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Surgical site infection rate in spine surgery, incidence, and risk factors: a ten-year retrospective cohort review in a developing neurosurgical centre

Abstract

Background/Objective

Surgical site infection (SSI) is the third common complication in spinal surgery and often results in poor clinical outcomes, prolonged hospital stays, and additional costs. This study estimated the incidence of SSI and identified risk factors in spine surgeries done within 10 years.

Methodology

This was a retrospective cohort review of all patients who had spine surgery between January 2014 and December 2023. Patients’ hospital records were retrieved, and relevant biodata and clinical information were obtained and entered into the Statistical Product and Service Solutions version 25. The incidence of SSI was computed and presented as a percentage, and a multivariable analysis to assess risk factors for SSI was done using the chi-square test and Fisher’s exact test. The level of significance was set at a p-value < 0.05 and a 95% Confidence Interval.

Results

The incidence of SSI was 11.7%; (24/206), predominantly caused by Staphylococcus Aureus (37.5%,P = 0.01) and largely (70%) occurred among patients admitted ≤ 48 h before surgery. The majority were superficial incisional SSIs (19/24,79.2%). They occurred commonly among patients operated for spondylotic disease (13/67,19.4%) and bacterial spondylitis (one out of the two patients) compared to the other spinal pathologies (p = 0.042). Similarly, infection rates were significantly higher in surgeries performed at the lumbar (14/63,22.2%) and thoracolumbar junction (4/31, 12.9%) compared to the cervical and thoracic spine (p = 0.009). This was found to increase the odds of developing SSI by 2.2 times (odds ratio: 2.20;CI:1.38–3.47, P = 0.001), The median duration of hospital stay was 36.5 days for patients with SSIs versus 23 days for patients without SSI (p = 0.008).

Conclusion

This study found a relatively high incidence of SSI, which was predominantly superficial incisional SSI, caused by Staphylococcus Aureus, particularly among patients admitted within 48 h before surgery. Significant risk factors for these infections are patients operated on for spondylotic disease and those who had lumbar or thoracolumbar spine surgeries.

Peer Review reports

Introduction

The occurrence of surgical site infection (SSI) after spinal surgery is a major source of perioperative morbidity and has been reported in several studies as the third most common complication in spine surgery [1]. This morbidity is associated with poor clinical outcomes, prolonged hospital stays, increased re-operation rates, and additional medical costs [1,2,3,4,5,6,7,8]. This constitutes a serious challenge for spine surgeons and patients as well. Despite the availability and wide range of prophylactic antibiotics and several peri-operative aseptic techniques used by spine surgeons, SSI remains a serious concern [9,10,11]. The reported incidence of SSI in the literature varies widely from study to study and depends on the number of patients, pathology, and procedure-related risk factors [7]. Previously, published literature has reported SSI rates ranging from 0.22 to 16.4% in some studies and from 0.5 to 20% in others [4, 5, 9, 10, 12]. However, some authors have suggested that the incidence of SSI will be higher if the Centre for Disease Control (CDC) guidelines for the diagnosis of SSI should be applied to the latter [13,14,15].

Several factors have been identified to play a role in the development of SSI after spine surgery. These includes surgery related factors such as, implant-related spinal surgeries, the type of spine surgery performed, and the duration of the procedure [5, 9, 16, 17]. Although spinal instrumentation surgeries have become an integral part of treatment options for spinal pathology they have been reported to increase the rate of SSI by up to 28% by some authors [9, 16,17,18]. This increase in SSI rate in implant surgery is due to increased exposure of the wound to air, extensive soft tissue dissection, and muscle/skin retraction [5, 9]. Compared with non-fusion spinal surgeries, spinal fusion surgeries have a 33% greater rate of SSI [9, 18]. In recent times, more pathological, patient and surgically-related risk factors for SSI in spinal surgery are increasingly being evaluated [2, 19]. Some of these risk factors include male gender, advanced age, a high body mass index (BMI > 30 kg/m2), smoking status, diabetes status, poor nutritional status (preoperative albumin level < 3.5 g/dL), history of preoperative infection at the surgical site and steroid therapy, blood loss at surgery, number of levels fused, revision status, surgical approach, and prolonged operative time (> 3 h) [3, 20,21,22,23]. From the various reports in the literature, it is obvious that the risks factors for SSI in spine surgery varies widely, and may depends on study design, heterogeneity of study population and location.

Spine surgery has become increasingly common in most healthcare systems around the globe, including Nigeria [24, 25] However, only three published articles from the Southern part of Nigeria reported on spine surgery infection rates, with the infection rates ranging from 11.8 to 16.1% [26,27,28]. Based on the wide range, and the varied risk factors seen in SSI across different institutions, and study locations globally, it is important for spine surgeons to identify the risk factors and burden of infections associated with these procedures within a given practice [24, 29, 30]. Understanding the role that patient-related, pathology-related, and surgery-related factors play in the development of SSI in spinal surgery will help prevent postoperative spinal infection and reduce the morbidity and high cost of care associated with this complication. This study aimed to determine the incidence of SSI and the microorganisms implicated in these infections. It also evaluated the risk factors associated with these infections and the association between pre-operative length of hospital admission and the cultured microorganisms, in spine surgeries performed within 10 years.

Materials and methods

Participants

This 10-year retrospective cohort study was conducted at Jos University Hospital (JUTH). Ethical approval for the study was obtained from the Jos University Teaching Hospital Research Ethics Committee (NHREC/JUTH/05/10/22), with reference number: JUTH/DCS/IREC/XXXI/569. Consent from individual patients to participate in the study was waived by the Research Ethics Committee of the institution due to the retrospective nature of the study design and data collection protocol. All patients who had spinal surgery at JUTH between January 2014 and December 2023 formed the study population. However, patients with missing or incomplete relevant data were excluded from the study.

