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Risk Factors for Surgical Site Infection in Neonates: A Systematic Review of the Literature and Meta-Analysis

Risk Factors for Surgical Site Infection in Neonates: A Systematic Review of the Literature and... SYSTEMATIC REVIEW published: 29 March 2019 doi: 10.3389/fped.2019.00101 Risk Factors for Surgical Site Infection in Neonates: A Systematic Review of the Literature and Meta-Analysis 1 2 3 2 Vincenzo Davide Catania , Alessandro Boscarelli , Giuseppe Lauriti , Francesco Morini and Augusto Zani * Division of General and Thoracic Surgery, The Hospital for Sick Children, University of Toronto, Toronto, ON, Canada, Neonatal Surgery Unit, Department of Medical and Surgical Neonatology, Bambino Gesù Children’s Hospital, IRCCS, Rome, Italy, Department of Pediatric Surgery, Spirito Santo Hospital and G. d’Annunzio University of Chieti and Pescara, Chieti, Italy Purpose: Surgical site infections (SSI) contribute to postoperative morbidity and mortality in children. Our aim was to evaluate the prevalence and identify risk factors for SSI in neonates. Methods: Using a defined strategy, three investigators searched articles on neonatal SSI published since 2000. Studies on neonates and/or patients admitted to neonatal Edited by: Oliver J. Muensterer, intensive care unit following cervical/thoracic/abdominal surgery were included. Risk Johannes Gutenberg University factors were identified from comparative studies. Meta-analysis was conducted Mainz, Germany according to PRISMA guidelines using RevMan 5.3. Data are (mean ± SD) prevalence. Reviewed by: Maximilian Weniger, Results: Systematic review—of 885 abstracts screened, 48 studies (27,760 neonates) Massachusetts General Hospital and were included. The incidence of SSI was 5.6% (1,564 patients). SSI was more frequent in Harvard Medical School, United States males (61.8%), premature babies (77.4%), and following gastrointestinal surgery (95.4%). Ana Catarina Fragoso, Meta-analysis—10 comparative studies (16,442 neonates; 946 SSI 5.7%) showed that Universidade do Porto, Portugal predictive factors for SSI development were gestational age, birth weight, age at surgery, *Correspondence: Augusto Zani length of surgical procedure, number of procedure per patient, length of preoperative augusto.zani@sickkids.ca hospital stay, and preoperative sepsis. Conversely, preoperative antibiotic use was not significantly associated with development of SSI. Specialty section: This article was submitted to Conclusions: Younger neonates and those undergoing abdominal procedures are at Pediatric Surgery, higher risk for SSI. Given the lack of evidence-based literature, prospective studies may a section of the journal Frontiers in Pediatrics help determine the risk factors for SSI in neonates. Received: 06 January 2019 Keywords: newborn, wound infection, neonatal surgery, risk factors, systematic review, meta-analysis Accepted: 05 March 2019 Published: 29 March 2019 Citation: INTRODUCTION Catania VD, Boscarelli A, Lauriti G, Morini F and Zani A (2019) Risk Surgical site infections (SSI) are infections that occur postoperatively in the area of the body where Factors for Surgical Site Infection in the surgery took place. SSI can be superficial and involve the skin only, or more serious and Neonates: A Systematic Review of the involve other tissues, organs, or implanted material. SSI are among the most common hospital Literature and Meta-Analysis. acquired diseases and are an important cause of morbidity and mortality in all patients, including Front. Pediatr. 7:101. doi: 10.3389/fped.2019.00101 neonates and infants (1, 2). Frontiers in Pediatrics | www.frontiersin.org 1 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates TABLE 1 | Defined search strategy. Whilst the incidence and risk factors for SSI in adults and more recently in children have been defined and management Publication guidelines have been established (3, 4), yet little is known about SSI in neonates and infants. Sources PubMed, Medline, Cochrane Collaboration, The incidence of SSI is 2–5% in adult patients undergoing Embase, Web of Science, Ovid inpatient surgery (3). Risk factors associated with SSI included Language Any co-morbidities, advanced age, risk indices, patient frailty, and Date Since 2000 surgery complexity (5). Subject Human studies In children the rate of SSI ranged from 2.5 to 5.4% and Study type Retrospective dirty wounds, inpatient status, increased duration of surgery, Prospective or certain surgical disciplines (cardiovascular, general surgery, Case control neurosurgery, and orthopedics) were associated with increased Cohort risk of developing an SSI (4). Excluded Grey Literature Previous studies have shown that the incidence of SSI in Case reports neonates and infants can be as high as 17% (1, 2). In this Case series <10 patients population of patients, several conditions have been reported Letters to be associated with an increased risk of SSI, including Editorials admission to the neonatal intensive care unit (NICU), history Keywords Neonate, Neonatal, Newborn of prematurity, low birth weight, mechanical ventilation, Surgery central venous access, associated co-morbidities, prolonged Surgical site infection antibiotic administration, postsurgical hyperglycemia, and Surgical wound infection neutropenia (1, 2, 6, 7). In the present study, we aimed to establish the incidence of SSI in neonates and to identifyprognostic factors that may studies, and opinion articles were excluded. The full text of help stratify which neonates are at increased risk to develop the potentially eligible studies was retrieved and independently this complication. A better understanding of the causes leading assessed for eligibility by the same three investigators. Any to SSI could reduce their incidence, help define guidelines, and disagreement over the eligibility of particular studies was eventually