Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors

Journal of Clinical Neuroscience xxx (2017) xxx–xxx

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Case study

Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors Timothy Y. Wang, Adam G. Back, Eliza Hompe, Kevin Wall, Oren N. Gottfried ⇑ Department of Neurological Surgery, Duke University Medical Center, Durham, NC, USA

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Article history: Received 25 October 2016 Accepted 22 January 2017 Available online xxxx Keywords: Surgical site infection Lumbar spine Pseudoarthrosis Fusion Irrigation and debridement Interbody cage

a b s t r a c t This study identifies the rate of pseudarthrosis following surgical debridement for deep lumbar spine surgical site infection and identify associated risk factors. Patients who underwent index lumbar fusion surgery from 2013 to 2014 were included if they met the following criteria: 1) age >18 years, 2) had debridement of deep lumbar SSI, and had 3) lumbar spine AP, lateral and flexion/extension X-rays and computed tomography (CT) at 12 months or greater postoperatively. Criteria for fusion included 1) solid posterolateral, facet, or disk space bridging bone, 2) no translational or angular motion on flexion/extension X-rays, and 3) intact posterior hardware without evidence of screw lucency or breakage. Twenty-five patients (age 63.2 ± 12.6 years, 10 male) involving 58 spinal levels met inclusion criteria. They underwent fusion at a mean of 2.32 [range 1–4] spinal levels. Sixteen (64.0%) patients received interbody grafts at a total of 34 (58.6%) spinal levels. All underwent surgical debridement with removal of all nonincorporated posterior bone graft and devascularized tissue. At one-year postoperatively, (56%) patients and 30 (52%) spinal levels demonstrated radiographic evidence of successful fusion. Interbody cage during initial fusion was significantly associated with successful arthrodesis at follow-up (p = 0.017). There is a high rate of pseudoarthrosis in 44% of patients (48% of levels) undergoing lumbar fusion surgery complicated by SSI requiring debridement. Use of interbody cage during initial fusion was significantly associated with higher rate of arthrodesis. Published by Elsevier Ltd.

1. Introduction Advances in surgical techniques and patient selection have resulted in improved outcomes following spine fusion. However, these procedures still require the introduction of foreign hardware and significant tissue dissection and manipulation of native anatomy. As a result, spine fusion patients can experience significant postoperative pain and other less common complications including cerebrospinal fluid (CSF) leak, hardware failure, hematoma, and nerve damage [9]. Surgical site infection is another uncommon but morbid complication for lumbar spine fusion, and has an incidence of 0.3%-9%, depending on a multitude of factors including preoperative diagnosis, type of operation, and patient demographics [1,11,17,21–23]. Following diagnosis of postoperative wound infection, patients typically undergo wound irrigation and debridement with removal of graft bone. Postoperatively, patients are then placed on oral or intravenous (IV) antibiotics and then monitored for resolution of infection [14].

Infection and debridement surgery has significant short-term and long-term sequelae including increased hospital stay, 30-day readmission, decreased quality of life and decreased satisfaction with the index procedure [7,19,26]. However, there is no consensus on the impact of irrigation and debridement or wound infection on long-term fusion rates. There has been previous laboratory data suggesting inflammatory markers associated with infection are beneficial in achieving bone growth [13,25,28]. However, other groups have not shown this association, and in fact, have suggested that the inflammatory response is detrimental for achieving successful arthrodesis [8]. Therefore, the authors designed a retrospective review to assess the rate of arthrodesis following irrigation and debridement following lumbar spine fusion. By doing so, the authors hope to better characterize the rate of arthrodesis following surgical debridement for wound infection, and identify any pre-, peri-, and post-operative factors predictive of either arthrodesis or pseudoarthrosis. 2. Materials and methods

⇑ Corresponding author at: Duke University Medical Center, Box 3807, Durham, NC 27710, USA. Fax: +1 919 684 7937. E-mail address: [email protected] (O.N. Gottfried).

Patients who were: 1) age P18 years at time of surgery, 2) had lumbar spine fusion between 2008 and 2014, 3) debridement of

http://dx.doi.org/10.1016/j.jocn.2017.01.020 0967-5868/Published by Elsevier Ltd.