Socio-demographic and clinical variables

First, the medical/surgical records of all consecutive patients who had spinal surgery performed by the four neurosurgeons at JUTH within the period of the study was obtained. The surgical records were obtained from the Theatre Operation Record System of the Neurosurgery Unit of JUTH. Whereas, the medical records of all the patients were retrieved from the hospital health records system. A predesigned proforma was used to extract relevant patient information which included, clinical demographic characteristics, comorbidities, social risk factors, indications for surgery, and radiological findings. Other perioperative data retrieved included the American Society of Anaesthesiologists (ASA) score, perioperative antibiotic use, number of spine levels operated on, type of implants used, duration of surgery, intraoperative blood loss, and units of blood transfused. These clinical variables were used to determine the risk factors for SSI.

Outcome measures assessed

The primary outcome of this study was to determine the incidence of SSI, and risk factors associated with this infection.

This study adopted the Centers for Disease Control and Prevention definition for the diagnosis of SSIs, which broadly classified these infections into, Incisional SSI (superficial incisional SSI or Deep incisional SSI) and Organ/space SSI [31].

Incisional SSI

is defined as an event that occurs within 30 days (superficial incisional SSI) or 30–90 days (deep incisional SSI) after a spine procedure (where day one is the procedure date), that involves the skin and subcutaneous tissue (superficial incisional SSI) or deep soft tissues (deep incisional SSI) of the incision, and that occurs in a patient who has at least one of the following:

  1. a)

    Purulent drainage from a superficial incision (superficial incisional SSI) or deep incision (deep incisional SSl).

  2. b)

    An organism identified from an aseptically obtained specimen from the superficial incision or subcutaneous tissue (superficial incisional SSI) by culture.

  3. c)

    A superficial incision (superficial incisional SSI) or deep incision (deep incisional SSI) that was deliberately opened by one of the surgeons or aspirated in the case of deep incisional SSI. In which an organism(s) was identified by culture or nonculture-based testing, or in both superficial and deep incisional SSI where culture or nonculture-based testing was not performed, and the patient had at least one of the following signs or symptoms: localized pain or tenderness, localized swelling, erythema, or heat for superficial incisional SSI, and addition of fever (> 38 °C) in deep incisional.

  4. d)

    A surgeon’s diagnosis of a superficial incisional SSI or where an abscess or other evidence of infection involving the deep incision was detected on gross anatomical examination, histopathological examination, or imaging test [31].

Organ/space SSI

is defined as a spinal abscess or infection occurring within 30 or 90 days following a spine procedure (where day one is the procedure date) that involves structures deeper than the fascial/muscle layers, and the patient had at least one of the following:

  1. 1.

    Organism(s) identified from abscess or purulent material found in the spinal epidural or subdural space by culture.

  2. 2.

    Abscess(es) or other evidence of spinal infection on gross anatomic or histopathological exam.

  3. 3.

    At least one of the following localized signs or symptoms: fever (> 38.0 °C), back pain or tenderness, radicular pain, paraparesis, or paraplegia, with either imaging test evidence definitive for spinal abscess/infection or organism(s) identified from blood by culture [31].

The data on surgical site infections and the other clinical parameters obtained from the medical health records system of the patients and the Theatre Operation Record System of the Neurosurgery Unit of JUTH as stated above were used to determine the risk factors for surgical site infection. Other secondary outcomes assessed were the pattern of microorganisms cultured, length of hospital stay before surgery and its association with cultured pathogens, and the association between the incidence of SSI and length of hospital stay. Although unpredictable biases could not be eliminated due to the inclusion of non-randomly selected participants, the reporting of this study was in line with the STROBE-recommended guidelines for reporting cohort studies.

Statistical analysis

Statistical analysis was done using Statistical Product and Service Solutions (SPSS) version 25. for Windows version 25.0 (released 2010; International Business Machines [IBM] Corporation, Armonk, New York). The distribution of continuous variables was assessed using the Kolmogorov‒Smirnov test, and such variables were reported as mean and standard deviation (mean ± standard deviation [SD]), or median, as appropriate. Descriptive statistics for categorical variables were employed using absolute number, frequencies and percentages. Inferential statistics for differences in categorical variables were assessed using the chi-squared test or Fisher’s exact test when the data were sparse, and a P value <. 05 was considered significant. Multivariable logistic regression was used to estimate the odds ratios (ORs) and 95% confidence intervals (CIs) for associations and predictors of SSI in spinal surgery, and the Mann‒Whitney U test was used to compare the mean length of hospital stay between patients with and without SSI.

Results

A total of 260 spine surgeries were performed within the period of the study. Of these, 54 (20.8%) were excluded from the analysis due to missing records (four patients) and incomplete data (50 patients). A total of 206 patients were therefore analyzed in this study. (see Fig. 1)

Fig. 1
figure 1

Schematic diagram of number of spine surgeries performed, number of patients studied and incidence of SSI

The mean age of the patients was 41.86 ± 16 years, and most (92, 44.2%) were aged 20–39 years. The majority of the patients were males (145/206, 70.4%) and trauma (106/206, 51.5%) was the most common indication for surgery, followed by degenerative spine disease with 67/206 (32.5%). The cervical spine with 87/206 (42.2%) and lumbar spine with 63/206 (30.6%) were the most common spinal segments operated. The posterior surgical approach with 127/206 (61.7%) was the most common surgical approach used, with instrumented/implant spinal surgeries performed in more than half (147/206, 71.4%) of the patients. The median duration of surgery was 4 h, and the average volume of blood loss was 325 ml,

A total of 24 patients had SSI giving an incidence rate of 11.7%. The majority (19/24, 79.2%) of which were superficial SSIs as shown in Fig. 2. Table 1 presents the factors evaluated for association with SSI. The following risk factors were not significantly associated with the development of SSI; patient age (p = 0.773), sex (p = 0.094), cigarette smoking status (p = 0.419), immune status (p = 0.419), previous spine surgery (p = 0.410), number of spinal segments operated on (p = 0.180), surgical access to the spine (p = 0.082), and spinal instrumentation (p = 0.106). Likewise, a multivariable binary logistic regression analysis revealed that the preoperative ASA score (p = 0.959, OR: 1.017, 95% CI: 0.534, 1.938), estimated blood loss (p = 0.937, OR: 1.000, 95% CI: 0.999, 1.001), and length of hospital stay before surgery (p = 0.256, OR: 1.021, 95% CI: 0.985, 1.058) were also not significantly associated with SSI as shown on Table 2.

