomial
(1—yes, 0—no), dependent variable. (The figure is used with permission from Barrow Neurological Institute, Phoenix, Arizona.)

Fig. 3. Graph of logistic regression analysis with the disc height index as the independent variable, and lumbar disc recurrence as the binomial (1—yes, 0—no),
dependent variable. (The figure is used with permission from Barrow Neurological Institute, Phoenix, Arizona.)
396 E. Belykh et al. / The Spine Journal 17 (2017) 390–400

Fig. 4. Graph of logistic regression analysis with the central angle of lumbar lordosis as the independent variable, and lumbar disc recurrence as the bino-
mial (1—yes, 0—no), dependent variable. (The figure is used with permission from Barrow Neurological Institute, Phoenix, Arizona.)

rLDH, but not all reoperations, and because some patients of 182 medical records of patients who underwent second-
with rLDH could have been missed on the long-term follow-up. ary operations and concluded that age was not a reliable
When assessing correlations of the variables with rLDH prognostic risk factor of rLDH; however, only 17 out of 98
in the subgroup of patients with early reherniations, we found (18%) male patients had a satisfactory long-term outcome com-
Spearman r values similar to the whole group of patients with pared with 12 out of 38 (32%) female patients, p<.05 [26].
rLDH, with the exception of BMI (Supplementary Dai et al. analyzed data from 39 patients who underwent
Appendix S2). Only when all patients were combined to- reoperation for rLDH and concluded that factors such as age,
gether did BMI have a significant, but low-powered, correlation gender, traumatic events, number of prior surgeries, level of
with recurrence. The BMI correlation with recurrence was herniation, side of recurrence, pain-free interval, duration of
insignificant in subgroups when assessed separately. Our results recurrent symptoms, walking capacity, and preoperative Jap-
suggest that subgroups of patients with early and late anese Orthopaedic Association score had no prognostic
reherniations after open microdiscectomy may have similar significance for rLDH [27]. Our study also did not reveal dif-
risk factors. ferences in patients’ age, gender, and side of herniation
between the groups of patients with and without rLDH. Al-
Non-modified patient risk factors though differences in preoperative visual analog scale scores
for leg and back pain were significant (p<.01 for both), the
Swartz and Trost reported that age, gender, smoking status, absolute clinical value of such differences is questionable.
the level of herniation, and duration of symptoms were not
associated with rLDH [7]. Based on the observations of 44 Smoking and BMI
pairs of homozygotic twins with a weight difference of more
than 8 kg, Videman et al. found that the cumulative load of Smoking has been proven to impair postoperative wound
larger body weight slightly delayed the process of disc de- repair in many surgical studies [28]. It is believed that toxic
generation [25]. Fritsch et al. conducted a retrospective analysis substances cause vasoconstriction and decrease nutrient supply

Table 5
Comparison of different models that estimate chances of recurrent lumbar disc herniation (rLDH) using Statistica software
Prediction based on the model
Model Odds ratio Lower 95% CI Higher 95% CI % Correct rLDH % Correct non-rLDH
Multiple logistic regression N/A N/A N/A 90.00 99.33
BMI (per 0.01 increase)‡ 1.09* N/A N/A 0 100.00
DHI (per 0.01 increase)‡ N/A* N/A N/A 60.00 99.00
sROM (per 1 degree increase)‡ 1.89* N/A N/A 20.00 99.33
Central angle of lumbar lordosis (per 1 degree increase)‡ 0.67* N/A N/A 56.00 96.33
Smoking (positive status) 6.31† 3.27 12.16 0 100.00
LDH type (protrusion) 5.90† 3.06 11.36 4.00 98.33
Pfirrmann (grade 3) 16.62† 8.10 34.11 76.00 84.00
BMI, body mass index; DHI, disc height index; sROM, sagittal segmental range of motion; LDH, lumbar disc herniation; CI, confidence interval; N/A,
not available.
* Odds ratio calculated using univariate logistic regression analysis.

Odds ratio calculated using free odds ratio calculator; % correct calculated using discriminant analysis (https://www.medcalc.org/calc/odds_ratio.php).

