Review article 389
Stiffness of various pin configurations for pediatric supracondylar humeral fracture: a systematic review on biomechanical studies Tony Lin-wei Chena, Chang-qiang Hea, Ting-qu Zhenga, Yan-qun Ganb, Ming-xiang Huanga, Yan-dong Zhengb and Jing-tao Zhaob To compare the biomechanical stability of various pin configurations for pediatric supracondylar humeral fractures under varus, internal rotation, and extension conditions. After electronic retrieval, 11 biomechanical studies were included. Stiffness values of pin configurations under different loading conditions were extracted and pooled. There were no statistically significant differences between two cross pins and two divergent lateral pins on the basis of the ‘Hamdi method’ (P = 0.249− 0.737). An additional pin did not strengthen two-pin construct (P = 0.124− 0.367), but better stabilized fractures with medial comminution (P < 0.01). Isolated lateral pins are preferable because of a better balance of a lower risk of nerve injury and comparable fixation strength. Limitations such as differences in experimental setup among recruited
studies and small sample size may compromise the methodologic power of this study. J Pediatr Orthop B 24:389–399 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
the development of cubitus varus and interfere with function recovery. A most recent meta-analysis basic on randomized controlled trials (RCT) reported that the risk of ulnar nerve injury was greater with cross pins [17]. However, the outcomes also indicated that there were no significant difference between the two major pin configurations in terms of radiographic outcomes, range of motion, and even postoperative life quality. It seems like there is a discrepancy in the findings between biomechanical studies and clinic trials.
Pediatric supracondylar humeral fracture (PSHF) is one of the most common elbow traumas. It has been reported that PSHF accounted for 10% of all fractures in children [1] and 75% for elbow fractures [2,3]. For years, a large volume of literatures on PSHF was published. Concepts of treatment evolved rapidly. Consensus has been achieved among orthopedic surgeons that displaced PSHF was best treated by close/open reduction and pin fixation [1,3–5]. However, controversy persists on the optimal pin configuration. The issue has been discussed both clinically and experimentally, and a solution remains pending. Generally, optimal pin configuration was predominantly determined by balancing the risk of iatrogenic ulnar nerve injury and preservation of adequate fracture stability from the fixation [3,4,6–8]. Cross pins and isolated lateral pins are presently the mainstream pin configurations for displaced PSHF. One general consensus among orthopedic surgeons was that cross pin had the advantage of superior fixation stiffness and the shortcoming of compromising neural function of the ulnar nerve. Using isolated lateral entry can avoid nerve injury while, as what was indicated in previous study, the construct may be relatively less biomechanical stable [9–16]. As the most direct consequence of inadequate stability is redisplacement and loss of reduction, the lateral entry pin technique was constantly assumed to be more likely to lead to 1060-152X Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Journal of Pediatric Orthopaedics B 2015, 24:389–399 Keywords: biomechanical study, supracondylar humeral fracture, systematic review a The First Clinical Medical College, Guangzhou University of Chinese Medicine and bThe First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, Guangdong, People’s Republic of China
Correspondence to Jing-tao Zhao, MD, Department of Orthopedics, First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, No. 16 Ji Chang Road, Baiyun District, Guangzhou, Guangdong 510405, People’s Republic of China Tel: +86 13922182520; e-mail: [email protected]
It was well recognized that cubitus varus consisted of deformities in three planes (varus, extension, and internal rotation) [18,19]. Efforts have been made in several in-vitro studies to compare the triplanar mechanical properties of different pin configurations. They were quite similar in methodology and design. Nevertheless, outcomes are inconsistent throughout these biomechanical studies. Whether isolated lateral pins yield inferior stability than cross pins in the aforementioned three directions remains uncertain. Therefore, we performed this systematic review aiming to compare the biomechanical stability of various pin configurations for PSHF under varus, internal rotation, and extension conditions. Pin configurations differed in (a) placement, (b) number, (c) start points, and (d) size. We hypothesized that (a) there was no significant difference in the triplanar stability between two cross pins DOI: 10.1097/BPB.0000000000000196
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
and isolated two lateral pins; (b) one additional lateral pin for the two-pin construct could enhance fixation stiffness; and (c) pin configuration with wider separation in the distal diaphysis region or with a larger size was mechanically more stable.
Method Search strategy
An electronic search of eight databases (Pubmed, EBSCO, Ovid Medline, Embase, Wiley, Proquest, Cochrane Central and China Biomedical literature database) was performed in our study. During the process, several characteristics such as study subject, intervention, and publish type were identified. Key words including ‘supracondylar’, ‘pin’, ‘Kirschner wire’, ‘biomechanical,’ and ‘vitro’ were used in retrieval. No restriction for language or publish period was applied. References from papers that were potentially considered included were also reviewed for extra information. Criteria
The literature screen was performed by two authors of this study (T.L.C. and C.Q.H.). Any disagreements in including results were settled by group discussion involving a third party who was blinded to the recruitment process. The inclusion criteria were as follows. (a) Type of study: only biomechanical studies on the stiffness of different pin configurations were included. Articles were accessible for full text and provided complete data; (b) material: cadaveric bone or synthetic composite humeri; (c) intervention: loading tests including varus, extension or internal rotation; (d) measurement: stiffness value, data provided in the form of displacement and load were also available; (e) fracture mode: simple fracture with the fracture line extended through the middle of the olecranon fossa (roughly 25–30 cm above the distal articular surface); and (f) pins: 1.5/1.6 mm Kirshner wires or pins with a larger size. Assessment of risk of bias
Two authors (J.T.Z. and T.Q.Z.) independently assessed the methodologic quality of the included studies. Although biomechanical study is not typical RCT, the research process is quite similar. Therefore, assessment of risk of bias for each included paper was performed using the Cochrane Collaboration ‘Risk of bias’ assessment tool. Any disagreement was resolved by discussion to reach a consensus. Data collection and analysis
Data were extracted by two authors (Y.G.G. and M.X.H.) separately using a piloted form. Basic information on the characteristics for each enrolled studies in terms of sample size, study subject, pin configuration, Kirschner wire size, and loading mode were recorded. We contacted the
investigators for details of original research when it was necessary. Data pooling was performed by two authors (T.L.C. and C.Q.H.) using Comprehensive Meta Analysis (version 2.2.064; Biostat Inc., Englewood, New Jersey, USA). In this study, the stiffness value was the sole variable, and a continuous variable as well. Therefore, the weighted mean difference and 95% confidence interval (CI) were calculated for each comparison. χ2 and I2 were tested to examine heterogeneity; an I2 value greater than 75% was considered to indicate a high level of heterogeneity, greater than 50% and less than 75% was considered to indicate a medium level, greater than 25% and less than 50% was considered to indicate a low level, and less than 25% barely exists. A random-effects model was utilized when a high level of heterogeneity was found. When there was medium level of heterogeneity, effects model was selected depending on specific conditions by discussion among the authors (T.L.C., J.T.Z., and Y.D.Z.). If possible, publication bias was assessed by constructing a funnel plot when the studies included were no fewer than 6 and meta-regression analysis was carried out when the number of studies included was no smaller than 10. Sensitivity analysis was also carried out to rule out studies with potentially considerable heterogeneity.
Results Article screening
After title and abstract screening, altogether, 13 articles were identified and all the full texts were obtained (Fig. 1). There was a good agreement among the reviewers in article selection as shown by a κ value of 0.75 (u = 3.20, P < 0.01). Recruitment of one study required further discussions involving the third party and consensus was eventually reached because the paper fulfilled the overall inclusion criteria considerably [20]. Two of the 13 studies were excluded because one used plastic materials as the study subject and another one used canine humeri [7,21]. Of the 11 studies included [13–15, 20,22–28], two used cadaveric bone [13,20] and nine used synthetic humeri [14,15,22–28]. Five studies repeatedly tested one specimen for different pin configurations [14, 15,24,25,27]. There were a total of 314 specimens, 12 kinds of pin configurations, three pin sizes, and five loading modes. The characteristics of all the studies included are shown in Table 1. All items are primarily identified according to authors’ descriptions. Unspecific details were supplemented by observing diagrams or radiographic images provided in the articles. For those addressing isolated lateral pin configurations, differences in the starting points of placement were identified and thus the groups were subdivided into two subgroups: ‘Hamdi’ and ‘capitellar’. The term ‘Hamdi’s method’ was used widely to refer to a group of lateral starting point techniques after Hamdi’s study and was generally characterized as ‘a direct lateral, extra-articular starting point,
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Review on supracondylar humeral fracture Chen et al. 391
Fig. 1
Computerized search of 8 database Studies identified (N = 309)
Duplication removed (N = 116)
Studies included with titles and abstracts (N = 193) Excluded for not meeting inclusion criteria (N = 180) Full-text articles assessed for eligibility (N = 13)
Excluded Plastic material (N = 1) Canine humeri (N = 1) Studies for meta-analysis (N = 11)
Flow diagram of the search and screening process of studies.
almost directly on the lateral epicondyle’ [24], whereas a ‘capitellar’ starting point was previously described as ‘the pin engaged the capitellum with a para-olecranon starting point’ [5,27]. The distal pin was suggested to cross the fracture site at the medial edge of the coronoid fossa in ‘Hamdi’s method’ [24] and placed as close to the midline as possible in the ‘capitellar’ method [27]. Studies that were published earlier before these definitions were commonly raised and used were categorized according to the procedure descriptions, schematic, and radiographs provided in the original articles. As a result, the study by Bloom et al. [23] was assigned to the ‘Hamdi’ group. The studies by Lee et al. [14] and Larson et al. [22] were assigned to the ‘capitellar’ group. The study by Zionts et al. [13] did not fall into any of the two categories and was thus addressed separately. Except for information in the table, Silva et al. [28] and Larson et al. [22] set fractures with medial comminution as control groups. Silva et al. [28] also recruited two divergent lateral pin configurations that had different pin spread at the fracture site. Wang et al. [15] and Feng et al. [25] stimulated fractures with oblique fracture lines that were considered simple fractures in this study and recruited in data pooling.