Please cite this article in press as: Wang TY et al. Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors. J Clin Neurosci (2017), http://dx.doi.org/10.1016/j.jocn.2017.01.020

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T.Y. Wang et al. / Journal of Clinical Neuroscience xxx (2017) xxx–xxx

deep lumbar SSI, and 4) lumbar spine anterior and posterior (AP), lateral flexion/extension X-rays and computed tomography (CT) at 12 months or greater postoperatively were retrospectively included for statistical analysis. Institutional Review Board (IRB) approval was obtained prior to data collection and chart review. Demographic data including age, sex, race, and body mass index (BMI) were recorded. Patient comorbidities including smoking status, diabetes, hypertension (HTN), osteoporosis, hyperlipidemia (HLD), chronic obstructive pulmonary disease (COPD), congestive heart failure (CHF), coronary artery disease (CAD), peripheral vascular disease (PVD) and atrial fibrillation (A-fib) were logged. Details of the initial surgical procedure including type of procedure, indications for surgery, spinal levels involved, estimated blood loss (EBL), urine output (UOP), operating room time, use of interbody cage, and use of intrawound vancomycin powder were recorded. Investigators also verified the any instances of intraoperative complications including neurological worsening and durotomy. Details of infection and debridement were recorded, including tissue culture results, date of debridement, and 30-day readmission. All patients underwent surgical debridement with removal of all non-incorporated posterior bone graft and devascularized tissue, pulse lavage with antibiotic, and drain placement. Intraoperative tissue cultures confirmed infectious etiology. Additional postoperative complications including mortality, pneumonia, UTI, and blood loss requiring packed red blood cell transfusion (pRBC) were recorded. All patients’ 12-month postoperative AP, lateral, and flexion/ extension lumbar spine plain films and lumbar spine CT scan were then reviewed for presence of bony fusion. Criteria for fusion included 1) solid posterolateral, facet, or disk space bridging bone, 2) no translational or angular motion on flexion/extension X-rays, and 3) intact posterior hardware without evidence of screw lucency or breakage. Patients with imaging that satisfied all three criteria were deemed to have achieved successful fusion. Those who did not completely satisfy all three criteria were deemed to have pseudoarthrosis. Patient examples of those who did and did not satisfy fusion criteria are shown in Figs. 1 and 2, respectively. Demographic, pre-, peri-, and postoperative data as well as infection and debridement data were then compared between patients who achieved successful fusion and those who did not. Statistical analysis was performed using JMP 12.0 (SAS Institute,

Inc., Cary, NC, USA). Patient characteristics were summarized as counts with percentages or means with standard deviation (SD), as appropriate. Number of vertebral levels was represented as mean [interquartile range]. Student’s t-test for independent samples was used to assess continuous data. Fisher exact tests were used to analyze categorical variables. Statistical significance was set at a 6 .05. 3. Results 3.1. Patient characteristics In total, 25 patients (15 female, 10 male) involving 58 spinal levels met inclusion criteria and were reviewed in this study. From 2008 to 2014, an additional 8 patients underwent lumbar spine fusion complicated by infection and wound debridement, but did not meet inclusion criteria due to lack of imaging follow-up. The mean age and BMI were 63.2 ± 12.6 years and 31.6 ± 7.5 kg/m2, respectively. Fifteen (60%) patients were obese (BMI >30.0 kg/ m2), 2 (8.0%) were active smokers, 4 (16.0%) had CAD, 19 (76.0%) had hypertension, and 7 (28.0%) had type II diabetes mellitus. Patient demographic data, comorbidities, and surgical levels are summarized in Table 1. A total of 11 (44.0%) patients and 28 (48.0%) spinal levels met criteria for failure of fusion. There were no significant differences in demographic data, risk factors, or comorbidities between the fusion and pseudoarthrosis groups, as detailed in Table 2. 3.2. Intraoperative data Of the 25 patients reviewed, 13 (52.0%) patients underwent lumbar fusion and 12 (48.0%) patients underwent lumbosacral fusion. The average number of fusion levels was 2.32 with a range of 1–4. The number of spinal levels involved was not statistically different between fusion and pseudoarthrosis groups. Ten (40.0%) patients underwent simultaneous laminectomy; 4 (16.0%) patients at 1 spinal level, 5 (20.0%) patients at 2 spinal levels, and 1 (4.0%) patients at 3 spinal levels. Number of laminectomy levels had no statistically significant association with successful fusion. Ten patients (40.0%) underwent fusion including an anterior approach, while 19 (76.0%) patients underwent fusion including a posterior