Fig. 2
figure 2

Showing surgical site infection rate

Table 1 Clinical factors associated with surgical site infection rate
Table 2 Multivariate logistic regression model for predictors of SSI

Regarding spine pathology, one (50%) out of the two patients with bacterial spondylitis compared to 19.4%(13/67) and 9.4% (10/106) of the patients with spondylotic disease and traumatic spine injury developed SSI respectively. This difference in the infection rate was found to be statistically significant (p = 0.042). Similarly, infection rates were significantly greater for surgeries of the lumbar spine with 14/63, (22.2%) and thoracolumbar spine with 4/31, (12.9%) compared to surgeries on other spinal segments as shown in Table 1. (p = 0.009) The multivariable regression model used revealed that the likelihood of acquiring SSI was 2.2 times higher when the lumbar and thoracolumbar segments were operated (See Table 2).

Table 1 shows that Staphylococcus aureus was responsible for 9/24 (37.5%) of SSI, followed by Escherichia. Coli with 6/24 (25%), while klebsiella and Pseudomonas aeruginosa were responsible for 3/24 (12.5%) each, negative culture was obtained in 3/24 (12.5%) of the SSI. Most of the organisms cultured in the study were responsible for superficial SSI, whereas, all the negative cultures were found in deep SSI ( p = 0.01), as seen in Table 3.

Table 3 Showing the relationship between the cultured pathogens and type of SSI

The median length of hospital stay (LOS) was 24 days, which was longer (36.5 days) for patients with SSI than for those without SSI (23 days). This association was found to be significant (p = 0.008 [Mann‒Whitney U test]). The association between length of hospital stay and the type of microorganism cultured was not significant (p = 0.525). However, most patients who developed SSI were admitted a day before surgery with a median duration of 7 days, and it was observed that all the infections that occurred in patients who spent more than two weeks on admission before surgery were caused by gram-negative Enterobacteriaceae family such as Escherichia coli with 4/8 (50%), and Klebsiella having 1/8 (12.5%), and also Pseudomonas aeruginosa with 3/8 (37.5%)], while none was caused by Staphylococcus aureus. On the contrary, the majority of the infections caused by Staphylococcus aureus totaling 7/10 (70%), occurred in patients who were admitted less than 48 h before spinal surgery (p = 0.003), as shown in Table 4. All the patients with SSI were treated with intravenous antibiotics sensitive to the cultured organism and surgical debridement, and the infections were resolved in all the patients. Two of the patients had more than two revision surgeries and implant removal was done in one of the patient before the complete resolution of the infection.

Table 4 Showing the relationship between the duration of hospital admission before surgery and the cultured microorganism

Discussion

The study presents the incidence and risk factors for SSI in a developing neurosurgical centre in Nigeria. The survey reports a relatively high incidence of SSI, predominantly caused by Staphylococcus Aureus, with most infections being superficial incisional surgical site infectious. Most of these infections occurred in patients with bacterial spondylitis, spondylotic diseases, and for surgeries done at the lumbar or thoracolumbar region. The 11.7% incidence of SSI reported in this survey is relatively high compared to less than 5% reported by some authors, as shown in Table 5 [1, 3,4,5,6, 8, 11, 12, 17, 19, 24, 32,33,34,35,36,37,38,39,40]. However, this is the lowest observed in Nigeria, based on publications by other authors in Nigeria, who reported SSI rates between 11.8% and 16.1%.26–28 On a general note, there is a wide range in the incidence of SSI reported across several studies ranging from as low as 0.18% to as high as 20% in others [4, 5, 9, 10, 12, 32, 41,42,43,44]. These suggest that the infection rate in this study is similar to that reported by several individual studies but relatively greater than the 3.1% overall pooled incidence of SSI in spine surgery reported in a Systematic Review and Meta-analysis by Zhou et al [33].

Table 5 Showing studies in the last 5 years (2020–2024) on surgical site infection rate, associated risk factors and microbial profile in spine surgery

The number of publications on the rate of SSI in spine surgery has increased in the past 15 years, indicating a growing interest in research related to this subject [45]. Several theories may explain this growing interest. First, there is a persistently high rate of SSI after spine surgery, despite the availability and wide range of prophylactic antibiotics and several peri-operative aseptic techniques used by spine surgeons [9,10,11]. Second, increased morbidity is caused by comorbid factors such as diabetes, antibiotic abuse, immune suppression, and cigarette smoking. Third, the use of spinal instrumentation in spine surgeries has increased, and finally, diagnostic sensitivity has improved. This may explain why the topic “Risk Factors for spinal SSI” was the most published topic relating to spinal SSI in the past 15 years, as reported in a bibliometric analysis by Wang et al. [45].