Larson et al. [22] investigated fractures with residual displacements. Zionts et al. [13] unequally assigned specimens to different groups and drilled in lateral pins in patterns that differed from all the other studies. Gottschalk et al. [27] did not specify the grouping method in their study. On the basis of the instructions in the method section, we believed that the authors divided the totaled 20 specimens into two major groups according to the lateral entry start point and 10 specimens in each group were repeatedly used throughout all subgroups. Other than the anatomically reduced group, Bloom et al. [23] also investigated specimens with residual displacement of 20° internal rotation. In Table 1, information on loading conditions indicated that the cycle was quite different between studies and five of these studies [13, 14,25,28] did not clarify this part in the article. Conversely, the loading rate was consistent throughout these researches. The values 0.5 degree/s and 0.5 mm/s seem to be uniform for the biomechanical test. Methodological quality of the studies included
Table 2 shows the result of assessment of the quality of the studies. ‘unknown’ was assigned to ‘blinding’ for all
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Varus, valgus, extension, internal, external
Internal
1.6 mm
1.6 mm
Unclear
Internal 1.6 mm
0.5 degree/s 0.5 mm/s Unclear
Varus, valgus, extension, internal, external 1.6 mm
Unclear
Varus, valgus, extension, internal, external 1.6 mm
Unclear
Unclear Varus, valgus, extension, internal, external
3 cycles
10 cycles Extension
10 cycles
0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 3 degree/s
2 cycles Varus, valgus, extension, internal, external
1.6 mm 2.0 mm 1.6 mm 2.8 mm 1.6 mm
5 cycles Varus, valgus, extension 1.6 mm
0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 0.5 degree/s Unclear Varus, internal 1.6 mm
1 degree/s Internal 2.0 mm
posterior and 1 lateral, 2 divergent lateral (capitellar) lateral and 1 medial divergent lateral (capitellar), 2 parallel lateral divergent lateral (capitellar), 2 parallel lateral and 1 medial divergent lateral (Hamdi), 1 lateral and 1 medial divergent medial divergent lateral (capitellar and Hamdi) divergent lateral (capitellar and Hamdi) divergent lateral (Hamdi), 2 divergent lateral (Hamdi) divergent lateral and 1 medial, 1 lateral and 1 medial divergent lateral (Hamdi), 2 divergent lateral (Hamdi) lateral and 1 medial parallel lateral divergent lateral (the two pins varied in degrees of divergence) divergent lateral (Hamdi), 2 divergent lateral (Hamdi) divergent lateral and 1 medial, 1 lateral and 1 medial divergent lateral (capitellar), 2 divergent lateral (capitellar) divergent lateral and 1 medial, 1 lateral and 1 medial parallel lateral, 2 divergent lateral (Hamdi) lateral and 1 medial divergent lateral, 2 divergent lateral parallel lateral, 1 lateral and 1 medial
5 cycles
studies because none of them provided adequate information indicating whether assessors were blind to the test procedure or not. For studies carried out on cadaveric bone, Zionts et al. [13] reported randomly dividing the specimens but did not mention a specific randomization method. Besides, only three specimens were assigned to two lateral crossed pins because of ‘minimum stability’. We thus assigned ‘unknown’ to ‘selective report’. Of those using synthetic humeri, five studies that performed repeated tests on a single specimen all reported using a randomized testing order without stating the randomization method used. Srikumaran et al. [26] did not provide details on the guiding device that normalized the cutting procedure. ‘Randomization’ for these studies was thus assigned as ‘unknown’ and so was ‘allocation concealment’. The results of assessment indicated that the average methodological quality of the studies included was just fair. Potential experimental heterogeneity may affect pooling outcomes. Two pins versus two pins (1.6 mm) One medial and one lateral versus two divergent lateral pins (Hamdi)
Indicates that a single specimen was used repeatedly.
Zionts et al. [13]
Lee et al. [14]
Larson et al. [22]
Bloom et al. [23]
Hamdi et al. [24]
Feng et al. [25]
Srikumaran et al. [26]
Gottschalk et al. [27]
Wang et al. [15]
a
Cadaveric bone
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri Silva et al. [28]
Cadaveric bone
30 3g×5 36 6g×6 9a 1g×9 20a 2 g × 10 48 6g×8 9a 1×9 12a 1 g × 12 64 8g×8 40 8g×5 9a 1×9 37 Unequal assign Marsland and Belkoff [20]
Subject Sample References
Table 1
Characteristics of the studies included
1 1 3 2 2 2 3 2 3 2 3 1 2 2 3 2 3 2 2 1 3 2
Cycle Loading Mode Pin size Pin configuration
Loading rate
392 Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
There were four studies comparing two cross and two divergent lateral pins following Hamdi’s method [14,15, 23,25]. The study by Srikumaran et al. [26] was not included because it measured torque by rotating the distal fragment in the extension test and the data could not be used in pooling. Bloom’s study investigated both anatomical reduced and malreduced specimens and data were extracted solely from the former. The test for heterogeneity showed that I2 values for varus, internal rotation, and extension were all greater than 50%, which indicated the existence of heterogeneity between studies. As subgroups and meta-regression analysis could not be carried out, a random-effects model was used. The data pooled showed no statistically significant differences between the two groups in the three tests (standard mean: − 1.190; 95% CI: − 3.211 to 0.832; P = 0.249, standard mean: − 0.901; 95% CI: − 3.749 to 1.947; P = 0.535, standard mean: − 0.296; 95% CI: − 2.025 to 1.433; P = 0.737). According to the forest plot (Fig. 2), although the pooled data did not yield statistical significance, a slightly greater resistant strength of the cross pin configuration consistently existed. Besides, the outcomes of the study by Srikumaran et al. [26] also supported that cross pins were more stable in sagittal extensional rotation. One medial and one lateral versus two divergent lateral pins (capitellar)
Two studies compared cross pins with two divergent lateral pins utilizing a capitellar starting point [20,22]. Data pooling could not be implemented because of the presence of high heterogeneity (I2 = 96.663%) and the number of studies was small. In their study on cadaveric bone, Marsland and Belkoff [20] found no significant
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Review on supracondylar humeral fracture Chen et al. 393
Table 2
Assessment of methodologic quality
Title Marsland and Belkoff [20] Silva et al. [28] Wang et al. [15] Gottschalk et al. [27] Srikumaran et al. [26] Feng et al. [25] Hamdi et al. [24] Bloom et al. [23] Larson et al. [22] Lee et al. [14] Zionts et al. [13]
Randomization
Allocation concealment
Blinding
Incomplete outcome
Selective reporting
L L U U U U U L L U U
U L U U L U U L L U U
U U U U U U U U U U U
L L L L L L L L L L L
L L L L L L L L L L U
L, low risk of bias; U, unclear.
Fig. 2
References
Standard difference in means and 95% CI
Statistics for each study
Outcome Standard difference in means −3.535 0.415 0.839 −2.761 −1.190
Lower Upper SE Variance limit limit Z-value P-value 0.800 0.641 −5.104 −1.967 −4.417 0.000 0.476 0.227 −0.519 1.349 0.871 0.384 0.492 0.242 −0.124 1.803 1.707 0.088 0.659 0.434 −4.052 −1.470 −4.191 0.000 1.031 1.064 −3.211 0.832 −1.154 0.249
Bloom et al. [23] Feng et al. [25] Lee et al. [14] Wang et al. [15]
Varus Varus Varus Varus
Bloom et al. [23] Feng et al. [25] Lee et al. [14] Wang et al. [15]
Internal Internal Internal Internal
0.073 3.130 −4.222 −2.683 −0.901
0.500 0.703 0.847 0.650 1.453
0.250 0.494 0.717 0.422 2.111
−0.908 1.053 0.145 1.752 4.509 4.452 −5.882 −2.562 −4.985 −3.957 −1.410 −4.129 −3.749 1.947 −0.620
0.885 0.000 0.000 0.000 0.535
Bloom et al. [23] Feng et al. [25] Lee et al. [14] Wang et al. [15]
Extension −3.037 Extension 0.782 Extension 1.606 Extension −0.746 −0.296
0.734 0.489 0.542 0.488 0.882
0.538 0.239 0.294 0.238 0.778
−4.475 −1.599 −4.140 −0.177 1.740 1.599 0.544 2.669 2.963 −1.702 0.209 −1.531 −2.025 1.433 −0.335
0.000 0.110 0.003 0.126 0.737 −8.00
−4.00
1 Medial and 1 lateral
0.00
4.00
8.00
2 divergent lateral (Hamdi)
One medial and one lateral versus two divergent lateral pins (Hamdi). CI, confidence interval.