Fig. 1. Patient case of successful interbody fusion at 1 year follow-up. The above patient had combined anterior-posterior approach L1-S1 interbody fusion with polyetheretherketone (PEEK) interbody grafts in all disk spaces. Initial lumbar fusion was complicated by wound infection with Pseudomonas aeruginosa, which resolved with debridement and ciprofloxacin therapy. Patient had interval posterior hardware removal 1-year following irrigation and debridement. The two anterior L5-S1 anterior screws were not removed. Lateral flexion (A) and extension (B) plain films showed no motion segment instability, and sagittal-view lumbar CT (C) showed successful bridging bone at disk spaces for all levels. The patient met all study criteria for successful fusion. Image series for this patient was obtained at 1-year follow-up from initial lumbar spine fusion.

Please cite this article in press as: Wang TY et al. Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors. J Clin Neurosci (2017), http://dx.doi.org/10.1016/j.jocn.2017.01.020

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T.Y. Wang et al. / Journal of Clinical Neuroscience xxx (2017) xxx–xxx

Fig. 2. Three patient cases of pseudarthrosis at 1 year follow-up. Panels D through F illustrate three separate patients who were categorized into the pseudarthrosis cohort. Patient D’s lateral plain film showed evidence of L2 screw loosening following L2-S1 fusion, Patient E’s lumbar spine CT showed vacuum disk phenomenon following L3-L5 fusion, and while Patient F’s lumbar spine CT showed complete bridging facet bone at L3-L4 and L4-L5, he showed incomplete bridging facet bone at L5-S1. All images were obtained at 1-year follow-up from initial lumbar spine fusion.

Table 1 Demographic data, comorbidities, and surgical levels. Patient

Sex

Age (years)

BMI (kg/m2)

Smoker

Comorbidities

Indication

Location

Fusion levels

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

F M M F M M F F F M F F F M F M M F F M F F M F F

67 79 74 52 69 74 66 73 71 44 45 64 65 70 38 74 58 72 74 82 47 55 39 65 64

21.0 30.6 31.8 30.6 29.3 41.0 36.6 28.0 29.3 18.7 46.6 37.2 22.7 32.4 24.4 34.3 47.5 35.7 39.4 33.2 28.9 35.4 25.1 31.0 19.1

0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0

HTN CAD, HTN, HLD DM, CAD, HTN DM, HLD HTN CAD, DVT, HTN DM, HTN HTN COPD, HTN, HLD – DM, HTN HTN, HLD – HTN HTN HTN, HLD DM, HTN HTN HTN, HLD CAD – DM, COPD, HTN – DM, HTN, HLD HTN

DEG DEG DEF DEG DEG DEG DEG DEF DEG TRAU DEF DEG DEG DEF TRAU DEG DEF DEG DEG DEG DEG DEG TRAU DEG DEG

L LS L LS LS L L L L LS LS L L L L L LS LS LS LS LS L LS LS L

3 4 2 3 3 2 2 2 3 1 1 2 1 1 3 3 1 5 1 3 2 3 2 3 2

M = male, F = female, HTN = hypertension, CAD = coronary artery disease, HLD = hyperlipidemia, DM = Type II diabetes mellitus, DVT = deep vein thrombosis, COPD = chronic obstructive pulmonary disease, DEG = degenerative disorders, DEF = deformity, TRAU = trauma, L = lumbar, LS = lumbosacral.