This study reviewed several explanatory variables as possible risk factors for SSI, and the authors, observed a significantly increased incidence of SSI in patients who had surgery for spondylotic disease and acute bacterial spondylitis. In a systematic review by Zhou et al.., and a retrospective case-control review by Amorim-Barbosa et al., neuromuscular scoliosis was found to be a significant risk factor for the development of SSI [33,34,35], while idiopathic scoliosis had the lowest incidence; this finding was also previously reported by other authors [33, 35, 46, 47]. On the contrary Watanabe et al. in a multicentre retrospective review of primary definitive fusion surgery for spinal deformity identified the type of scoliosis as a risk factor for the development of SSI [36]. Other aetiological risk factors in the literature associated with high risk of SSI include Lumbar spinal stenosis, thoracolumbar and or lumbar burst fractures [5]. In this study, it was also observed that lumbar and thoracolumbar junction surgeries were associated with a significant incidence of SSI, compared to the thoracic and cervical spine. This finding is similar to that reported by AlGamdi et al., and Dong et al., who also reported a higher incidence of SSI in lumbar spine surgeries, compared to the thoracic and cervical spine surgeries in their studies [38]. However, these differences in SSI rates in their study were not statistically significant [37, 38]. Furthermore, the systematic and meta-analysis by Zhou et al., reported a slightly higher SSI rate in the thoracic and cervical spine segment surgeries compared to the lumbar spine, although inferential statistic was not done in their report [33]. The reason why SSI may be common in the lumbar spine spine has not been fully studied. However, the increase in subcutaneous fat in the lumbar region and the depth and distance between the skin and laminar have been reported to be risk factors for SSI in cervical and lumbar spine surgeries [39]. Secondly, the increased thickness of paraspinal muscle in the lumbar region may require more surgical time to expose the vertebral elements during lumbar surgery, and the use of retractors for a longer time to retract these muscles which might result in tissue ischemia, are all factors that may explain why lumbar spine surgery may be associated with increased risk for SSI. It has also been reported that wound proximity to the perineum as seen in lumbar spine surgery could increase the risk of SSI in spine surgery involving the lumbosacral region [48].

Despite the observation in this study that SSIs occurred more in female patients, cigarette smokers, immunosuppressed patients, patients who had posterior spinal surgery, and those whose surgery lasted longer than 2 h, these differences were not statistically significant. The duration of surgery as a risk factor for SSI has also been widely reported, with several authors attributing surgical timing ≥ 3 h as a significant cut-off time that is associated with SSI. Peng et al. reported a fourfold-fold greater risk for SSI in patients who underwent spinal surgery lasting ≥ 3 [33, 49]. However, other authors did not establish this relationship in their study [33, 50, 51]. This finding is similar to that of this present study where all SSIs occurred in patients whose surgery lasted more than two hours, but this difference was not statistically significant.

Surgical site infection often prolongs the course of the disease and duration of hospital stay [1,2,3,4,5,6,7,8]. This often results in increased medical bills, and the overall psychological consequences may affect the prognosis and outcome of care [1,2,3,4,5,6,7,8]. This study revealed a significantly longer duration of hospital stay in patients with SSI. However, the impact of this prolonged duration on the cost of care for these patients was not evaluated. A systematic review by Patel et al. reported that patients who developed SSIs had a longer Length of hospital stay (LOS) with a range of 7.1–19.3 days compared to a range of, 4.0–9.3 days for those without SSI. This is consistent with findings reported by other researchers [9, 52,53,54].

The most common organism cultured in this study was Staphylococcus aureus, which is reportedly the most common causative microorganism, responsible for about 41–90% of spinal SSIs [9, 36, 55, 40]. Patel et al. suggested that the pooled average contribution of Staphylococcus aureus infections to spinal SSIs was 49.3% The meta-analysis by Zhou et al., also reported similar percentages of Staphylococcus aureus (37.9%) and Staphylococcus epidermidis (22.7%) infection in spinal SSI [33]. Staphylococcus aureus is the most common pathogen implicated in SSI following spine surgery, this is because direct inoculation of the microorganism from skin commensal during the surgical procedure, is the most likely route of wound contamination [10]. The other two possible routes of infection are haematogenous spread and early post-operative contamination; these routes are commonly associated with gram-negative organisms such as Pseudomonas aeruginosa, Escherichia coli, and Proteus species. [10] In this study gram gram-negative Enterobacteriaceae such as Escherichia coli Klebsiella and Pseudomonas aeruginosa were other organism isolated from the wound cultures. The involvement of gram-negative organisms as observed in the present study has also been previously reported by other authors [56]. However, there is a wide variation in the reported frequency of involvement of causative agents of SSI across various studies [56]. This reflects the heterogeneity of patients, practice location, as well as different diagnostic approaches used.

The authors observed that the association between the duration of hospital stay before surgery and the cultured pathogen has not been documented in the literature. Most of the reports in the literature are on the association between the length of hospital stay and the occurrence of SSI [37]. In this study we did not find any significant association between the entire length of hospital stay and the cultured microorganism. However, it was observed that patients with shorter duration of hospital admission before surgery who developed SSI, it was largely attributable to Staphylococcus aureus infection. Whereas, admissions lasting more than two weeks before surgery were associated with SSI caused by gram-negative Enterobacteriaceae [Escherichia coli and Klebsiella] and Pseudomonas aeruginosa. The reason(s) for this may not be clear; however, the possible theory could be that patients with shorter lengths of hospital stay might have had their wounds contaminated by direct inoculation from skin commensal. Whereas, patients who were admitted for a longer time before surgery, might have had their wound contaminated from haematogenous spread from a non-diagnosed or sub-clinical infection in the gut, chest, urinary tract, or blood, before surgery within the period of hospital stay.

In effect, attempts should be made to prevent the colonization and contamination of wounds from skin commensal or from haematogenous spread as noted in the finding of this study. A series of procedures, such as the use of meticulous skin preparation, operation field disinfection, timely prophylactic antibiotics administration, intraoperative wound lavage with different solutions, intrawound antibiotic application, and early removal of drains are all attempts aimed at reducing the incidence of SSI in spinal surgeries [57]. Consequently, the effect of wound lavage with diluted povidone-iodine, and the use of intra-wound vancomycin has been shown to significantly reduce the incidence of SSI in spine surgeries by some authors [15, 26, 57, 58]. These measures are being adopted by the authors, In addition, the emphasis on reducing the pre-operative duration of hospital admission and preoperative septic screening to isolate and treat sub-clinical infections as noted in this study could be further strategies employed to mitigate the development of SSI in spine surgery.