differences in stiffness between the two configurations in the internal rotation test. In contrast, Larson et al. [22] reported significantly greater stability of cross pins with an intact medial column. Two parallel lateral pins versus two divergent lateral pins
Parallel and divergent displacements of two isolated lateral pins were compared in three studies. However, the outcomes of Hamdi’s research [24] were only introduced graphically. Thus, data pooling was only possible for the other two studies [14,28] (Fig. 3). A fixed-effects mode was used following a test of heterogeneity (I2 = 0.000 and
70.930% for varus and internal rotation). Pooled data indicated significant differences between the two groups and divergent displacement of the pins was more mechanically stable than parallel (standard mean: 1.336; 95% CI: 0.544–2.127; P = 0.001, standard mean: 2.300; 95% CI: 1.350–3.251; P = 0.000). Two pins versus three pins (1.6 mm) One medial and one lateral versus three lateral pins
Three studies addressed three lateral pins and cross pins [22,23,25]. However, one of them focused solely on internal rotation deformation [22], whereas the other two applied five loading modes [23,25]. Therefore, data
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
Fig. 3
References
Outcome
Statistics for each study Standard difference in means
SE
Variance
Standard difference in means and 95% CI
Lower Upper limit limit Z-value P-value
Lee et al. [14] Varus
1.285
0.518
0.268
0.271 2.300
2.482
0.013
Silva et al. [28] Varus
1.413
0.645
0.417
0.148 2.678
2.190
0.029
1.336
0.404
0.163
0.544 2.127
3.307
0.001
Internal
1.789
0.558
0.311
0.696 2.882
3.207
0.001
Silva et al. [28] Internal
3.881
0.980
0.961
1.959 5.802
3.959
0.000
2.300
0.485
0.235
1.350 3.251
4.745
0.000
Lee et al. [14]
−8.00
−4.00
0.00
2 parallel lateral
4.00
8.00
2 divergent lateral
Two parallel lateral pins versus two divergent lateral pins. CI, confidence interval.
Fig. 4
References
Outcome
Statistics for each study Standard difference in means
SE
Variance
Standard difference in means and 95% CI
Lower Upper limit limit Z-value P-value
Bloom et al. [23] Varus
−0.245
0.502
0.252 −1.228 0.739 −0.488
0.626
Varus
0.629
0.483
0.233 −0.317 1.576
1.303
0.193
0.209
0.348
0.121 −0.473 0.891
0.601
0.548
Bloom et al. [23] Internal
0.796
0.519
0.270 −0.222 1.814
1.533
0.125
Feng et al. [25] Internal Larson et al. [22] Internal
5.060 1.617 2.369
0.966 0.729 1.145
0.933 0.531 1.310
3.166 6.953 0.189 3.045 0.126 4.613
5.237 2.219 2.070
0.000 0.026 0.038
Bloom et al. [23] Extension
0.223
0.502
0.252 −0.760 1.206
0.445
0.656
Extension
0.912
0.495
0.245 −0.058 1.883
1.842
0.065
0.572
0.352
0.124 −0.119 1.263
1.623
0.105
Feng et al. [25]
Feng et al. [25]
−8.00
−4.00
0.00
1 medial and 1 lateral
4.00
8.00
3 lateral pins
One medial and one lateral versus three lateral pins. CI, confidence interval.
pooling of two studies was performed for varus and extension and three studies for internal rotation (Fig. 4). High heterogeneity existed in internal rotation (I2 = 86.784%), whereas I2 values were acceptable for varus and extension (36.481 and 0.000%). A randomeffects mode was used to pool data of internal rotation. The results showed that three pins were more stable in internal rotating deformation (standard mean: 2.369; 95% CI: 0.126–4.613; P = 0.038) and the two configurations were comparable in resisting varus and extension displacements (standard mean: 0.209; 95% CI: − 4.73–0.891;
P = 0.548, standard mean: 0.572; 95% CI: − 0.119–1.263; P = 0.105). Two lateral pins versus three lateral pins
The greatest difference between two lateral pins and three lateral pins lies in the additional third pin irrespective of entry position of the first two pins as long as the comparison was performed within configurations that utilized the same starting points. Therefore, data pooling was applied for all studies that included two pin configurations. The study by Larson et al. [22] was excluded
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Review on supracondylar humeral fracture Chen et al. 395
Fig. 5
References
Outcome
Bloom et al. [23] Feng et al. [25] Gottschalk et al. [27] Silva et al. [28]
Varus Varus Varus Varus
Bloom et al. [23] Feng et al. [25] Gottschalk et al. [27] Silva et al. [28]
Internal Internal Internal Internal
Bloom et al. [23] Feng et al. [25]
Statistics for each study Standard difference in means 1.942 0.218 −0.398 3.259 1.121
Extension Extension Gottschalk et al. [27] Extension
Standard difference in means and 95% CI
Lower Upper SE Variance limit limit Z-value P-value 0.606 0.368 0.753 3.130 3.202 0.001 0.224 −0.709 1.145 0.461 0.645 0.473 0.452 0.204 −1.283 0.487 −0.881 0.378 0.776 1.533 4.986 3.700 0.000 0.881 0.729 0.531 −0.308 2.550 1.538 0.124
−0.412 −0.541 −1.056 −0.500 −0.179
1.590 1.153 1.325 0.824 0.700 −0.398 1.825 1.117 0.799 1.244
0.589 0.392 −0.178 0.663 0.310
0.511 0.476 0.448 0.593 0.249
0.261 0.226 0.201 0.352 0.062
2.578 0.221 0.345 0.958
0.676 0.473 0.451 0.654
0.458 1.252 3.904 0.224 −0.706 1.148 0.203 −0.538 1.228 0.428 −0.325 2.240
3.810 0.467 0.765 1.463
0.249 0.410 0.691 0.264 0.214
0.000 0.640 0.444 0.143 −8.00
−4.00
0.00
2 lateral pins
4.00
8.00
3 lateral pins
Two lateral pins versus three lateral pins. CI, confidence interval.
later because of the presence of obvious heterogeneity in the sensitivity analysis (Fig. 5). For the rest of the four studies [23,25,27,28], data of internal rotation were pooled by fixed-effects mode (I2 = 0.000%), and varus and extension were pooled by the random-effects mode (all the I2 values exceeded 75%). The results showed no statistically significant differences in the mechanical stability of the three directions between the two configurations (standard mean: 1.121; 95% CI: − 0.308 to 2.550; P = 0.124, standard mean: 0.310; 95% CI: − 0.179 to 0.799; P = 0.214, standard mean: 0.958; 95% CI: − 0.325 to 2.240, P = 0.143).
Two cross pins versus three cross pins
Heterogeneity tests indicated a medium level of heterogeneity (I2 = 52.669%). The study by Bloom et al. [23] enrolled all five loading modes, whereas Larson et al. [22] solely performed internal rotation (Fig. 6). Data pooling by the fixed-effects mode yielded no significant difference (standard mean: 0.364; 95% CI: − 0.427 to 1.156; P = 0.367). The additional third pin did not seem to improve the stability of fixation in resisting internal rotation. In terms of varus and extension, Bloom et al. [23] conversely reported a slightly smaller stiffness value of three cross pins compared with two cross pins, although the authors concluded that the overall results of analysis of variance supported a greater stability of three-pin structures.
Three pins versus three pins (1.6 mm)
Meta-analysis was not carried out because only two studies addressed the issue and the test of heterogeneity yielded a high I2-value (I2 = 89.691%). Larson et al. [22] reported a significantly greater torsional stability of three cross pins (two divergent lateral and one medial) compared with three lateral pins. According to Bloom et al. [23], compared with three lateral pins, the stiffness value of three cross pins was higher in varus and internal rotation, but smaller in extension. Two pins versus three pins for fractures with comminution
Data pooling of the two studies [22,28] addressing fractures with medial comminution was performed by the fixed-effects mode because of the presence of a low level of heterogeneity (I2 = 34.308%). The results showed that fractures fixed with the additional third pin that aimed to stabilize the medial column were significantly more resistant to internal rotation than those with only two lateral pins (standard mean: − 7.965; 95% CI: − 10.507 to − 5.423; P = 0.000; Fig. 7). According to Silva et al. [28], the addition of a third medial pin also increased varus bending stiffness of the fixation. Larger pin size versus a 1.6 mm Kirschner wire
Only two studies included different pin sizes in the investigation: one used 2.0 mm smooth pins and the other used
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
Fig. 6
References
Outcome
Statistics for each study Standard difference in means
SE
Variance
Standard difference in means and 95% CI
Lower Upper limit limit Z-value P-value
Bloom et al. [23] Internal
0.845
0.522
0.272 −0.178 1.868
1.619
0.105
Larson et al. [22] Internal
−0.352
0.637
0.406 −1.602 0.897 −0.553
0.580
0.364
0.404
0.163 −0.427 1.156
0.367
0.903
−8.00
−4.00
0.00
2 cross pins
4.00
8.00
3 cross pins
Two cross pins versus three cross pins. CI, confidence interval.