Logistic regression model.
E. Belykh et al. / The Spine Journal 17 (2017) 390–400 397

to the intervertebral disc, as well as diminish the activity of rLDH significantly correlates with the following param-
cellular tissue repair mechanisms [29]. Our study further sup- eters: DHI, Pfirrmann disc degeneration grade, type of
ports the existing data [30] that smoking is associated with a herniation, sROM, central angle of lumbar lordosis, and type
higher risk of rLDH. Nonetheless, we doubt that persistent I Modic changes of adjacent vertebral bodies.
smoking status, as a single predictor, would influence clin- The question of whether all patients would benefit from
ical decision making regarding a change of treatment tactics. preoperative flexion-extension lumbar spine radiography
However, we believe that in multivariable risk assessment, remains unanswered. Although it may be unnecessary in some
smoking status adds validity to the rLDH odds estimation. cases, we found this diagnostic method useful for our prac-
Obesity (BMI>30) was also shown to be an independent tice, as it may provide additional information about the
risk factor for rLDH after microdiscectomy [31]. Our study dynamic stability of the spinal segments.
also showed a weak but significant correlation (r=.12, p<.05)
between BMI and rLDH. This correlation is stronger (r=.23, Disc degeneration grade
p<.5) in the cohort of patients with BMI >30 than in the cohort The association of Pfirrmann grade with the risk of rLDH
with BMI ≤30. was previously suggested by Kim et al. [32] and confirmed
Cessation of smoking is frequently recommended before in our study. Only Pfirrmann grades 3 and 4 were recorded
surgery. However, the time required for the risks to de- in our study, and grade 3 had higher odds of recurrence than
crease to a level equivalent to the non-smoking population grade 4. Pfirrmann grade 4 is associated with disc collapse,
after smoking cessation is still unknown. The BMI, al- and such patients either had not presented with LDH or were
though alterable in the long term, is also difficult to change treated with fusion and were not included in our study.
before surgery. Pfirrmann grade 1 is roughly normal and is not characteris-
tic of LDH, whereas grade 2 discs have clear differentiation
between the nucleus and annulus with normal or slightly de-
Intraoperative variables
creased disc height. Our findings are in line with the
The risk for rLDH was shown to be significantly higher biomechanical model of LDH, where herniations were re-
in fragmented herniations with an annular defect (9 out of producibly created by cyclic loading in mildly degenerated
33, 27%), compared with the fragment or fissure (1 out of disc specimens but not in the moderately and severely de-
89, 1%), fragment contained (4 out of 42, 10%), or no frag- generated discs [33].
ment contained (2 out of 16, 12%) types of LDH [13].
Differences in intraoperative details of LDH removal in each Disc height and segmental range of motion
type of LDH result in the differences in the competence of The results of this study are aligned with the results of basic
the annulus. Such decreased annular competence leads to sig- biomechanical studies of LDH development [34,35]. In bio-
nificantly higher reherniation and reoperation rates for patients mechanical ex vivo models, LDH was produced by a highly
with larger annular defects. We have previously demon- compressive load at high flexion angles [34,35] due to the
strated that different microdiscectomy techniques lead to rupture of collagen fibers of the annulus at the site of attach-
variations in complication profiles and different risks for rLDH ment to the vertebral end plate [36]. End plate changes may
[8]. In the current study, LDHs were classified as protru- also contribute to decreased collagen fiber attachment to the
sion, extrusion, or fragmented herniations. Interestingly, our annulus and may explain the increased risk of rLDH. The study
study showed that the protrusion type of LDH is found more findings indicate that increased DHI and increased sROM are
often in the cohort of patients who develop rLDH (70%, 35 significant risk factors of rLDH. From the biomechanical point
out of 50) than in the control group (28%, 84 out of 300). of view, larger disc height before discectomy could lead to
The estimation of the size of the annular defect in different a higher disc height decrease after nucleus removal and in-
herniation types is beyond the scope of the current study. creased segmental mobility. DHI and sROM were significantly
correlated (r=.78, p<.05) in our study, confirming the bio-
Radiological variables mechanical link between these parameters. A decrease in disc
height could be observed as a naturally occurring process of
Kim et al. have examined the radiological risk factors for age and progression of degeneration. Restoration of disc height
rLDH after microdiscectomy at the L4–L5 levels in the great- is critical for foraminal decompression and overall sagittal
est detail [32]. The study revealed no significant correlation spinal alignment.
between the disc degeneration grade and recurrence. However,
the authors demonstrated that the incidence of rLDH was lower Lumbar lordosis
in discs with Pfirrmann degeneration grades I and II (1 out The angle of lumbar lordosis had an insignificant corre-
of 33, 3%) and VI (0 out of 13, 0%) than in discs with grades lation with sROM and low negative correlation with DHI
III, IV, and V (13 out of 111, 12%). According to this study, (r=−.17, p<.05). Lower lumbar lordosis, ie, flat lumbar spine,
factors that have significant correlation with rLDH include is associated with biomechanically suboptimal sagittal spinal
smoking, increased DHI, and increased segmental sROM [32]. alignment and distribution of body weight. A decrease in
Our study further reinforces these findings. We identified that lumbar lordosis significantly increases the risk of disc
398 E. Belykh et al. / The Spine Journal 17 (2017) 390–400