approach. Five patients (20.0%) underwent fusion using a combined anterior and posterior approach. Eleven (100%) pseudoarthrosis patients had index fusion involving a posterior approach, compared to 8 (57.1%) patients with successful arthrodesis (p = 0.02). Sixteen patients (64.0%) received an interbody graft at the time of initial lumbar fusion. Of these 16 patients who received interbody graft, only bone morphogenic protein (BMP) was inserted in 4 (25.0%) grafts, solely autograft in 11 (68.8%), BMP and autograft in 2 (12.5%), and Osteotech MagniFuse (Medtronic, Fridley, MN, USA) bone graft with autograft in 2 (12.5%). The presence of an interbody graft was found to be statistically associated with successful arthrodesis (85.7% vs. 36.4%, p = 0.02). Operative time, estimated blood loss (EBL), and urine output (UOP) did not statistically differ between cohorts. Likewise, other intraoperative variables such as durotomy, use of a drain,

steroid use, and pRBC transfusion were not statistically different across fusion and pseudoarthrosis groups. Intraoperative data is summarized in Table 3.

3.3. Postoperative complications Four (16.0%) patients contracted a urinary tract infection (UTI), 1 (4.0%) developed pneumonia, 3 (12.0%) had a postoperative hematoma, 7 (28.0%) developed sepsis, and 1 (4.0%) experienced acute renal failure (ARF). Between fusion and non-fusion groups, there were no significant differences in the prevalence or type of postoperative complications. There was no evidence of residual infection or cases of patient mortality within the 1-year followup period.

Please cite this article in press as: Wang TY et al. Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors. J Clin Neurosci (2017), http://dx.doi.org/10.1016/j.jocn.2017.01.020

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T.Y. Wang et al. / Journal of Clinical Neuroscience xxx (2017) xxx–xxx

Table 2 Patient characteristics for pseudarthrosis (non-fusion) and fusion groups. Characteristic

Pseudoarthrosis

Fusion

p

N Total spinal levels Male Age (years) BMI (mg/kg2) Obesity Current smoker CAD Hypertension DM CHF HLD COPD

11 (44.0%) 28 (48.3%) 3 (27.3%) 60.5 ± 3.8 29.7 ± 2.3 5 (45.5%) 1 (9.1%) 1 (9.1%) 10 (90.9%) 3 (27.3%) 0 (0%) 2 (18.2%) 1 (9.1%)

14 (56.0%) 30 (51.7%) 7 (50.0%) 65.4 ± 3.4 33.1 ± 2.0 10 (71.4%) 1 (7.1%) 3 (21.4%) 9 (64.3%) 4 (28.6%) 0 (0%) 5 (35.7%) 1 (7.1%)

– – 0.41 0.35 0.27 0.24 1.00 0.60 0.18 1.00 – 0.41 1.00

CAD = coronary artery disease, DM = Type II diabetes mellitus, CHF = congestive heart failure, HLD = hyperlipidemia, COPD = chronic obstructive pulmonary disease.

Table 3 Intraoperative variables. Intraoperative variables Location Lumbar Lumbosacral Minimally invasive Fusion levels 1 2 3 4+ Laminectomy Laminectomy levels 0 1 2 3 Anterior approach Posterior approach Combined anterior/posterior (same day) Combined anterior/posterior (staged) Drain Durotomy Intraoperative steroid use Operative time (minutes) Estimated blood loss (mL) Urine output (mL) Blood transfusion Interbody graft *

Pseudarthrosis (N = 11)

Fusion (N = 14)

p

5 (45.5%) 6 (54.5%) 1 (9.1%)

8 (57.1%) 6 (42.9%) 4 (28.6%)

2 3 3 3 4

(18.2%) (27.3%) (27.3%) (27.3%) (36.4%)

5 5 4 0 6

(35.7%) (35.7%) (28.6%) (0%) (42.9%)

7 (63.6%) 2 (18.2%) 1 (9.1%) 1 (9.1%) 3 (27.3%) 11 (100%) 2 (18.28%)

8 2 4 0 7 8 1

(57.1%) (14.3%) (28.6%) (0%) (50.0%) (57.1%) (7.14%)

1 (9.14%)

1 (7.14%)

1.00

8 (72.732%) 2 (18.28%) 1 (9.14%) 258.5 ± 32.3 429.6 ± 156.0 630.3 ± 161.5 0 (0%) 4 (36.4%)

7 (50.028%) 2 (14.38%) 3 (21.412%) 259.1 ± 29.7 607.1 ± 138.2 652.7 ± 126.7 2 (14.38%) 12 (85.7%)

0.41 1.00 0.60 0.98 0.40 0.91 0.49 0.02*

0.56

0.34 0.20

1.00 0.47

1.00 0.02* 0.56

Indicates statistically significant result where p < 0.05.