The limitations of this study are similar to those associated with retrospective design. These include a significant proportion of incomplete data with the potential under or over-reporting of the incidence and risk factors for SSI in this centre. Also, the inclusion of non-randomly selected participants may have resulted in difficulty in eliminating unpredictable biases. This single-institution-based study had a limited dataset and the lack of significance of some of the parameters of potential interest may reflect insufficient statistical power for generalization. The lack of anaerobic cultures medium in the facility where this study was conducted may also mean that the authors might have missed the possibility of culturing anaerobes, especially in culture-negative patients.

Conclusion

This study reveals a relatively high incidence of SSI in our practice which are predominantly superficial incisional infections caused by Staphylococcus aureus, particularly among patients admitted within 48 hours before surgery. The significant risk factors are spondylitic disease and surgery in the lumbar/thoracolumbar regions. These findings are useful for pre-operative counseling and assessment of patients undergoing spinal surgeries, to ultimately reduce morbidity, length of stay, and eventually the costs of care in these patients.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

ASA:

American society of anaesthesiologists

BMI:

Body mass index

CDC:

Centre for disease control

CI:

Confident interval

IBM:

International business machine

JUTH:

Jos university teaching hospital

LOS:

Length of hospital stay

OR:

Odd ratio

SD:

Standard deviation

SPSS:

Statistical

SSI:

Surgical site infection

References

  1. Phillips BT, Sheldon ES, Orhurhu V, Ravinsky RA, Freiser ME, Asgarzadeh M, et al. Preoperative versus extended postoperative antimicrobial prophylaxis of surgical site infection during spinal surgery: A comprehensive systematic review and Meta-Analysis. Adv Ther. 2020;37(6):2710–33. Epub 2020 May 15. PMID: 32415484; PMCID: PMC7467442.

    PubMed  PubMed Central  Google Scholar 

  2. Kuroiwa M, Schol J, Sakai D, Horikita N, Hiyama A, Katoh H, et al. Predictive factors for successful treatment of deep incisional surgical site infections following instrumented spinal surgeries: retrospective review of 1832 cases. Diagnostics (Basel). 2022;12(2):551. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/diagnostics12020551. PMID: 35204640; PMCID: PMC8871453.

    Article  PubMed  Google Scholar 

  3. Deng H, Chan AK, Ammanuel SG, Chan AY, Oh T, Skrehot HC, et al. Risk factors for deep surgical site infection following thoracolumbar spinal surgery. J Neurosurgery: Spine SPI. 2020;32(2):292–301. https://doiorg.publicaciones.saludcastillayleon.es/10.3171/2019.8.SPINE19479

    Article  Google Scholar 

  4. Zhang F, Liu X, Tan Z, Li J, Fu D, Zhu L. Effect of postoperative hypoalbuminemia and supplement of human serum albumin on the development of surgical site infection following spinal fusion surgery: a retrospective study. Eur Spine J. 2020;29(7):1483–1489. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00586-020-06306-w. Epub 2020 Feb 11. PMID: 32048052.

  5. Zhang T, Lian X, Chen Y, Cai B, Xu J. Clinical outcome of postoperative surgical site infections in patients with posterior thoracolumbar and lumbar instrumentation. J Hosp Infect. 2022;128:26–35. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.jhin.2022.06.014. Epub 2022 Jul 1. PMID: 35788013.

    Article  CAS  PubMed  Google Scholar 

  6. Lubelski D, Feghali J, Ehresman J, Pennington Z, Schilling A, Huq S, et al. Web-Based calculator predicts Surgical-Site infection after thoracolumbar spine surgery. World Neurosurg. 2021;151:e571–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.wneu.2021.04.086. Epub 2021 Apr 30. PMID: 33940258.

    Article  PubMed  Google Scholar 

  7. Spatenkova V, Bradac O, Jindrisek Z, Hradil J, Fackova D, Halacova M. Risk factors associated with surgical site infections after thoracic or lumbar surgery: a 6-year single centre prospective cohort study. J Orthop Surg Res. 2021;16(1):265. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13018-021-02418-1. PMID: 33858467; PMCID: PMC8048320.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Zhang X, Liu P, You J. Risk factors for surgical site infection following spinal surgery: A meta-analysis. Med (Baltim). 2022;101(8):e28836. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/MD.0000000000028836. PMID: 35212281; PMCID: PMC8878791.

    Article  Google Scholar 

  9. Patel H, Khoury H, Girgenti D, Welner S, Yu H. Burden of surgical site infections associated with select spine operations and involvement of Staphylococcus aureus. Surg infect (Larchmt). 2017;18(4):461–73. https://doiorg.publicaciones.saludcastillayleon.es/10.1089/sur.2016.186. Epub 2016 Nov 30. PMID: 27901415; PMCID: PMC5466015.

  10. Chahoud J, Kanafani Z, Kanj SS. Surgical site infections following spine surgery: eliminating the controversies in the diagnosis. Front Med (Lausanne). 2014;1:7.

    PubMed  Google Scholar 

  11. Kobayashi K, Ando K, Kato F, Kanemura T, Sato K, Hachiya Y, Matsubara Y, Sakai Y, Yagi H, Shinjo R, Ishiguro N, Imagama S. Seasonal variation in incidence and causal organism of surgical site infection after PLIF/TLIF surgery: A multicenter study. J Orthop Sci. 2021;26(4):555–9. Epub 2020 Aug 13. PMID: 32800525.

    PubMed  Google Scholar 

  12. Zuo Q, Zhao K, Dong B, Zhou Y, Wang X, Maimaiti A, Tian P. Analysis of risk factors for surgical site infection in spinal surgery patients and study of direct economic losses. BMC Musculoskelet Disord. 2024;25(1):1096. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12891-024-08149-8. PMID: 39736591; PMCID: PMC11686983.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hickok NJ. What are biofilms? Spine (Phila Pa 1976). 2018;43:S7–S8.