Fig. 7
References
Outcome
Larson et al. [22] Internal Silva et al. [28]
Internal
Statistics for each study Standard difference Lower Upper in means SE Variance limit limit Z-value P-value −10.505 2.433 5.917 −15.272 −5.737 −4.318 0.000 −6.957 1.533 −7.965 1.297
2.350 −9.962 −3.952 −4.538 1.682 −10.507 −5.423 −6.142
Standard difference in means and 95% CI
0.000 0.000 −20.00
−10.00
0.00
3 cross pins
10.00
20.00
2 lateral pins
Two pins versus three pins for fractures with comminution. CI, confidence interval.
2.8 mm Steinmann pins [26,27]. Unsurprisingly, both the studies reported a stiffer construct for a larger pin size than a 1.6 mm Kirschner wire. According to Gottschalk et al. [27], 2.0 mm pins were significantly more stable in internal and external rotation deformation (P < 0.01). Comparisons between small pins and larger pins all reached statistical significance in the study by Srikumaran et al. [26]. Other comparisons
Unlike most of the other studies included, Zionts et al. [13] used a different lateral pin pattern. In the two divergent lateral and three divergent lateral pin configurations, the most distal two pins came cross each other at the fracture site. As it is commonly accepted, the greatest stability of pin fixation requires maximal pin separation at the fracture site and an adequate amount of bone proximal and distal to the fragment should be engaged [4,16]. This helps to explain the obvious weaker torsional strength of two to three lateral pins than two cross pins in Zionts’s study. Wang et al. [15] used two divergent medial pins configuration and they reported that this configuration was significantly more resistant to varus and torsion than two divergent lateral pins (P = 0.002, 0.001, and 0.02, respectively). It seemed like two divergent medial pins could provide as much stability as two cross pins under each loading condition. In their in-vitro study, Marsland and Belkoff [20] tested the mechanical
property of a novel pin configuration that combined an intrafocal posterior pin with a lateral pin. This technique was reported to be potentially safer and to provide torsional stiffness comparable to that of standard two cross and two lateral pins (P > 0.9).
Discussion This study provides an outline summarizing the current results of biomechanical tests of various pin configurations. The multiple comparisons showed that classic two cross pins (one medial pin and one lateral pin) did not show significant mechanical superiority over two divergent lateral pins on the basis of the ‘Hamdi’s method’ under varus, internal rotation, and extension conditions. Outcomes of studies comparing two cross pins and two lateral pins on the basis of the ‘capitellar’ method were conflicting. This is in contrast to the usual thoughts kept by the majority of orthopedic surgeons. On comparing two pins and three pins, the additional pin did not seem to enhance the stability of the two-pin construct as much as expected. Significance was only achieved on comparison between two cross pins and three lateral pins under the internal rotation condition. Although a few biomechanical tests directly compared different three-pin configurations, there seemed to be an agreement between the two recruited studies that three cross pins had greater stiffness in torsion than three lateral pins.
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Review on supracondylar humeral fracture Chen et al. 397
Except for these findings, some results were just within expectation. Two divergent pins were stiffer than two parallel pins because of the wider separation at the fracture site and better engagement of both the columns. An additional pin was effective in stabilizing the medial comminution, and reasonably, pins with greater diameter were stiffer than a 1.6 mm Kirschner wire. For other pin configurations, concerns were that two medial pins may be more susceptible to postoperative ulnar nerve injury and the novel posterior pin method was mechanically less stable. Whether these would have an impact on clinical outcomes remains uncertain. Conclusions cannot be drawn without further exploration. According to related studies [8,19], although varus angulation of the distal fragment was the only factor that could create significant varus deformity in isolation, internal rotation could augment the effects of displacements on other planes and reduce the stability of the fracture. Extension was relatively not as important in shaping cubitus varus because it can be ‘auto-molded’ with time through potential bony growth [29]. However, all the three components of the deformity were suggested to correct because it was reported that a certain amount of failure in correcting the varus was attributed to uncorrected internal rotation deformity [30,31]. Therefore, this study did not provide adequate mechanical evidences to support the choice of a cross pin configuration over isolated lateral pins. Some potential limitations of this systematic review must be acknowledged. First, low to medium level of heterogeneity presented among the included studies. Differences in specimen property, fracture modeling standardization, loading condition, and assessment method could have inevitably influenced the outcomes. Marsland and Belkoff [20] found that the stiffness of pin fixation decreased as the loading cycle increased. As the loading cycle was nonuniform and even unclear among the included studies, this defect may compromise the methodologic power of this study. Second, the sample size of this metaanalysis was small. Thus, we could not perform metaregression and assess publishing bias as an approach to decrease heterogeneity. The methodologic quality of the studies included was averagely fair. As mentioned previously, limitations mainly existed in randomization and allocation. Information on the generation of a random sequence was generally unspecified. Third, biomechanical studies were carried out aiming to show the superiority of one technique over the other. However, statistically insignificant differences between two treatments should not simply be interpreted as equivalence or noninferiority. In addition, how much difference in the strength of fixations are required to impact the clinical outcomes remains uncertain. Further study is expected to address the problem. Besides all these biomechanical outcomes, recent RCTs tended to achieve consensus on which choice should be
made [32–35]. The medial pin was consistently reported to have a higher overall risk of iatrogenic ulnar nerve injury compared with isolated lateral pins. Conversely, no statistical differences were found between the two configurations in terms of radiographic outcomes, joint function, and even postoperative life quality [17,36,37]. Thus, it was concluded that the aim of greater fixing stability is to maintain reduction and maximally eliminate redisplacement such as cubitus varus, but a lower stiffness value of one pin configuration does not necessarily result in loss of reduction as long as it provides sufficient strength to resist deformity during normal daily activities. Besides, a cast/back slab was routinely prescribed for the patients following the initial treatment in most clinic settings [38–42], which apparently confers extra stiffness to the entire fracture complex. None of those biomechanical studies took into account this additional strength during the tests. It has been speculated that isolated lateral pins combining a certain duration of external immobilization would be effective in preventing secondary deformity. A survey recently conducted by Lee et al. [43] indicated that general orthopedic surgeons tended to prefer the lateral pinning technique rather than the cross pinning technique largely because of greater concerns of iatrogenic ulnar nerve injury. Fixation stability came second in the choice of treatment. As both biomechanical and clinical studies did not adequately support the use of cross pins, we thus suggested a selection of isolated lateral pins. As proposed by Lee et al. [44], avoiding the worst clinical scenario might be more important and affordable than obtaining favorable clinical results at the potential cost of disastrous complications. Nerve palsy or injury could be symptomatic, long-lasting, and sometimes incurable. Although several new techniques for proper pin displacement have been introduced to reduce the incidence of ulnar nerve injury [45–48], these methods are generally subjective and require a long learning curve. Meanwhile, isolated lateral pins are believed to provide adequate stability if key points for optimal pin placement can be fulfilled [5]. In this study, although the additional third pin did not confer extra stability for simple fractures, for communited fractures, it is still advocated by some practitioners if there are concerns in terms of firm fixation or detection of unacceptable movement at the fracture site [1, 22,28]. We suggest a customized treatment strategy with respect to specific circumstances and a low threshold of adding the third pin when there is a comminution. In addition, pin size is more of an in-situ assessment than a technical problem. Pins of size 2.0 mm could be used according to the scale of the patient’s skeletal structure [49,50]. Conclusion
In summary, there were no statistically significant differences in stiffness between two cross pins and two divergent lateral pins in resisting varus, internal rotation,
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
and extension deformations. An additional lateral pin did not strengthen two-pin construct when fixing simple fractures, whereas those with medial comminution could be better stabilized by a third cross pin placed across the medial column. Larger pin size was stiffer than a 1.6 mm Kirschner wire. Isolated lateral pins were thus advocated because of a better balance of a lower risk of nerve injury and comparable fixation strength. A proper lateral pinplacement technique should be followed to ensure effectiveness and any adjustments to the treatment strategy should be made with respect to specific circumstances.
Acknowledgements We would like to express our gratitude to the statistician, Dr Xinlin Chen, for his professional guidance and continued encouragement in the process of statistical analysis.
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Conflicts of interest
There are no conflicts of interest. 27
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Todorovic L, Petrovski M, Kamiloski M, Cvetanovska V. Minimally invasive treatment of 56 consecutive supracondylar fractures of the humerus in children. Prilozi 2013; 34:124–127. 42 Kish AJ, Hennrikus WL. Fixation of type 2a supracondylar humerus fractures in children with a single pin. J Pediatr Orthop 2014; 34:e54–e57. 43 Lee S, Park MS, Chung CY, Kwon DG, Sung KH, Kim TW, et al. Consensus and different perspectives on treatment of supracondylar fractures of the humerus in children. Clin Orthop Surg 2012; 4:91–97. 44 Lee KM, Chung CY, Gwon DK, Sung KH, Kim TW, Choi IH, et al. Medial and lateral crossed pinning versus lateral pinning for supracondylar fractures of the humerus in children: decision analysis. J Pediatr Orthop 2012; 32:131–138. 45 Shannon FJ, Mohan P, Chacko J, D’Souza LG. ‘Dorgan’s’ percutaneous lateral cross-wiring of supracondylar fractures of the humerus in children. J Pediatr Orthop 2004; 24:376–379.