3.4. Indications for irrigation and debridement All patients had a deep lumbar surgical site infection requiring postoperative antibiotic management and surgical debridement. The average time to infection for all patients after the lumbar fusion was 32.5 ± 29.0 days. Two (8.0%) patients developed infection greater than 90 days, postoperatively. Average time to surgical debridement was 29.8 ± 23.1 days. Nineteen (76.0%) patients had a single-agent infection and 6 (24.0%) patients had a multiple agent infection. 12 (48.0%) patients had gram-negative cultures and 14 (56.0%) patients had gram-positive cultures. Intraoperative tissue culture confirmed Staphylococcus aureus (48.0%) as the most common agent of infection with no significant difference between bacterial species and fusion rate. Twenty (80.0%) patients required a single irrigation and debridement procedure, 4 (16.0%) patients required two debridements, and 1 (4.0%) patient required three

debridements. No patients required hardware removal. No patients had persistent bacterial infections at 1-year follow-up imaging. The time to onset of infection, type of bacteria isolated from each culture, and postoperative antibiotic management are summarized in Table 4. 4. Discussion The goals of spinal surgery ultimately remain in achieving adequate decompression of neural elements and achievement of successful arthrodesis through the incorporation of spinal instrumentation. Despite appropriate pre-incisional antibiotics and skin preparation, infection remains a well-known complication of spinal surgery. Current literature estimates the rate of spine surgery wound infection between 0.3% and 9%, depending on risk factors including diabetes, smoking, obesity, malnutrition, and operation times [1,11,13,17,21–23,25]. When instrumentation is added to decompression, there is an increased risk of infection related to both the implantation of hardware and increased length of surgical time [8,28]. Management of post-operative infections in patients with spinal hardware traditionally involves antibiotic therapy and surgical washout of the wound to remove necrotic tissue. An additional goal of wound washout is to decrease intrawound bacterial load. Antibiotics initially remain broad following surgical debridement with pending cultures. Antibiotic coverage is then narrowed to target the isolated strain or strains of bacteria identified via culture. Irrigation and debridement coupled with antibiotic therapy is an effective method of resolving postoperative wound infection; however, it is not well known the effect of infection on achieving long-term fusion. Our case series on spinal infections evaluates the effect these infections on achieving successful spinal arthrodesis. 4.1. Factors reducing the rate of spinal fusion Achieving successful arthrodesis is related to a number of factors including reducing motion, malnutrition, osteoporosis, smoking, chronic steroid use, and obesity. Addressing these factors preoperatively will promote higher rates of successful fusion [20]. Many of these factors affecting fusion rates also raise the risk of post-operative infection. Infection is known to increase biological inflammatory markers, such as COX2, interleukin-1b and TNF-a which have been shown in past laboratory studies to inhibit bone growth; however, there is contradictory laboratory evidence suggesting that this inflammatory response may actually be beneficial to achieving bone growth [16,24]. Anti-inflammatory medications are commonly avoided in patients undergoing spinal fusion as they have been shown to inhibit achievement of bony fusion. Gajraj, Dumont et al., and Maxy et al. suggest the usage of non-steroidal anti-inflammatory drugs in the postoperative period inhibits osteogenesis and rates of successful bony fusion [6,10,18]. Our study assessed the rate of successful arthrodesis after adequate treatment of postoperative spine infections. As determined by aforementioned radiographic criteria, successful fusion was achieved on follow-up imaging in 14 (56.0%) patients and 30 (51.7%) spinal levels. This is significantly reduced compared to the 74–90% fusion rate described in the literature for patients undergoing uncomplicated posterior lumbar fusion [2,4,5,12,15,27]. Further analysis of our patient group revealed that the use of interbody cage during the initial fusion was significantly associated with successful arthrodesis at follow-up (85.7% vs. 36.4%, p = 0.017) despite having post-operative infections. It is well known that interbody grafts improve fusion rates after spinal fusion surgery; however, it is interesting that patients who have