  14. McClelland S 3rd, Takemoto RC, Lonner BS, Andres TM, Park JJ, Ricart-Hoffiz PA, et al. Analysis of postoperative thoracolumbar spine infections in a prospective randomized controlled trial using the centers for disease control surgical site infection criteria. Int J Spine Surg. 2016;10:14. https://doiorg.publicaciones.saludcastillayleon.es/10.14444/3014. PMID: 27441172; PMCID: PMC4943169.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Onishi Y, Masuda K, Tozawa K, Karita T. Outcomes of an Intraoperative Povidone-Iodine Irrigation Protocol in Spinal Surgery for Surgical Site Infection Prevention. Clin Spine Surg. 2019;32(10):E449-E452. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BSD.0000000000000908. PMID: 31609802.

  16. Smith JS, Shaffrey CI, Sansur CA, Berven SH, Fu KM, Broadstone PA, Scoliosis Research Society Morbidity and Mortality Committee. Rates of infection after spine surgery based on 108,419 procedures: a report from the Scoliosis Research Society Morbidity and Mortality Committee. Spine (Phila Pa 1976). 2011;36(7):556– 63. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0b013e3181eadd41. PMID: 21192288.

  17. Kobayashi Y, Inose H, Ushio S, Yuasa M, Hirai T, Yoshii T, Okawa A. Body Mass Index and Modified Glasgow Prognostic Score Are Useful Predictors of Surgical Site Infection After Spinal Instrumentation Surgery: A Consecutive Series. Spine (Phila Pa 1976). 2020;45(3):E148-E154. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0000000000003226. PMID: 31513100.

  18. Meredith DS, Kepler CK, Huang RC, Brause BD, Boachie-Adjei O. Postoperative infections of the lumbar spine: presentation and management. Int Orthop. 2012;36(2):439– 44. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00264-011-1427-z. Epub 2011 Dec 10. PMID: 22159548; PMCID: PMC3282873.

  19. Kim DR, Yoon BH, Ki Park Y, Moon BG. Significance of surgical first assistant expertise for surgical site infection prevention: propensity score matching analysis. Med (Baltim). 2023;102(15):e33518. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/MD.0000000000033518. PMID: 37058026; PMCID: PMC10101257.

    Article  Google Scholar 

  20. Lee NJ, Shin JI, Kothari P, Kim JS, Leven DM, Steinberger J, et al. Incidence, impact, and risk factors for 30-Day wound complications following elective adult spinal deformity surgery. Global Spine J. 2017;7(5):417–24. Epub 2017 Apr 20. PMID: 28811985; PMCID: PMC5544156.

    PubMed  PubMed Central  Google Scholar 

  21. Ogihara S, Yamazaki T, Inanami H, Oka H, Maruyama T, Miyoshi K, et al. Risk factors for surgical site infection after lumbar laminectomy and/or discectomy for degenerative diseases in adults: A prospective multicenter surveillance study with registry of 4027 cases. PLoS ONE. 2018;13(10):e0205539. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0205539. PMID: 30325940; PMCID: PMC6191117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Habiba S, Nygaard ØP, Brox JI, Hellum C, Austevoll IM, Solberg TK. Risk factors for surgical site infections among 1,772 patients operated on for lumbar disc herniation: a multicentre observational registry-based study. Acta Neurochir (Wien). 2017;159(6):1113–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00701-017-3184-2. Epub 2017 Apr 20. PMID: 28424918.

    Article  PubMed  Google Scholar 

  23. Fei Q, Li J, Lin J, Li D, Wang B, Meng H, et al. Risk factors for surgical site infection after spinal surgery: A Meta-Analysis. World Neurosurg. 2016;95:507–15. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.wneu.2015.05.059. Epub 2015 Jun 6. PMID: 26054871.

    Article  PubMed  Google Scholar 

  24. Lasry O, Ailon T, Charest-Morin R, Dea N, Dvorak M, Fisher C, et al. Accuracy of hospital-based surveillance systems for surgical site infection after adult spine surgery: a bayesian latent class analysis. J Hosp Infect. 2021;117:117–23. Epub 2021 Jul 14. PMID: 34273471.

    CAS  PubMed  Google Scholar 

  25. 25, Martin BI, Turner JA, Mirza SK, Lee MJ, Comstock BA, Deyo RA. Trends in Health Care Expenditures, Utilization, and Health Status Among US Adults With Spine Problems, 1997–2006;1997:8.

  26. Inojie MO, Okwunodulu O, Ndubuisi CA, Campbell FC, Ohaegbulam SC. Prevention of surgical site infection following open spine surgery: the efficacy of intraoperative wound irrigation with normal saline containing gentamicin versus dilute Povidone-Iodine. World Neurosurg. 2023;173:e1. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.wneu.2022.12.134. -e10,ISSN 1878–8750.

    Article  PubMed  Google Scholar 

  27. Ojo OA, Owolabi BS, Oseni AW, Kanu OO, Bankole OB. Surgical site infection in posterior spine surgery. Niger J Clin Pract. 2016 Nov-Dec;19(6):821–826. https://doiorg.publicaciones.saludcastillayleon.es/10.4103/1119-3077.183237. PMID: 27811458.

  28. Adeolu AA, Oremakinde AA, Komolafe EO. Early results of two methods of posterior spinal stabilization in Nigerians. Niger J Clin Pract. 2014;17(1):51– 5. https://doiorg.publicaciones.saludcastillayleon.es/10.4103/1119-3077.122838. PMID: 24326808.

