Risk factors for surgical site infection following thyroid surgery: a systematic review and meta-analysis

Introduction

Surgical site infection (SSI) ranks among the most prevalent categories of postoperative complications (1), posing significant threats to patient safety and imposing substantial economic burdens on healthcare systems. A recent large-scale investigation into patients undergoing thyroid surgery affirmed that superficial SSIs are amongst the primary types of postoperative complications (2). Adhering to contemporary clinical guidelines (3), prophylactic antibiotics are conventionally prescribed for class II, III, and IV incisions given their heightened risk of infection; in contrast, for class I incisions (defined as clean, lacking signs of infection or inflammation), which typically exhibit lower infection rates, guidelines recommend against the routine use of prophylactic antibiotics. Nonetheless, thyroid surgery, predominantly categorized as clean surgery with class I incisions, has seen of an unexpectedly high rate of prophylactic antibiotic utilization, reaching up to 50% (4). Specifically, SSI affecting thyroid surgery, characterized as infection at the surgical incision site or within deeper tissues, is acknowledged as a major complication of thyroidectomy, with reported incidence rates primarily ranging from 0.09% to 2.9% (5). It is significant to note that, despite its classification as clean surgery, the incidence of SSI in thyroid surgery remains substantial, especially in light of the increasing prevalence of thyroid diseases and the resultant uptick in the frequency of thyroid procedures. SSI can precipitate complications such as wound dehiscence, which prolongs the healing timeline (6). Moreover, they contribute to extended hospital stays, augment healthcare expenses, and escalate the risks associated with systemic infections and other severe complications. Research indicates that the SSI rate for head and neck surgeries stands at 0.37%, yet each case entails an approximate additional hospitalization cost of $20,000 (7). Consequently, the adoption of effective preventive measures becomes indispensable for mitigating the incidence of SSI post-thyroid surgery. Clinicians engaged in thyroidectomies must remain vigilant regarding the risks of SSI and judiciously consider the administration of prophylactic antibiotics to strike a balance between infection control and antibiotic stewardship.

Acknowledging that SSI is a pivotal determinant of surgical success and patient outcomes, this study endeavors to systematically explore the incidence and potential risk factors of SSI following thyroid surgery through a meta-analysis and systematic review. The objectives of this research are to ascertain and quantify the incidence of SSI post-thyroid surgery and to delineate the multifaceted risk factors impacting SSI occurrence. The overarching aim is to furnish evidence-based guidance for clinical practice, optimize SSI prevention protocols, thereby alleviating the strain on healthcare resources and accelerating patient recovery timelines. We present this article in accordance with the MOOSE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-24-330/rc).

Methods

Literature search

An extensive literature search was conducted across multiple databases including PubMed, Embase, Cochrane Library, Web of Science, China Biology Medicine (CBM), China National Knowledge Infrastructure (CNKI), and Wanfang Data. The search was finalized on June 15, 2024. Additionally, we conducted a supplementary search for relevant literatures up to October 4, 2024.

The search strategy specifically sought out cohort studies and case-control studies that incorporated multivariate analyses to investigate risk factors for SSI pertinent to thyroid surgery. Keywords combined with free-text terms were utilized for the search strategy: “thyroid”, “surgical site infection”, and “risk factors”. The supplementary search strategy used keywords in combination with free text terms: “thyroid”, “surgical site infection”, and “predictive factors”. EndNote 21 was utilized for literature management.

Inclusion and exclusion criteria

Inclusion criteria: (I) studies must adhere to the diagnostic criteria for SSI (3). (II) Peer-reviewed case-control studies and cohort studies investigating risk factors for SSI in patients undergoing thyroid surgery are eligible for inclusion. The research must feature multivariate analysis of SSI risk factors. Primary outcome measure: results of multivariate risk factor analysis. Secondary outcome measure: incidence rate of SSI in patients who have undergone thyroid surgery. Exclusion criteria: conference abstracts, meta-analyses, protocols, letters to the editor, duplicate publications, systematic reviews, articles without full-text availability, studies lacking accessible data, and animal experiments will not be considered.