Please cite this article in press as: Wang TY et al. Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors. J Clin Neurosci (2017), http://dx.doi.org/10.1016/j.jocn.2017.01.020

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T.Y. Wang et al. / Journal of Clinical Neuroscience xxx (2017) xxx–xxx Table 4 Infection management. Patient

Time to infection (days)

Culture type

Bacteria species

Time to debridement (days)

Antibiotic regimen

Interbody graft

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

15 18 58 21 34 17 25 15 11 18 14 37 13 21 112 76 11 42 26 20 6 113 18 58 14

Gram Gram+ Gram Gram+ Gram+ Gram Gram Gram ,+ Gram

E. coli MSSA Pseudomonas MSSA MRSA Coag-neg staph, Enterobacter Corynebacterium MRSA, E. coli Enterobacter, Klebsiella Candida MRSA MRSA Candida

15 23 30 21 34 17 25 32 11 18 14 31 13 28 49 76 11 42 26 20 6 113 18 59 14

Ceftriaxone Vancomycin, Ciprofloxacin Piperacillin/tazobactam Cefazolin Vancomycin, Ceftazadine Meropenem Vancomycin Vancomycin, Ciprofloxacin Vancomycin, Meropenem Cefazolin, Fluconazole Nafcillin Vancomycin Vancomycin, Ciprofloxacin Vancomycin, Ertapenem Vancomycin, Ciprofloxacin Cefazolin Piperacillin/tazobactam Ciprofloxacin Ciprofloxacin Vancomycin Ciprofloxacin Vancomycin Vancomycin Cefalexin Nafcillin

N N N Y N Y Y N Y Y Y N Y Y N Y Y Y Y Y Y Y N Y N

Gram+ Gram+ Gram ,+ Gram ,+ Gram+ Gram ,+ Gram Gram Gram+ Gram Gram+ Gram+ Gram+ Gram+

Coag-neg staph, Proteus MSSA MSSA, Pseudomonas Pseudomonas Bacteroides MSSA E. coli Coag-neg staph MSSA MRSA MSSA

E. coli = Escherichia coli, MSSA = Methicillin-susceptible Staphylococcus aureus, MRSA = Methicillin-resistant Staphylococcus aureus, Coag-neg staph = Coagulase-negative staphylococcus.

post-operative infections after spinal fusion that included interbody grafts did not seem to suffer from the same reduction in fusion rate. Lumbar fusion procedures with bone graft along the weight-bearing axis have been shown to increase the rate of fusion, and despite a treated infection, they appear to maintain the ability to improve rates of fusion [3]. There are several limitations to this study. The total number of infections studied over the course of this manuscript’s 6-year study period is small, and thus we recommend future work to incorporate larger patient samples—possibly from multiple institutions. Additionally, this study does not assess the relationship between radiographic and clinical outcomes. With these limitations in mind, it is still important to note that this is the first study to assess the impact of infection on rates of arthrodesis following lumbar spine surgery. This study is the first to suggest that for patients undergoing lumbar fusion complicated by wound infection, usage of interbody graft results in fusion rates similar to those reported by the literature for uncomplicated fusion. Ultimately, further studies are needed to examine the relationship between infection, arthrodesis, and interbody graft placement would allow for better understanding of the effects of inflammation on the fusion process.

5. Conclusion Post-operative infection results in a high rate of pseudoarthrosis in patients undergoing lumbar fusion surgery complicated by SSI requiring debridement. The use of interbody cage during initial fusion was significantly associated with higher rate of arthrodesis likely from the retained and protected bone graft not removed at debridement as well as increased stability. Despite postoperative infection, when interbody grafts are placed there is a high rate of fusion.

Disclosures No funding of any kind was received for this manuscript.

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Please cite this article in press as: Wang TY et al. Impact of surgical site infection and surgical debridement on lumbar arthrodesis: A single-institution analysis of incidence and risk factors. J Clin Neurosci (2017), http://dx.doi.org/10.1016/j.jocn.2017.01.020