  29. Cizik AM, Lee MJ, Martin BI, Bransford RJ, Bellabarba C, Chapman JR, et al. Using the spine surgical invasiveness index to identify risk of surgical site infection. J Bone Joint Surg Am. 2012;94:335–42. https://doiorg.publicaciones.saludcastillayleon.es/10.2106/JBJS.J.01084

    Article  PubMed  PubMed Central  Google Scholar 

  30. Whitehouse JD, Friedman ND, Kirkland KB, Richardson WJ, Sexton DJ. The impact of surgical-site infections following orthopedic surgery at a community hospital and a university hospital: adverse quality of life, excess length of stay, and extra cost. Infect Control Hosp Epidemiol. 2002;23:183–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1086/502033

    Article  PubMed  Google Scholar 

  31. National Healthcare Safety Network (NHSN). Patient Safety Component Manual. Chapter 9, Surgical Site Infection Event (SSI) published January 2024 available from: https://www.cdc.gov/nhsn/pdfs/pscmanual/pcsmanual_current.pdf

  32. Kim LY, Halperin SJ, Grauer JN. Surgical site infection following isolated lumbar discectomy increases odds of revision lumbar surgery within first 6 months, but not beyond. Spine J. 2024;24(8):1459–66. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.spinee.2024.03.017. Epub 2024 Apr 1. PMID: 38570035.

    Article  PubMed  Google Scholar 

  33. Zhou J, Wang R, Huo X, Xiong W, Kang L, Xue Y. Incidence of Surgical Site Infection After Spine Surgery: A Systematic Review and Meta-analysis. Spine (Phila Pa 1976). 2020;45(3):208–216. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0000000000003218. PMID: 31464972.

  34. Amorim-Barbosa T, Sousa R, Rodrigues-Pinto R, Oliveira A. Risk factors for acute surgical site infection after spinal instrumentation procedures: A Case-Control study. Int J Spine Surg. 2021;15(5):1025–30. Epub 2021 Oct 14. PMID: 34649951; PMCID: PMC8651194. https://doiorg.publicaciones.saludcastillayleon.es/10.14444/8130

  35. Chan V, Shumilak G, Jafari M, Fehlings MG, Yang MMH, Skaggs DL. Risk stratification for early postoperative infection in Pediatric spinal deformity correction: development and validation of the Pediatric scoliosis infection risk score (PSIR score). Eur Spine J. 2024 Jun 10. Epub ahead of print. PMID: 38858267. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00586-024-08359-7

  36. Song C, Zhang W, Luo C, Zhao X. Prognostic factors for surgical site infection in patients with spinal metastases and following surgical treatment. Med (Baltim). 2024;103(11):e37503. PMID: 38489716; PMCID: PMC10939512. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/MD.0000000000037503

    Article  CAS  Google Scholar 

  37. AlGamdi SS, Alawi M, Bokhari R, Bajunaid K, Mukhtar A, Baeesa SS. Risk factors for surgical site infection following spinal surgery in Saudi Arabia: a retrospective case-control study. Medicine. 2021;100:17e25567.

    Google Scholar 

  38. Dong X, Zhou Y. Cross-sectional analysis of risk factors for surgical site infection secondary to spinal internal fixation via the posterior approach. J Int Med Res. 2022;50(5):3000605221099254. PMID: 35579195; PMCID: PMC9130821. https://doiorg.publicaciones.saludcastillayleon.es/10.1177/03000605221099254

    Article  CAS  PubMed  Google Scholar 

  39. AlEissa S, Konbaz F, AlHelal F, Abalkhail M, AlSalman M, AlMutlaq M et al. Correlation of lumbar spine fat thickness and surgical site infection in degenerative lumbar spine surgery. J Spine Pract (JSP) 2023;20:1–8.

  40. Watanabe K, Yamaguchi T, Suzuki S, Suzuki T, Nakayama K, Demura S, Japan Spinal Deformity Institute Study Group. Surgical Site Infection Following Primary Definitive Fusion for Pediatric Spinal Deformity: A Multicenter Study of Rates, Risk Factors, and Pathogens. Spine (Phila Pa 1976). 2021;46(16):1097–1104. PMID: 33496537. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0000000000003960

  41. Yamamoto EA, Mazur-Hart DJ, Yoo J, Orina JN. Surgical site infection in thoracic and lumbar fractures: incidence and risk factors in 11,401 patients from a nationwide administrative database. Spine J. 2023;23(2):281–6.

  42. Xin B, Cao S, Bai G, Huang X, Ye C, Hu R, et al. Risk factors for postoperative surgical site infection in patients undergoing spinal tumor surgery. Clin Spine Surg. 2023;36(10):E478–83. Epub 2023 Jul 14. PMID: 37448177. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BSD.0000000000001494

    Article  PubMed  Google Scholar 

  43. Deng S, Xie J, Niu T, Wang J, Han G, Xu J, et al. Association of modic changes and postoperative surgical site infection after posterior lumbar spinal fusion. Eur Spine J. 2024;33(8):3165–74. Epub 2024 May 31. PMID: 38816538. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00586-024-08329-z

    Article  PubMed  Google Scholar 

  44. Liu Y, Chen Q, Wang Y, He J. The area ratio of modic changes has predictive value for postoperative surgical site infection in lumbar spine surgery: a retrospective study. BMC Musculoskelet Disord. 2024;25(1):137. PMID: 38347482; PMCID: PMC10863181. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12891-024-07257-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wang X, Lin Y, Yao W, Zhang A, Gao L, Feng F. Surgical site infection in spinal surgery: a bibliometric analysis. J Orthop Surg Res. 2023;18(1):337. PMID: 37158874; PMCID: PMC10165768. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13018-023-03813-6

    Article  PubMed  PubMed Central  Google Scholar 

  46. Cahill PJ, Warnick DE, Lee MJ, Gaughan J, Vogel LE, Hammerberg KW et al. Infection after spinal fusion for pediatric spinal deformity: thirty years of experience at a single institution. Spine (Phila Pa 1976). 2010;35(12):1211-7. PMID: 20445480. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0b013e3181c212d1

  47. Rihn JA, Lee JY, Ward WT. Infection after the surgical treatment of adolescent idiopathic scoliosis: evaluation of the diagnosis, treatment, and impact on clinical outcomes. Spine (Phila Pa 1976). 2008;33(3):289–94. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0b013e318162016e

    Article  PubMed  Google Scholar 

  48. Marmouset D, Haseny B, Dukan R, Saint-Etienne A, Missenard G, Court C, Bouthors C. Characteristics, survivals and risk factors of surgical site infections after En bloc sacrectomy for primary malignant sacral tumors at a single center. Orthop Traumatol Surg Res. 2022;108(4):103197. Epub 2022 Jan 7. PMID: 35007788.