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Zaltz I, Waters PM, Kasser JR. Ulnar nerve instability in children. J Pediatr Orthop 1996; 16:567–569. Green DW, Widmann RF, Frank JS, Gardner MJ. Low incidence of ulnar nerve injury with crossed pin placement for pediatric supracondylar humerus fractures using a mini-open technique. J Orthop Trauma 2005; 19:158–163. Eidelman M, Hos N, Katzman A, Bialik V. Prevention of ulnar nerve injury during fixation of supracondylar fractures in children by ‘flexion-extension cross-pinning’ technique. J Pediatr Orthop B 2007; 16:221–224. Kocher MS, Kasser JR, Waters PM, Bae D, Snyder BD, Hresko MT, et al. Lateral entry compared with medial and lateral entry pin fixation for completely displaced supracondylar humeral fractures in children. A randomized clinical trial. J Bone Joint Surg Am 2007; 89:706–712. Lee YH, Lee SK, Kim BS, Chung MS, Baek GH, Gong HS, et al. Three lateral divergent or parallel pin fixations for the treatment of displaced supracondylar humerus fractures in children. J Pediatr Orthop 2008; 28:417–422.
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Stiffness of various pin configurations for pediatric supracondylar humeral fracture: a systematic review on biomechanical studies Tony Lin-wei Chena, Chang-qiang Hea, Ting-qu Zhenga, Yan-qun Ganb, Ming-xiang Huanga, Yan-dong Zhengb and Jing-tao Zhaob To compare the biomechanical stability of various pin configurations for pediatric supracondylar humeral fractures under varus, internal rotation, and extension conditions. After electronic retrieval, 11 biomechanical studies were included. Stiffness values of pin configurations under different loading conditions were extracted and pooled. There were no statistically significant differences between two cross pins and two divergent lateral pins on the basis of the ‘Hamdi method’ (P = 0.249− 0.737). An additional pin did not strengthen two-pin construct (P = 0.124− 0.367), but better stabilized fractures with medial comminution (P < 0.01). Isolated lateral pins are preferable because of a better balance of a lower risk of nerve injury and comparable fixation strength. Limitations such as differences in experimental setup among recruited
studies and small sample size may compromise the methodologic power of this study. J Pediatr Orthop B 24:389–399 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Introduction
the development of cubitus varus and interfere with function recovery. A most recent meta-analysis basic on randomized controlled trials (RCT) reported that the risk of ulnar nerve injury was greater with cross pins [17]. However, the outcomes also indicated that there were no significant difference between the two major pin configurations in terms of radiographic outcomes, range of motion, and even postoperative life quality. It seems like there is a discrepancy in the findings between biomechanical studies and clinic trials.
Pediatric supracondylar humeral fracture (PSHF) is one of the most common elbow traumas. It has been reported that PSHF accounted for 10% of all fractures in children [1] and 75% for elbow fractures [2,3]. For years, a large volume of literatures on PSHF was published. Concepts of treatment evolved rapidly. Consensus has been achieved among orthopedic surgeons that displaced PSHF was best treated by close/open reduction and pin fixation [1,3–5]. However, controversy persists on the optimal pin configuration. The issue has been discussed both clinically and experimentally, and a solution remains pending. Generally, optimal pin configuration was predominantly determined by balancing the risk of iatrogenic ulnar nerve injury and preservation of adequate fracture stability from the fixation [3,4,6–8]. Cross pins and isolated lateral pins are presently the mainstream pin configurations for displaced PSHF. One general consensus among orthopedic surgeons was that cross pin had the advantage of superior fixation stiffness and the shortcoming of compromising neural function of the ulnar nerve. Using isolated lateral entry can avoid nerve injury while, as what was indicated in previous study, the construct may be relatively less biomechanical stable [9–16]. As the most direct consequence of inadequate stability is redisplacement and loss of reduction, the lateral entry pin technique was constantly assumed to be more likely to lead to 1060-152X Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Journal of Pediatric Orthopaedics B 2015, 24:389–399 Keywords: biomechanical study, supracondylar humeral fracture, systematic review a The First Clinical Medical College, Guangzhou University of Chinese Medicine and bThe First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, Guangdong, People’s Republic of China
Correspondence to Jing-tao Zhao, MD, Department of Orthopedics, First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, No. 16 Ji Chang Road, Baiyun District, Guangzhou, Guangdong 510405, People’s Republic of China Tel: +86 13922182520; e-mail: [email protected]
It was well recognized that cubitus varus consisted of deformities in three planes (varus, extension, and internal rotation) [18,19]. Efforts have been made in several in-vitro studies to compare the triplanar mechanical properties of different pin configurations. They were quite similar in methodology and design. Nevertheless, outcomes are inconsistent throughout these biomechanical studies. Whether isolated lateral pins yield inferior stability than cross pins in the aforementioned three directions remains uncertain. Therefore, we performed this systematic review aiming to compare the biomechanical stability of various pin configurations for PSHF under varus, internal rotation, and extension conditions. Pin configurations differed in (a) placement, (b) number, (c) start points, and (d) size. We hypothesized that (a) there was no significant difference in the triplanar stability between two cross pins DOI: 10.1097/BPB.0000000000000196
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
and isolated two lateral pins; (b) one additional lateral pin for the two-pin construct could enhance fixation stiffness; and (c) pin configuration with wider separation in the distal diaphysis region or with a larger size was mechanically more stable.
Method Search strategy
An electronic search of eight databases (Pubmed, EBSCO, Ovid Medline, Embase, Wiley, Proquest, Cochrane Central and China Biomedical literature database) was performed in our study. During the process, several characteristics such as study subject, intervention, and publish type were identified. Key words including ‘supracondylar’, ‘pin’, ‘Kirschner wire’, ‘biomechanical,’ and ‘vitro’ were used in retrieval. No restriction for language or publish period was applied. References from papers that were potentially considered included were also reviewed for extra information. Criteria
The literature screen was performed by two authors of this study (T.L.C. and C.Q.H.). Any disagreements in including results were settled by group discussion involving a third party who was blinded to the recruitment process. The inclusion criteria were as follows. (a) Type of study: only biomechanical studies on the stiffness of different pin configurations were included. Articles were accessible for full text and provided complete data; (b) material: cadaveric bone or synthetic composite humeri; (c) intervention: loading tests including varus, extension or internal rotation; (d) measurement: stiffness value, data provided in the form of displacement and load were also available; (e) fracture mode: simple fracture with the fracture line extended through the middle of the olecranon fossa (roughly 25–30 cm above the distal articular surface); and (f) pins: 1.5/1.6 mm Kirshner wires or pins with a larger size. Assessment of risk of bias
Two authors (J.T.Z. and T.Q.Z.) independently assessed the methodologic quality of the included studies. Although biomechanical study is not typical RCT, the research process is quite similar. Therefore, assessment of risk of bias for each included paper was performed using the Cochrane Collaboration ‘Risk of bias’ assessment tool. Any disagreement was resolved by discussion to reach a consensus. Data collection and analysis
Data were extracted by two authors (Y.G.G. and M.X.H.) separately using a piloted form. Basic information on the characteristics for each enrolled studies in terms of sample size, study subject, pin configuration, Kirschner wire size, and loading mode were recorded. We contacted the
investigators for details of original research when it was necessary. Data pooling was performed by two authors (T.L.C. and C.Q.H.) using Comprehensive Meta Analysis (version 2.2.064; Biostat Inc., Englewood, New Jersey, USA). In this study, the stiffness value was the sole variable, and a continuous variable as well. Therefore, the weighted mean difference and 95% confidence interval (CI) were calculated for each comparison. χ2 and I2 were tested to examine heterogeneity; an I2 value greater than 75% was considered to indicate a high level of heterogeneity, greater than 50% and less than 75% was considered to indicate a medium level, greater than 25% and less than 50% was considered to indicate a low level, and less than 25% barely exists. A random-effects model was utilized when a high level of heterogeneity was found. When there was medium level of heterogeneity, effects model was selected depending on specific conditions by discussion among the authors (T.L.C., J.T.Z., and Y.D.Z.). If possible, publication bias was assessed by constructing a funnel plot when the studies included were no fewer than 6 and meta-regression analysis was carried out when the number of studies included was no smaller than 10. Sensitivity analysis was also carried out to rule out studies with potentially considerable heterogeneity.