Data extraction

Data extraction was conducted by two independent reviewers, both of whom are thyroid surgeons with extensive clinical experience, who systematically screened the literature. This process involved reading titles, abstracts, and full texts to select studies according to the predetermined inclusion and exclusion criteria. For any studies where there was uncertainty regarding eligibility, consultation with pertinent experts was sought to resolve discrepancies. Throughout the screening procedure, strict adherence to the inclusion and exclusion criteria was maintained. Pertinent indicators were extracted from the studies, and a cross-checking mechanism was implemented to ensure the consistency of the data extracted from the literature. The main contents of the data extraction included the first author’s name, publication year, country of origin, study design, sample size, gender, and age demographics.

Literature evaluation criteria

The Newcastle-Ottawa Scale (NOS) (8) was employed to assess the quality of the studies, evaluating three domains: selection of study groups (up to 4 points), comparability between groups (up to 2 points), and ascertainment of exposure or outcome (up to 3 points). Disagreements during the assessment by the two researchers were discussed until consensus was reached, with consultation of a third party if necessary. The total score ranges from 0 to 9 points, with scores ≤4 indicating low quality, 5–6 points indicating moderate quality, and ≥7 points indicating high quality.

Statistical analysis

Statistical analysis was conducted using Stata version 15.1. Risk estimates across studies, regardless of whether they were reported as odds ratio (OR), risk ratio (RR), or hazard ratio (HR), were uniformly described as ORs. A pooled OR and its 95% confidence interval (CI) were calculated. Based on the results of heterogeneity tests (Q-test) and the I² statistic, an appropriate model was chosen for the calculation of the combined OR. Sensitivity analyses were conducted by sequentially removing individual studies when I²>50% to assess the robustness of the findings. If I²>50%, a random-effects model was applied; if I²≤50%, a fixed-effects model was used. Publication bias was assessed using Egger’s test, with a significance level α=0.05. A P value <0.05 was considered statistically significant.

Results

Literature search and selection process

A comprehensive literature search was conducted in databases (PubMed, Web of Science, Embase, Cochrane Library, CBM, CNKI, and Wanfang Data) targeting cohort studies and case-control studies that featured multivariate analyses of risk factors for SSI following thyroid surgery. EndNote 21 was utilized for efficient literature management. The initial search identified 297 records, from which 130 duplicates were removed, leaving 167 unique records. Applying the exclusion criteria and reviewing titles and abstracts led to the preliminary selection of 13 studies. Upon full-text review, four articles were excluded: one with a study population of head and neck surgery patients (7); one without multifactorial analysis (9); one focusing on non-SSIs (NSSIs) (10); and one deemed unsuitable for inclusion due to the quality of the literature after discussion (11). And supplement search results identified 41 records, from which five duplicate studies were removed, leaving 36 records, exclude studies that do not involve predictive or risk factors. Ten studies met the inclusion criteria and were ultimately included in the analysis. The detailed methodology of the literature search and selection process, including the application of inclusion and exclusion criteria, is illustrated in Figure 1. The search records from the initial search in relevant databases are provided in Tables S1-S6. The data from the supplementary search are provided in Tables S7-S11.

Figure 1 Flow diagram of study selection. CBM, China Biology Medicine. CNKI, China National Knowledge Infrastructure.

Characteristics of included studies

A total of ten studies (12-21) were included in the analysis, consisting of eight case-control studies and two cohort studies. These studies collectively encompassed 127,467 patients, of whom 703 developed postoperative SSI. Detailed characteristics of the included studies are delineated in Table 1. All 10 studies, including both the case-control and cohort designs, underwent quality assessment using the NOS, with scores ranging from 7 to 9, which reflects a generally high quality of the included studies. The particular quality assessments are presented in Table 2.

Postoperative SSI incidence following thyroid surgery

Nine studies reported the incidence of postoperative SSI following thyroid surgery. Heterogeneity testing (I²=97.83%; P<0.001) indicated substantial heterogeneity, prompting the use of a random-effects model for analysis. The results suggest a postoperative SSI incidence of [effect size (ES) =0.02; 95% CI: (0.02, 0.03)]. Due to the considerable heterogeneity of the metric, a sensitivity analysis was conducted by sequentially removing individual studies, which revealed minimal sensitivity and stable results. An Egger’s test was performed to assess publication bias, yielding a P=0.04, suggesting a higher likelihood of publication bias for this metric. See Figures S1,S2 for further details.