degeneration and primary LDH [37]. Our study also showed back of the case-control study design is the uncertainty about
a significant reduction of lumbar lordosis in the cohort of pa- the causation of the risk factors. Thus, we built our rLDH risk
tients with rLDH. This decrease in lumbar lordosis was calculator based on the assumption of the causality of the
associated with the protrusion type of LDH (r=−.25, p<.05) factors shown to be significantly different between the groups.
when all 350 patients were analyzed, although the power of Additionally, we assessed data from only 350 patients of
the correlation was weak and became insignificant in the sub- the entire cohort of 1,368 patients. All 50 patients with rLDH
group analysis. out of 78 who underwent reoperation were included in Group
1, whereas only 300 (out of 1,290) initially treated patients
Facet joint degeneration were included in Group 2. Such factors as availability of com-
Facet joint cartilage degeneration grade and cartilage scle- plete patient follow-up information and the necessity to
rosis grade correlated well with each other (r=.76, p<.05) but manually assess the images archived drove us to choose this
had a low-power correlation with rLDH (r=.29 and r=.27, re- study methodology. Such selection could lead to biases if the
spectively, p<.05). Both grades were significantly correlated selected patients are different from the general cohort of pa-
with sROM (r=.31 and r=.30, respectively, p<.05), confirm- tients without rLDH. We assume that random patient selection
ing the association of degenerative spinal instability with the decreased the chances for bias and that the 300 patients without
changes in the facet joints [38]. rLDH composed a representative control group. Also, this study
did not assess the difference in complication rates between
Multivariate logistic regression model the surgeons.
We performed a multivariate logistic regression analysis We did not assess patients who underwent discectomy at
to assess the odds of rLDH. The regression analysis allowed the L3–L4 level because there were no reherniations at this
us to identify a set of predictive factors that may play an in- level. Thus, our results should be extrapolated to the L3–L4
fluential role in the development of rLDH. Our study level with caution.
elaborated on a valuable clinical hypothesis that a risk for Studies that combine intraoperative factors such as annular
rLDH could be predicted from patient characteristics. The gen- defect size and the amount of disc material removed have been
eralized non-linear regression model was developed to aid in suggested, but the predictive values of such intraoperative pa-
quantitative odds estimation. Knowledge of the objective risk rameters can be determined only during surgery. There are
rate plays an essential role in deciding on the method and several drawbacks to intraoperative predictors. First, if in-
extent of surgical treatment for LDH during patient consul- traoperative parameters indicated a high risk of recurrence,
tation. If a high risk of rLDH is identified, the surgeon can the surgeon would not have much time to adjust or change
plan ahead for preventive methods and modify the surgical the surgical plan. Second, the intraoperative predictors could
procedure accordingly. For example, several approaches could not be known at the time of the preoperative patient counseling.
be considered to prevent rLDH in high-risk patients, such as Quantitative longitudinal parameters such as DHI, sROM,
lumbar fusion [39], annular repair [40], or implantable devices, and the central angle of lumbar lordosis could have
to close the annular defect [41]. interobserver differences between the studies. Further studies
The algorithm and rLDH risk calculator that was devel- should also be done to validate the interobserver and
oped allows for the preoperative assessment of the rLDH risk. intraobserver accuracy of such measurements.
We have implemented this scoring system in our practice and
believe that this system improves clinical decision making Conclusions
for patients with LDH. However, this model needs to be tested,
preferably in a multicenter, prospective, adequately powered Seven parameters were significant predictors of rLDH at
trial. The question of whether the use of this preoperative in- the level of the previous microdiscectomy: BMI, DHI,
formation could change how clinical care is delivered and hypermobility of the spinal motion segment, flattening of
whether it could decrease the incidence of rLDH remains lumbar lordosis, smoking, disc protrusion, and Pfirrmann grade
unanswered. III disc degeneration. The non-linear logistic regression model
we developed for the estimation of the chances of rLDH based
on the multivariate assessment of risk factors was signifi-
Study limitations
cantly more satisfactory than any single predictor model and
This study has several limitations. Our multiple logistic was able to predict 90% of rLDH correctly in the study. This
regression analysis did not include some relevant risk factors study further reinforces the evidence that preoperative ra-
that were identified as significant independent predictors in diological parameters can be used to predict the risk of rLDH
other studies. For example, we did not examine the size of after microdiscectomy. Surgeons could use this information
the annular defect. The association of large annular defects to advise patients of their risk for reherniation and as a premise
with rLDH was previously investigated elsewhere [13]. The for selective use of various approaches aimed to prevent re-
annular defect variable is typically assessed intraopera- currence, such as annulus suturing and barrier implants. Further
tively, and annulus repair strategies are implemented to studies are needed to evaluate the model with other sets of
decrease the risk of reherniation [40]. An inherent draw- patients.
E. Belykh et al. / The Spine Journal 17 (2017) 390–400 399

Acknowledgments [15] Yurac R, Zamorano JJ, Lira F, Valiente D, Ballesteros V, Urzua A. Risk
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