    PubMed  Google Scholar 

  49. Peng XQ, Sun CG, Fei ZG, Zhou QJ. Risk factors for surgical site infection after spinal surgery: A systematic review and Meta-Analysis based on Twenty-Seven studies. World Neurosurg. 2019;123:e318–29. Epub 2018 Nov 26. PMID: 30496932.

    PubMed  Google Scholar 

  50. Watanabe M, Sakai D, Matsuyama D, Yamamoto Y, Sato M, Mochida J. Risk factors for surgical site infection following spine surgery: efficacy of intraoperative saline irrigation. J Neurosurg Spine. 2010;12(5):540-6. PMID: 20433302. https://doiorg.publicaciones.saludcastillayleon.es/10.3171/2009.11.SPINE09308

  51. Blam OG, Vaccaro AR, Vanichkachorn JS, Albert TJ, Hilibrand AS, Minnich JM et al. Risk factors for surgical site infection in the patient with spinal injury. Spine (Phila Pa 1976). 2003;28(13):1475-80. PMID: 12838110. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/01.BRS.0000067109.23914.0A

  52. Ee WW, Lau WL, Yeo W, Von Bing Y, Yue WM. Does minimally invasive surgery have a lower risk of surgical site infections compared with open spinal surgery? Clin Orthop Relat Res. 2014;472(6):1718–24. Epub 2013 Jul 12. PMID: 23846605; PMCID: PMC4016449. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11999-013-3158-5

    Article  PubMed  Google Scholar 

  53. Ramo BA, Roberts DW, Tuason D, McClung A, Paraison LE, Moore HG 4th et al. Surgical site infections after posterior spinal fusion for neuromuscular scoliosis: a thirty-year experience at a single institution. J Bone Joint Surg Am. 2014;96(24):2038-48. PMID: 25520337. https://doiorg.publicaciones.saludcastillayleon.es/10.2106/JBJS.N.00277

  54. Veeravagu A, Patil CG, Lad SP, Boakye M. Risk factors for postoperative spinal wound infections after spinal decompression and fusion surgeries. Spine (Phila Pa 1976). 2009;34(17):1869–72. PMID: 19644339. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/BRS.0b013e3181adc989

    Article  PubMed  Google Scholar 

  55. Mesfin A, Botros M, Benn L, Kulp A. Risk factors for surgical site infections and the effects of betadine irrigation and intrawound Vancomycin powder on infection rates in spine tumor surgery. Cureus. 2024;16(7):e64591. PMID: 39144892; PMCID: PMC11324008. https://doiorg.publicaciones.saludcastillayleon.es/10.7759/cureus.64591

    Article  PubMed  PubMed Central  Google Scholar 

  56. Margaryan D, Renz N, Bervar M, Zahn R, Onken J, Putzier M, et al. Spinal implant-associated infections: a prospective multicentre cohort study. Int J Antimicrob Agents. 2020;56(4):106116. Epub 2020 Jul 26. PMID: 32726675. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ijantimicag.2020.106116

    Article  CAS  PubMed  Google Scholar 

  57. Shu L, Muheremu A, Shoukeer K, Ji Y. Prophylactic application of Vancomycin powder in preventing surgical site infections after spinal surgery. World Neurosurg. 2023;171:e542–53. Epub 2022 Dec 16. PMID: 36529431. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.wneu.2022.12.066

    Article  PubMed  Google Scholar 

  58. Ushirozako H, Hasegawa T, Yamato Y, Yoshida G, Yasuda T, Banno T et al. Impact of intrawound vancomycin powder on prevention of surgical site infection after posterior spinal surgery. J Neurosurg Spine. 2021;34(4):656–664. PMID: 34874533. https://doiorg.publicaciones.saludcastillayleon.es/10.3171/2020.8.SPINE20992

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Acknowledgements

Our sincere appreciation to Dr. Nwibo E.O, Kyesmen N.I, Olalere S.A, Bakwa N.D, and SJ Jatau for participating and assisting in most of the surgeries and for proper data documentation. For editing the use of English in the manuscript we appreciate Prof. Jeno-Mary Enighe.

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This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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DJA, DJS, and GMB; performed all the surgeries and were involved in Conceptualization of the research idea, development of the Methodology, Writing of the Original manuscript text and subsequent review. in addition data analysis, prepartion of tables and figure was performed by JDA. WDS; participated in Methodology and study design, obtaining data from the theatre registry of the hospital writingData curation, Writing of Original draft preparation and reviewing of the manuscript All authors reviewed the manuscript.

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Correspondence to Dumura Jeneral Alfin.

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This study was approved by the Jos University Teaching Hospital Research Ethics Committee (NHREC/JUTH/05/10/22), with reference number: JUTH/DCS/IREC/XXXI/569.

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The authors declare no competing interests.

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Alfin, D.J., Shilong, D.J., Bot, G.M. et al. Surgical site infection rate in spine surgery, incidence, and risk factors: a ten-year retrospective cohort review in a developing neurosurgical centre. BMC Surg 25, 127 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12893-025-02846-4

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