Results Article screening
After title and abstract screening, altogether, 13 articles were identified and all the full texts were obtained (Fig. 1). There was a good agreement among the reviewers in article selection as shown by a κ value of 0.75 (u = 3.20, P < 0.01). Recruitment of one study required further discussions involving the third party and consensus was eventually reached because the paper fulfilled the overall inclusion criteria considerably [20]. Two of the 13 studies were excluded because one used plastic materials as the study subject and another one used canine humeri [7,21]. Of the 11 studies included [13–15, 20,22–28], two used cadaveric bone [13,20] and nine used synthetic humeri [14,15,22–28]. Five studies repeatedly tested one specimen for different pin configurations [14, 15,24,25,27]. There were a total of 314 specimens, 12 kinds of pin configurations, three pin sizes, and five loading modes. The characteristics of all the studies included are shown in Table 1. All items are primarily identified according to authors’ descriptions. Unspecific details were supplemented by observing diagrams or radiographic images provided in the articles. For those addressing isolated lateral pin configurations, differences in the starting points of placement were identified and thus the groups were subdivided into two subgroups: ‘Hamdi’ and ‘capitellar’. The term ‘Hamdi’s method’ was used widely to refer to a group of lateral starting point techniques after Hamdi’s study and was generally characterized as ‘a direct lateral, extra-articular starting point,
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Review on supracondylar humeral fracture Chen et al. 391
Fig. 1
Computerized search of 8 database Studies identified (N = 309)
Duplication removed (N = 116)
Studies included with titles and abstracts (N = 193) Excluded for not meeting inclusion criteria (N = 180) Full-text articles assessed for eligibility (N = 13)
Excluded Plastic material (N = 1) Canine humeri (N = 1) Studies for meta-analysis (N = 11)
Flow diagram of the search and screening process of studies.
almost directly on the lateral epicondyle’ [24], whereas a ‘capitellar’ starting point was previously described as ‘the pin engaged the capitellum with a para-olecranon starting point’ [5,27]. The distal pin was suggested to cross the fracture site at the medial edge of the coronoid fossa in ‘Hamdi’s method’ [24] and placed as close to the midline as possible in the ‘capitellar’ method [27]. Studies that were published earlier before these definitions were commonly raised and used were categorized according to the procedure descriptions, schematic, and radiographs provided in the original articles. As a result, the study by Bloom et al. [23] was assigned to the ‘Hamdi’ group. The studies by Lee et al. [14] and Larson et al. [22] were assigned to the ‘capitellar’ group. The study by Zionts et al. [13] did not fall into any of the two categories and was thus addressed separately. Except for information in the table, Silva et al. [28] and Larson et al. [22] set fractures with medial comminution as control groups. Silva et al. [28] also recruited two divergent lateral pin configurations that had different pin spread at the fracture site. Wang et al. [15] and Feng et al. [25] stimulated fractures with oblique fracture lines that were considered simple fractures in this study and recruited in data pooling.
Larson et al. [22] investigated fractures with residual displacements. Zionts et al. [13] unequally assigned specimens to different groups and drilled in lateral pins in patterns that differed from all the other studies. Gottschalk et al. [27] did not specify the grouping method in their study. On the basis of the instructions in the method section, we believed that the authors divided the totaled 20 specimens into two major groups according to the lateral entry start point and 10 specimens in each group were repeatedly used throughout all subgroups. Other than the anatomically reduced group, Bloom et al. [23] also investigated specimens with residual displacement of 20° internal rotation. In Table 1, information on loading conditions indicated that the cycle was quite different between studies and five of these studies [13, 14,25,28] did not clarify this part in the article. Conversely, the loading rate was consistent throughout these researches. The values 0.5 degree/s and 0.5 mm/s seem to be uniform for the biomechanical test. Methodological quality of the studies included
Table 2 shows the result of assessment of the quality of the studies. ‘unknown’ was assigned to ‘blinding’ for all
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Varus, valgus, extension, internal, external
Internal
1.6 mm
1.6 mm
Unclear
Internal 1.6 mm
0.5 degree/s 0.5 mm/s Unclear
Varus, valgus, extension, internal, external 1.6 mm
Unclear
Varus, valgus, extension, internal, external 1.6 mm
Unclear
Unclear Varus, valgus, extension, internal, external
3 cycles
10 cycles Extension
10 cycles
0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 3 degree/s
2 cycles Varus, valgus, extension, internal, external
1.6 mm 2.0 mm 1.6 mm 2.8 mm 1.6 mm
5 cycles Varus, valgus, extension 1.6 mm
0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 0.5 degree/s 0.5 mm/s 0.5 degree/s Unclear Varus, internal 1.6 mm
1 degree/s Internal 2.0 mm
posterior and 1 lateral, 2 divergent lateral (capitellar) lateral and 1 medial divergent lateral (capitellar), 2 parallel lateral divergent lateral (capitellar), 2 parallel lateral and 1 medial divergent lateral (Hamdi), 1 lateral and 1 medial divergent medial divergent lateral (capitellar and Hamdi) divergent lateral (capitellar and Hamdi) divergent lateral (Hamdi), 2 divergent lateral (Hamdi) divergent lateral and 1 medial, 1 lateral and 1 medial divergent lateral (Hamdi), 2 divergent lateral (Hamdi) lateral and 1 medial parallel lateral divergent lateral (the two pins varied in degrees of divergence) divergent lateral (Hamdi), 2 divergent lateral (Hamdi) divergent lateral and 1 medial, 1 lateral and 1 medial divergent lateral (capitellar), 2 divergent lateral (capitellar) divergent lateral and 1 medial, 1 lateral and 1 medial parallel lateral, 2 divergent lateral (Hamdi) lateral and 1 medial divergent lateral, 2 divergent lateral parallel lateral, 1 lateral and 1 medial
5 cycles
studies because none of them provided adequate information indicating whether assessors were blind to the test procedure or not. For studies carried out on cadaveric bone, Zionts et al. [13] reported randomly dividing the specimens but did not mention a specific randomization method. Besides, only three specimens were assigned to two lateral crossed pins because of ‘minimum stability’. We thus assigned ‘unknown’ to ‘selective report’. Of those using synthetic humeri, five studies that performed repeated tests on a single specimen all reported using a randomized testing order without stating the randomization method used. Srikumaran et al. [26] did not provide details on the guiding device that normalized the cutting procedure. ‘Randomization’ for these studies was thus assigned as ‘unknown’ and so was ‘allocation concealment’. The results of assessment indicated that the average methodological quality of the studies included was just fair. Potential experimental heterogeneity may affect pooling outcomes. Two pins versus two pins (1.6 mm) One medial and one lateral versus two divergent lateral pins (Hamdi)
Indicates that a single specimen was used repeatedly.
Zionts et al. [13]
Lee et al. [14]
Larson et al. [22]
Bloom et al. [23]
Hamdi et al. [24]
Feng et al. [25]
Srikumaran et al. [26]
Gottschalk et al. [27]
Wang et al. [15]
a
Cadaveric bone
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri
Synthetic humeri Silva et al. [28]
Cadaveric bone
30 3g×5 36 6g×6 9a 1g×9 20a 2 g × 10 48 6g×8 9a 1×9 12a 1 g × 12 64 8g×8 40 8g×5 9a 1×9 37 Unequal assign Marsland and Belkoff [20]
Subject Sample References
Table 1
Characteristics of the studies included
1 1 3 2 2 2 3 2 3 2 3 1 2 2 3 2 3 2 2 1 3 2
Cycle Loading Mode Pin size Pin configuration
Loading rate
392 Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
There were four studies comparing two cross and two divergent lateral pins following Hamdi’s method [14,15, 23,25]. The study by Srikumaran et al. [26] was not included because it measured torque by rotating the distal fragment in the extension test and the data could not be used in pooling. Bloom’s study investigated both anatomical reduced and malreduced specimens and data were extracted solely from the former. The test for heterogeneity showed that I2 values for varus, internal rotation, and extension were all greater than 50%, which indicated the existence of heterogeneity between studies. As subgroups and meta-regression analysis could not be carried out, a random-effects model was used. The data pooled showed no statistically significant differences between the two groups in the three tests (standard mean: − 1.190; 95% CI: − 3.211 to 0.832; P = 0.249, standard mean: − 0.901; 95% CI: − 3.749 to 1.947; P = 0.535, standard mean: − 0.296; 95% CI: − 2.025 to 1.433; P = 0.737). According to the forest plot (Fig. 2), although the pooled data did not yield statistical significance, a slightly greater resistant strength of the cross pin configuration consistently existed. Besides, the outcomes of the study by Srikumaran et al. [26] also supported that cross pins were more stable in sagittal extensional rotation. One medial and one lateral versus two divergent lateral pins (capitellar)
Two studies compared cross pins with two divergent lateral pins utilizing a capitellar starting point [20,22]. Data pooling could not be implemented because of the presence of high heterogeneity (I2 = 96.663%) and the number of studies was small. In their study on cadaveric bone, Marsland and Belkoff [20] found no significant
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Review on supracondylar humeral fracture Chen et al. 393
Table 2
Assessment of methodologic quality
Title Marsland and Belkoff [20] Silva et al. [28] Wang et al. [15] Gottschalk et al. [27] Srikumaran et al. [26] Feng et al. [25] Hamdi et al. [24] Bloom et al. [23] Larson et al. [22] Lee et al. [14] Zionts et al. [13]
Randomization
Allocation concealment
Blinding
Incomplete outcome
Selective reporting
L L U U U U U L L U U
U L U U L U U L L U U
U U U U U U U U U U U
L L L L L L L L L L L
L L L L L L L L L L U
L, low risk of bias; U, unclear.