Multivariate meta-analysis

Surgical duration greater than 2 hours

Five studies mentioned surgical duration greater than 2 hours. Heterogeneity testing (I²=0.0%; P>0.99) indicated no significant heterogeneity, leading to the use of a fixed-effects model for analysis. The analysis results suggest that a surgical duration greater than 2 hours is a risk factor for postoperative SSI in patients undergoing thyroid surgery, with statistically significant differences [OR =4.50; 95% CI: (2.74, 7.37); P<0.001]. See Figure 2 and Table 3 for details.

Figure 2 Forest plot of the effect of surgical duration greater than 2 hours on SSI following thyroid surgery. OR, odds ratio; CI, confidence interval; SSI, surgical site infection.

Presence of comorbidities

Seven studies reported on comorbidities, referring to chronic health conditions existing before undergoing thyroid surgery, such as diabetes and hypertension. One study differentiated between insulin-dependent diabetes mellitus (IDDM) and non-IDDM (NIDDM) among diabetic patients, and both types were included in the analysis. Heterogeneity testing (I²=79.0%; P<0.001) indicated significant heterogeneity, leading to the use of a random-effects model for analysis. The analysis results suggest that the presence of comorbidities is associated with an increased risk of postoperative SSI in patients undergoing thyroid surgery, with statistically significant differences [OR =1.91; 95% CI: (1.16, 3.15); P=0.01]. See Figure 3 and Table 3 for details.

Figure 3 Forest plot of the effect of presence of comorbidities on SSIs following thyroid surgery. OR, odds ratio; CI, confidence interval; SSI, surgical site infection.

Age greater than 50 years

Four studies reported on age greater than 50 years. Heterogeneity testing (I²=52.5%; P=0.06) indicated no significant heterogeneity, leading to the use of a random-effects model for analysis. The analysis results suggest that age greater than 50 years is associated with an increased risk of postoperative SSI in patients undergoing thyroid surgery, with statistically significant differences [OR =1.81; 95% CI: (1.24, 2.64); P=0.002]. See Figure 4 and Table 3 for details.

Figure 4 Forest plot of the effect of age greater than 50 years on SSI following thyroid surgery. OR, odds ratio; CI, confidence interval; SSI, surgical site infection.

Incision length greater than 5 cm

Three studies reported on incision length greater than 5 cm. Heterogeneity testing (I²=0.0%; P=0.97) indicated no significant heterogeneity, leading to the use of a fixed-effects model for analysis. The analysis results suggest that incision length greater than 5 cm is associated with an increased risk of postoperative SSI in patients undergoing thyroid surgery, with statistically significant differences [OR =2.79; 95% CI: (1.92, 4.04); P<0.001]. See Figure 5 and Table 3 for details.

Figure 5 Forest plot of the effect of incision length greater than 5 cm on SSI following thyroid surgery. OR, odds ratio; CI, confidence interval; SSI, surgical site infection.

Lymph node dissection

Three studies reported on lymph node dissection. Heterogeneity testing (I²=60.6%; P=0.08) indicated moderate heterogeneity, leading to the use of a random-effects model for analysis. The analysis results suggest that lymph node dissection is associated with an increased risk of postoperative SSI in patients undergoing thyroid surgery, with statistically significant differences [OR =1.90; 95% CI: (1.28, 2.80); P=0.001]. See Figure 6 and Table 3 for details.

Figure 6 Forest plot of the effect of lymph node dissection on SSI following thyroid surgery. OR, odds ratio; CI, confidence interval; SSI, surgical site infection.

Male

Four studies reported sex differences. Heterogeneity testing (I²=10.5%; P=0.34) indicated no significant heterogeneity, and thus a fixed-effects model was used for the analysis. The analysis revealed that males were associated with an increased risk of postoperative SSI in thyroid surgery patients, and this difference was statistically significant [OR =1.78; 95% CI: (1.38, 2.29); P<0.001]. See Figure 7 and Table 3 for details.

Figure 7 Forest plot of male’s effect on SSIs following thyroid surgery. OR, odds ratio; CI, confidence interval; SSI, surgical site infection.