Fig. 2
References
Standard difference in means and 95% CI
Statistics for each study
Outcome Standard difference in means −3.535 0.415 0.839 −2.761 −1.190
Lower Upper SE Variance limit limit Z-value P-value 0.800 0.641 −5.104 −1.967 −4.417 0.000 0.476 0.227 −0.519 1.349 0.871 0.384 0.492 0.242 −0.124 1.803 1.707 0.088 0.659 0.434 −4.052 −1.470 −4.191 0.000 1.031 1.064 −3.211 0.832 −1.154 0.249
Bloom et al. [23] Feng et al. [25] Lee et al. [14] Wang et al. [15]
Varus Varus Varus Varus
Bloom et al. [23] Feng et al. [25] Lee et al. [14] Wang et al. [15]
Internal Internal Internal Internal
0.073 3.130 −4.222 −2.683 −0.901
0.500 0.703 0.847 0.650 1.453
0.250 0.494 0.717 0.422 2.111
−0.908 1.053 0.145 1.752 4.509 4.452 −5.882 −2.562 −4.985 −3.957 −1.410 −4.129 −3.749 1.947 −0.620
0.885 0.000 0.000 0.000 0.535
Bloom et al. [23] Feng et al. [25] Lee et al. [14] Wang et al. [15]
Extension −3.037 Extension 0.782 Extension 1.606 Extension −0.746 −0.296
0.734 0.489 0.542 0.488 0.882
0.538 0.239 0.294 0.238 0.778
−4.475 −1.599 −4.140 −0.177 1.740 1.599 0.544 2.669 2.963 −1.702 0.209 −1.531 −2.025 1.433 −0.335
0.000 0.110 0.003 0.126 0.737 −8.00
−4.00
1 Medial and 1 lateral
0.00
4.00
8.00
2 divergent lateral (Hamdi)
One medial and one lateral versus two divergent lateral pins (Hamdi). CI, confidence interval.
differences in stiffness between the two configurations in the internal rotation test. In contrast, Larson et al. [22] reported significantly greater stability of cross pins with an intact medial column. Two parallel lateral pins versus two divergent lateral pins
Parallel and divergent displacements of two isolated lateral pins were compared in three studies. However, the outcomes of Hamdi’s research [24] were only introduced graphically. Thus, data pooling was only possible for the other two studies [14,28] (Fig. 3). A fixed-effects mode was used following a test of heterogeneity (I2 = 0.000 and
70.930% for varus and internal rotation). Pooled data indicated significant differences between the two groups and divergent displacement of the pins was more mechanically stable than parallel (standard mean: 1.336; 95% CI: 0.544–2.127; P = 0.001, standard mean: 2.300; 95% CI: 1.350–3.251; P = 0.000). Two pins versus three pins (1.6 mm) One medial and one lateral versus three lateral pins
Three studies addressed three lateral pins and cross pins [22,23,25]. However, one of them focused solely on internal rotation deformation [22], whereas the other two applied five loading modes [23,25]. Therefore, data
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
Fig. 3
References
Outcome
Statistics for each study Standard difference in means
SE
Variance
Standard difference in means and 95% CI
Lower Upper limit limit Z-value P-value
Lee et al. [14] Varus
1.285
0.518
0.268
0.271 2.300
2.482
0.013
Silva et al. [28] Varus
1.413
0.645
0.417
0.148 2.678
2.190
0.029
1.336
0.404
0.163
0.544 2.127
3.307
0.001
Internal
1.789
0.558
0.311
0.696 2.882
3.207
0.001
Silva et al. [28] Internal
3.881
0.980
0.961
1.959 5.802
3.959
0.000
2.300
0.485
0.235
1.350 3.251
4.745
0.000
Lee et al. [14]
−8.00
−4.00
0.00
2 parallel lateral
4.00
8.00
2 divergent lateral
Two parallel lateral pins versus two divergent lateral pins. CI, confidence interval.
Fig. 4
References
Outcome
Statistics for each study Standard difference in means
SE
Variance
Standard difference in means and 95% CI
Lower Upper limit limit Z-value P-value
Bloom et al. [23] Varus
−0.245
0.502
0.252 −1.228 0.739 −0.488
0.626
Varus
0.629
0.483
0.233 −0.317 1.576
1.303
0.193
0.209
0.348
0.121 −0.473 0.891
0.601
0.548
Bloom et al. [23] Internal
0.796
0.519
0.270 −0.222 1.814
1.533
0.125
Feng et al. [25] Internal Larson et al. [22] Internal
5.060 1.617 2.369
0.966 0.729 1.145
0.933 0.531 1.310
3.166 6.953 0.189 3.045 0.126 4.613
5.237 2.219 2.070
0.000 0.026 0.038
Bloom et al. [23] Extension
0.223
0.502
0.252 −0.760 1.206
0.445
0.656
Extension
0.912
0.495
0.245 −0.058 1.883
1.842
0.065
0.572
0.352
0.124 −0.119 1.263
1.623
0.105
Feng et al. [25]
Feng et al. [25]
−8.00
−4.00
0.00
1 medial and 1 lateral
4.00
8.00
3 lateral pins
One medial and one lateral versus three lateral pins. CI, confidence interval.
pooling of two studies was performed for varus and extension and three studies for internal rotation (Fig. 4). High heterogeneity existed in internal rotation (I2 = 86.784%), whereas I2 values were acceptable for varus and extension (36.481 and 0.000%). A randomeffects mode was used to pool data of internal rotation. The results showed that three pins were more stable in internal rotating deformation (standard mean: 2.369; 95% CI: 0.126–4.613; P = 0.038) and the two configurations were comparable in resisting varus and extension displacements (standard mean: 0.209; 95% CI: − 4.73–0.891;
P = 0.548, standard mean: 0.572; 95% CI: − 0.119–1.263; P = 0.105). Two lateral pins versus three lateral pins
The greatest difference between two lateral pins and three lateral pins lies in the additional third pin irrespective of entry position of the first two pins as long as the comparison was performed within configurations that utilized the same starting points. Therefore, data pooling was applied for all studies that included two pin configurations. The study by Larson et al. [22] was excluded
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Review on supracondylar humeral fracture Chen et al. 395
Fig. 5
References
Outcome
Bloom et al. [23] Feng et al. [25] Gottschalk et al. [27] Silva et al. [28]
Varus Varus Varus Varus
Bloom et al. [23] Feng et al. [25] Gottschalk et al. [27] Silva et al. [28]
Internal Internal Internal Internal
Bloom et al. [23] Feng et al. [25]
Statistics for each study Standard difference in means 1.942 0.218 −0.398 3.259 1.121
Extension Extension Gottschalk et al. [27] Extension
Standard difference in means and 95% CI
Lower Upper SE Variance limit limit Z-value P-value 0.606 0.368 0.753 3.130 3.202 0.001 0.224 −0.709 1.145 0.461 0.645 0.473 0.452 0.204 −1.283 0.487 −0.881 0.378 0.776 1.533 4.986 3.700 0.000 0.881 0.729 0.531 −0.308 2.550 1.538 0.124
−0.412 −0.541 −1.056 −0.500 −0.179
1.590 1.153 1.325 0.824 0.700 −0.398 1.825 1.117 0.799 1.244
0.589 0.392 −0.178 0.663 0.310
0.511 0.476 0.448 0.593 0.249
0.261 0.226 0.201 0.352 0.062
2.578 0.221 0.345 0.958
0.676 0.473 0.451 0.654
0.458 1.252 3.904 0.224 −0.706 1.148 0.203 −0.538 1.228 0.428 −0.325 2.240
3.810 0.467 0.765 1.463
0.249 0.410 0.691 0.264 0.214
0.000 0.640 0.444 0.143 −8.00
−4.00
0.00
2 lateral pins
4.00
8.00
3 lateral pins
Two lateral pins versus three lateral pins. CI, confidence interval.
later because of the presence of obvious heterogeneity in the sensitivity analysis (Fig. 5). For the rest of the four studies [23,25,27,28], data of internal rotation were pooled by fixed-effects mode (I2 = 0.000%), and varus and extension were pooled by the random-effects mode (all the I2 values exceeded 75%). The results showed no statistically significant differences in the mechanical stability of the three directions between the two configurations (standard mean: 1.121; 95% CI: − 0.308 to 2.550; P = 0.124, standard mean: 0.310; 95% CI: − 0.179 to 0.799; P = 0.214, standard mean: 0.958; 95% CI: − 0.325 to 2.240, P = 0.143).
Two cross pins versus three cross pins
Heterogeneity tests indicated a medium level of heterogeneity (I2 = 52.669%). The study by Bloom et al. [23] enrolled all five loading modes, whereas Larson et al. [22] solely performed internal rotation (Fig. 6). Data pooling by the fixed-effects mode yielded no significant difference (standard mean: 0.364; 95% CI: − 0.427 to 1.156; P = 0.367). The additional third pin did not seem to improve the stability of fixation in resisting internal rotation. In terms of varus and extension, Bloom et al. [23] conversely reported a slightly smaller stiffness value of three cross pins compared with two cross pins, although the authors concluded that the overall results of analysis of variance supported a greater stability of three-pin structures.
Three pins versus three pins (1.6 mm)
Meta-analysis was not carried out because only two studies addressed the issue and the test of heterogeneity yielded a high I2-value (I2 = 89.691%). Larson et al. [22] reported a significantly greater torsional stability of three cross pins (two divergent lateral and one medial) compared with three lateral pins. According to Bloom et al. [23], compared with three lateral pins, the stiffness value of three cross pins was higher in varus and internal rotation, but smaller in extension. Two pins versus three pins for fractures with comminution
Data pooling of the two studies [22,28] addressing fractures with medial comminution was performed by the fixed-effects mode because of the presence of a low level of heterogeneity (I2 = 34.308%). The results showed that fractures fixed with the additional third pin that aimed to stabilize the medial column were significantly more resistant to internal rotation than those with only two lateral pins (standard mean: − 7.965; 95% CI: − 10.507 to − 5.423; P = 0.000; Fig. 7). According to Silva et al. [28], the addition of a third medial pin also increased varus bending stiffness of the fixation. Larger pin size versus a 1.6 mm Kirschner wire
Only two studies included different pin sizes in the investigation: one used 2.0 mm smooth pins and the other used
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
Fig. 6
References
Outcome
Statistics for each study Standard difference in means
SE
Variance
Standard difference in means and 95% CI
Lower Upper limit limit Z-value P-value
Bloom et al. [23] Internal
0.845
0.522
0.272 −0.178 1.868
1.619
0.105
Larson et al. [22] Internal
−0.352
0.637
0.406 −1.602 0.897 −0.553
0.580
0.364
0.404
0.163 −0.427 1.156
0.367
0.903
−8.00
−4.00
0.00
2 cross pins
4.00
8.00
3 cross pins
Two cross pins versus three cross pins. CI, confidence interval.
Fig. 7
References
Outcome
Larson et al. [22] Internal Silva et al. [28]
Internal
Statistics for each study Standard difference Lower Upper in means SE Variance limit limit Z-value P-value −10.505 2.433 5.917 −15.272 −5.737 −4.318 0.000 −6.957 1.533 −7.965 1.297
2.350 −9.962 −3.952 −4.538 1.682 −10.507 −5.423 −6.142
Standard difference in means and 95% CI
0.000 0.000 −20.00
−10.00
0.00
3 cross pins
10.00
20.00
2 lateral pins
Two pins versus three pins for fractures with comminution. CI, confidence interval.
2.8 mm Steinmann pins [26,27]. Unsurprisingly, both the studies reported a stiffer construct for a larger pin size than a 1.6 mm Kirschner wire. According to Gottschalk et al. [27], 2.0 mm pins were significantly more stable in internal and external rotation deformation (P < 0.01). Comparisons between small pins and larger pins all reached statistical significance in the study by Srikumaran et al. [26]. Other comparisons
Unlike most of the other studies included, Zionts et al. [13] used a different lateral pin pattern. In the two divergent lateral and three divergent lateral pin configurations, the most distal two pins came cross each other at the fracture site. As it is commonly accepted, the greatest stability of pin fixation requires maximal pin separation at the fracture site and an adequate amount of bone proximal and distal to the fragment should be engaged [4,16]. This helps to explain the obvious weaker torsional strength of two to three lateral pins than two cross pins in Zionts’s study. Wang et al. [15] used two divergent medial pins configuration and they reported that this configuration was significantly more resistant to varus and torsion than two divergent lateral pins (P = 0.002, 0.001, and 0.02, respectively). It seemed like two divergent medial pins could provide as much stability as two cross pins under each loading condition. In their in-vitro study, Marsland and Belkoff [20] tested the mechanical
property of a novel pin configuration that combined an intrafocal posterior pin with a lateral pin. This technique was reported to be potentially safer and to provide torsional stiffness comparable to that of standard two cross and two lateral pins (P > 0.9).
Discussion This study provides an outline summarizing the current results of biomechanical tests of various pin configurations. The multiple comparisons showed that classic two cross pins (one medial pin and one lateral pin) did not show significant mechanical superiority over two divergent lateral pins on the basis of the ‘Hamdi’s method’ under varus, internal rotation, and extension conditions. Outcomes of studies comparing two cross pins and two lateral pins on the basis of the ‘capitellar’ method were conflicting. This is in contrast to the usual thoughts kept by the majority of orthopedic surgeons. On comparing two pins and three pins, the additional pin did not seem to enhance the stability of the two-pin construct as much as expected. Significance was only achieved on comparison between two cross pins and three lateral pins under the internal rotation condition. Although a few biomechanical tests directly compared different three-pin configurations, there seemed to be an agreement between the two recruited studies that three cross pins had greater stiffness in torsion than three lateral pins.
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Review on supracondylar humeral fracture Chen et al. 397
Except for these findings, some results were just within expectation. Two divergent pins were stiffer than two parallel pins because of the wider separation at the fracture site and better engagement of both the columns. An additional pin was effective in stabilizing the medial comminution, and reasonably, pins with greater diameter were stiffer than a 1.6 mm Kirschner wire. For other pin configurations, concerns were that two medial pins may be more susceptible to postoperative ulnar nerve injury and the novel posterior pin method was mechanically less stable. Whether these would have an impact on clinical outcomes remains uncertain. Conclusions cannot be drawn without further exploration. According to related studies [8,19], although varus angulation of the distal fragment was the only factor that could create significant varus deformity in isolation, internal rotation could augment the effects of displacements on other planes and reduce the stability of the fracture. Extension was relatively not as important in shaping cubitus varus because it can be ‘auto-molded’ with time through potential bony growth [29]. However, all the three components of the deformity were suggested to correct because it was reported that a certain amount of failure in correcting the varus was attributed to uncorrected internal rotation deformity [30,31]. Therefore, this study did not provide adequate mechanical evidences to support the choice of a cross pin configuration over isolated lateral pins. Some potential limitations of this systematic review must be acknowledged. First, low to medium level of heterogeneity presented among the included studies. Differences in specimen property, fracture modeling standardization, loading condition, and assessment method could have inevitably influenced the outcomes. Marsland and Belkoff [20] found that the stiffness of pin fixation decreased as the loading cycle increased. As the loading cycle was nonuniform and even unclear among the included studies, this defect may compromise the methodologic power of this study. Second, the sample size of this metaanalysis was small. Thus, we could not perform metaregression and assess publishing bias as an approach to decrease heterogeneity. The methodologic quality of the studies included was averagely fair. As mentioned previously, limitations mainly existed in randomization and allocation. Information on the generation of a random sequence was generally unspecified. Third, biomechanical studies were carried out aiming to show the superiority of one technique over the other. However, statistically insignificant differences between two treatments should not simply be interpreted as equivalence or noninferiority. In addition, how much difference in the strength of fixations are required to impact the clinical outcomes remains uncertain. Further study is expected to address the problem. Besides all these biomechanical outcomes, recent RCTs tended to achieve consensus on which choice should be
made [32–35]. The medial pin was consistently reported to have a higher overall risk of iatrogenic ulnar nerve injury compared with isolated lateral pins. Conversely, no statistical differences were found between the two configurations in terms of radiographic outcomes, joint function, and even postoperative life quality [17,36,37]. Thus, it was concluded that the aim of greater fixing stability is to maintain reduction and maximally eliminate redisplacement such as cubitus varus, but a lower stiffness value of one pin configuration does not necessarily result in loss of reduction as long as it provides sufficient strength to resist deformity during normal daily activities. Besides, a cast/back slab was routinely prescribed for the patients following the initial treatment in most clinic settings [38–42], which apparently confers extra stiffness to the entire fracture complex. None of those biomechanical studies took into account this additional strength during the tests. It has been speculated that isolated lateral pins combining a certain duration of external immobilization would be effective in preventing secondary deformity. A survey recently conducted by Lee et al. [43] indicated that general orthopedic surgeons tended to prefer the lateral pinning technique rather than the cross pinning technique largely because of greater concerns of iatrogenic ulnar nerve injury. Fixation stability came second in the choice of treatment. As both biomechanical and clinical studies did not adequately support the use of cross pins, we thus suggested a selection of isolated lateral pins. As proposed by Lee et al. [44], avoiding the worst clinical scenario might be more important and affordable than obtaining favorable clinical results at the potential cost of disastrous complications. Nerve palsy or injury could be symptomatic, long-lasting, and sometimes incurable. Although several new techniques for proper pin displacement have been introduced to reduce the incidence of ulnar nerve injury [45–48], these methods are generally subjective and require a long learning curve. Meanwhile, isolated lateral pins are believed to provide adequate stability if key points for optimal pin placement can be fulfilled [5]. In this study, although the additional third pin did not confer extra stability for simple fractures, for communited fractures, it is still advocated by some practitioners if there are concerns in terms of firm fixation or detection of unacceptable movement at the fracture site [1, 22,28]. We suggest a customized treatment strategy with respect to specific circumstances and a low threshold of adding the third pin when there is a comminution. In addition, pin size is more of an in-situ assessment than a technical problem. Pins of size 2.0 mm could be used according to the scale of the patient’s skeletal structure [49,50]. Conclusion
In summary, there were no statistically significant differences in stiffness between two cross pins and two divergent lateral pins in resisting varus, internal rotation,
Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Journal of Pediatric Orthopaedics B 2015, Vol 24 No 5
and extension deformations. An additional lateral pin did not strengthen two-pin construct when fixing simple fractures, whereas those with medial comminution could be better stabilized by a third cross pin placed across the medial column. Larger pin size was stiffer than a 1.6 mm Kirschner wire. Isolated lateral pins were thus advocated because of a better balance of a lower risk of nerve injury and comparable fixation strength. A proper lateral pinplacement technique should be followed to ensure effectiveness and any adjustments to the treatment strategy should be made with respect to specific circumstances.
Acknowledgements We would like to express our gratitude to the statistician, Dr Xinlin Chen, for his professional guidance and continued encouragement in the process of statistical analysis.
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26
Conflicts of interest
There are no conflicts of interest. 27
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