Sensitivity analyses

To assess the impact of each study on the aggregate findings, sensitivity analyses were performed by sequentially excluding one study at a time. The results indicated that the pooled ESs and their corresponding 95% CIs were not significantly altered by the exclusion of any single study. This suggests that the overall conclusions drawn from the meta-analysis are robust and reliable.

Publication bias

Egger’s test was applied to each risk factor to assess publication bias. Among the six risk factors with statistically significant differences, surgery time greater than 2 hours (P=0.03) and the presence of comorbidities (P=0.01) showed evidence of publication bias as risk factors for postoperative SSI in patients undergoing thyroid surgery. The remaining four risk factors, including age greater than 50 years (P=0.97), incision length greater than 5 cm (P=0.057), lymph node dissection (P=0.78), and male (P=0.57), had P values greater than 0.05, indicating no evidence of publication bias. See Table 3 for details.

Discussion

This meta-analysis explores risk factors for SSI following thyroid surgery. The incidence of SSI across the included studies ranged from 0.36% to 24%. Increased risk factors for SSI in thyroid surgery patients include surgical duration greater than 2 hours, presence of comorbidities, age greater than 50 years, incision length greater than 5 cm, lymph node dissection, and male.

Longer surgical procedures increase the exposure time of the incision, thereby increasing the opportunity for bacterial invasion and increasing the risk of postoperative SSI (22). Some surgeries can suppress the patient’s immune system, which is another potential reason for increased SSI risk (23). One study has shown that laparoscopic radical nephrectomy with an operative time of more than 3 hours is an independent risk factor for postoperative SSI (24). In addition, each 20-minute increase in operating time increases the risk of postoperative SSI by approximately 25% (25). Another study showed that patients with surgery times longer than 120 minutes had a significantly higher rate of postoperative SSI than those with surgery times within 120 minutes, consistent with the above studies (26). To reduce the risk of SSIs, surgical teams should aim to control the duration of surgery, implement efficient workflows, minimize unnecessary delays and technical complexity, and maintain strict aseptic techniques to effectively prevent SSIs.

Age is one of the most important factors influencing the incidence of SSI. Studies have shown that the risk of postoperative infection increases significantly in patients over the age of 50 years (27). Another study showed a similar trend, with patients aged 65 years and older undergoing thyroidectomy having twice the risk of postoperative complications compared to those under 65 years, and this risk increasing to five times for patients aged 80 years and older (28). With advancing age, patients experience a decline in immune function and weakened tissue repair capacity, both of which contribute to a significantly increased risk of postoperative infection. Honig et al. also found (29) that aging increases the risk of delayed wound healing and skin necrosis, which exacerbates the risk of postoperative SSI.

Many studies examine the relationship between diabetes or hypertension and postoperative SSI separately, so we discuss these conditions separately. There is evidence that diabetic patients have a significantly higher incidence of postoperative SSI than non-diabetic patients (30,31). A study on diabetes and SSI (32) confirmed that perioperative prophylactic antibiotics are an independent protective factor against SSI. Hypertensive patients are also more prone to infection due to vascular dysfunction and impaired tissue repair. Studies suggest that hypertension is an independent risk factor for SSI (33). Therefore, medical teams should thoroughly assess patients’ age and comorbidity status preoperatively and develop personalized preventive measures and treatment strategies to reduce the risk of SSIs, thereby improving patient safety and cure rates.

The length of the incision is a significant factor that influences the incidence of postoperative SSI. It is generally accepted that longer incisions are associated with an increased risk of infection. This is due to the fact that they are more susceptible to contamination from the surrounding environment and exposure to microbes. Furthermore, longer incisions necessitate a longer healing period, thereby extending the window of infection risk. Furthermore, the extent of exposure of long incisions is a significant consideration, as it increases the patient’s exposure to the external environment and potential microorganisms, thereby increasing the likelihood of infection. It is therefore imperative that the size of the incision and the protective measures employed during surgical planning and execution receive special attention, with a view to minimizing the occurrence of postoperative infections. It is incumbent upon surgeons to meticulously plan incision pathways, endeavor to minimize incision size and adhere rigorously to aseptic techniques in order to effectively mitigate the risk of SSI.

Lymph node dissection, a common procedure in thyroid surgery, increases the complexity and duration of surgery, thus elevating the risk of postoperative infections. A number of studies have demonstrated that patients who undergo lymph node dissection have a markedly elevated incidence of postoperative SSI in comparison to those who do not undergo this procedure (7). Additionally, another study has demonstrated that lymph node dissection is significantly associated with an elevated risk of postoperative infection, indicating that this procedure is an important risk factor for SSI (34). Moreover, Jin et al. (35) discovered that prophylactic central neck dissection in clinically node-negative thyroid cancer patients undergoing total thyroidectomy markedly elevated the incidence of surgical site wound infections in comparison to total thyroidectomy alone. This indicates that for non-malignant surgical procedures, the unnecessary performance of prophylactic cervical lymph node dissections can be reduced in order to prevent potential SSIs. However, for curative surgeries for malignant tumors, more precise indicators are required to inform surgical decisions and ensure optimal patient outcomes. In instances where lymph node dissection is undertaken, it is imperative that efforts are made to minimize the duration of the surgical procedure in order to reduce the risk of postoperative infections.

With regard to the utilization of prophylactic antibiotics prior to surgical procedures, the extant research evidence is inconclusive. Some studies have demonstrated that there is no significant correlation between thyroid postoperative infection and the administration of prophylactic antibiotics. Consequently, the routine utilization of prophylactic antimicrobial therapy is not advised (9,19,36), which may be attributable to the specific antibiotic employed. However, other studies have indicated that prophylactic antimicrobial therapy is considered an appropriate course of action in cases where there is a potential risk of SSI, such as the use of 2 g of piperacillin or 1g of cefazolin (37). Conversely, there is evidence that preoperative use of chlorhexidine gluconate shower can effectively reduce the risk of postoperative SSI in patients (38). Despite its limited application in clinical practice, this measure can be considered, particularly for planned surgery patients with relevant risk factors, to reduce the incidence of SSI after thyroid surgery.

Our findings indicate that males have a significantly higher risk of SSI following thyroid surgery compared to females. This finding is consistent with other studies on SSI related to various surgical procedures (39,40), but the underlying mechanisms still require further investigation. One possible explanation for this difference lies in biological sex differences. For instance, males and females differ in immune responses, hormone levels, and skin microbiota, all of which may influence the incidence of SSI. Specifically, androgens have been shown to suppress certain functions of the immune system (41), potentially leading to weaker resistance to infection in males. In addition to biological factors, social behaviors, and lifestyle factors may also be involved. Males are more likely to engage in physical labor or high-risk activities, which can increase their exposure to pathogens. They may also be less stringent in adhering to preoperative hygiene guidelines compared to females. Furthermore, potential biases in the care provided by healthcare providers to different sexes are worthy of consideration. Despite the emphasis placed on equitable treatment in modern medicine, evidence suggests that sex bias may still exist in practice, affecting preoperative assessment, the execution of aseptic techniques during surgery, and the quality of postoperative care.

This study is limited in the following ways: firstly, the number of articles included is relatively small, with the majority of them originating from China, which may introduce selection bias; secondly, during the analysis process, we did not differentiate between OR, RR, and HR. Although the practical differences among these three are minimal, there are inherent distinctions in what they measure regarding disease risk, which may lead to some degree of bias in the results.

Conclusions

The incidence of SSI in patients who underwent thyroid surgery was found to be 2%. The risk factors for SSI in patients who underwent thyroid surgery include surgical duration greater than 2 hours, presence of comorbidities, age greater than 50 years, incision length greater than 5 cm, lymph node dissection, and male. It is recommended that surgeons pay close attention to patients who present with these risk factors and take preventive measures to prevent possible SSI. We look forward to more relevant research in the future to guide us in further reducing SSI after thyroid surgery.

Acknowledgments

Funding: This work was supported by the Zhejiang Medical and Health Science and Technology Plan Project (No. 2022KY939) and the Project of Medical Scientific and Technology Program in Hangzhou (No. A20200821).

Footnote

Reporting Checklist: The authors have completed the MOOSE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-24-330/rc

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-330/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-24-330/coif). All authors report that this work was supported by the Zhejiang Medical and Health Science and Technology Plan Project (No. 2022KY939) and the Project of Medical Scientific and Technology Program in Hangzhou (No. A20200821). The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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