improve outcome. resolved through discussion with the other two authors (FM and AZ). Outcome measures included demographic data, METHODS type and district of surgery, SSI development, preoperative systemic infection, preoperative antibiotic prophylaxis, length of To investigate the incidence and risk factors of SSI in neonates, procedure, and number of procedure per patient. Risk factors of we conducted a systematic review of the literature and SSI were identified from comparative studies. complemented it with a meta-analysis of comparative studies. Both the systematic review and the meta-analysis Statistical Analysis were drafted according to the Preferred Reporting Items Data were analyzed using GraphPad Prism 6.2 Macintosh for Systematic Reviews and Meta-Analyses (PRISMA) Version (10). Data were compared using Fisher’s exact test and statement (8). The protocol for this systematic review are expressed as mean ± SD. When median and range were was registered on PROSPERO—international prospective reported, mean± SD were estimated, as previously reported (11). register of systematic reviews (registration number: The meta-analysis was conducted with RevMan 5.3 (12), using CRD42017069003) (9). Using a defined search strategy, the fixed-effects model to produce risk ratio (RR) for categorical three investigators (VDC, AB, and GL) independently variables and mean differences (MD) for continuous variables, searched scientific databases (PubMed, Medline, Cochrane along with 95% confidence intervals (CI). We produced I values Collaboration, Embase, Web of Science, Ovid) using a to assess homogeneity and quantify the dispersion of effect sizes. combination of keywords (Table 1). MeSH headings and terms used were “neonate OR newborn” AND “surgery OR Quality Assessment surgical” AND “wound infection OR surgical site infection” Risk of bias for individual studies was assessed in duplicate (VDC (Supplementary File 1). and GL) using the methodological index for non-randomized All gray literature publications (i.e., reports, theses, conference studies (MINORS) (13). Differences between the two reviewers proceedings, bibliographies, commercial documentations, were resolved through consensus and discussion with another and official documents not published commercially) were author (AZ). The total score for this 12-item instrument ranges excluded. Only studies on neonates (<44 wks gestational 0–24 points with a validated “gold standard” cut-off of 19.8. age) and/or neonates admitted to the NICU following Two authors (FM and AZ) independently evaluated cervical/thoracic/abdominal surgery published since 2,000 were the present systematic reviews and meta-analysis using A included. Case reports, case series with <10 patients, animal Measurement Toll to Assess Systematic Reviews (AMSTAR) Abbreviations: SSI, surgical site infection; NICU, neonatal intensive care unit. (14). The PRISMA checklist of our study was then completed (8). Frontiers in Pediatrics | www.frontiersin.org 2 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 1 | Diagram of workflow in the systematic review and meta-analysis. RESULTS database (16). No randomized studies were included. The papers included reported 946 cases of SSI out of 16,442 patients (5.7%). Systematic Review The distribution of surgical districts is significantly different Of the 885 abstracts analyzed, 48 full articles, for a total of between patients who developed SSI and those who did not 27,760 patients (16,517 males, 59.5%) met our inclusion criteria (Table 3). SSI development was significantly associated with (2, 15–61) (Figure 1). The overall incidence of SSI was 5.6% (n abdominal surgery (288/2,059 cases, 13.9%) in comparison with = 1,564) with a slight prevalence of male gender (61.8%) and other surgical districts. In 13,845 patients the surgical district premature babies (77.4%, gestational age at birth: 33 ± 7 weeks). was not specified. When reported, the most common type of The majority of neonates with SSI had gastrointestinal and/or abdominal surgery was laparotomy for congenital abdominal wall colorectal surgery (95.4%), followed by thoracic (3.0%), and other defect (601 cases), necrotizing enterocolitis (133), malrotation (1.6%) procedures. (33), small bowel atresia (34), volvulus (17), or not specified congenital bowel obstruction (418). Comparative Studies We analyzed 10 comparative studies (Tables 2a,b) (16–18, 22, 24, Meta-Analysis 34, 45, 47, 51, 60). Among these articles, there were only two The meta-analysis of the 10 comparative studies (16–18, 22, 24, prospective cohort studies (45, 60) and one national prospective 34, 45, 47, 51, 60) showed that there was a slight albeit significant Frontiers in Pediatrics | www.frontiersin.org 3 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates Frontiers in Pediatrics | www.frontiersin.org 4 March 2019 | Volume 7 | Article 101 TABLE 2a | Studies comparing SSI versus no-SSI neonates (preoperative data). References Year Type of SSI (No.) [%] Gestational age Birth weight (grams) Preoperative hospital Preoperative sepsis Preoperative study (weeks) stay (days) (No.) [%] antibiotics prophylaxis (No.) [%] SSI No-SSI SSI No-SSI SSI No-SSI SSI No-SSI SSI No-SSI § § § § Garcia et al. (24) 2005 R 125/279 [44.8] 38 (26–41) 36 (24–40) 2,700 2,108 2 (1–119) 2 (1–105) 77 [61.6] 72 [46.7] n.r. n.r. § § (625–4,200) (700–4,200) Baird et al. (16) 2012 PD 48/395 [12.1] 36 (r 30–40) 36 (r 25–41) n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. § § § § Rojo R (47) 2012 R 40/90 [44.4] 32 (25–40) 34 (24–40) 2,121 ± 945 2,546 ± 1,179 3 (0–90) 0.25 (0–120) 20 [50] 20 [40] 36 [90] 40 [80] # # Lejus et al. (34) 2013 R 11/286 [3.8] 37 (35–38) 38 (37–39) 2,530 3,000 n.r. n.r. 3 [27.3] 18 [6.6] 7 [63.6] 94 [34.2] # # (2,340–3,115) (2,719–3,500) Segal et al. (51) 2014 R 31/498 [6.2] 33 ± 6 33 ± 6 2,190 ± 1,127 2,152 ± 1,158 n.r. n.r. n.r. n.r. n.r. n.r. # # Battin M (18) 2016 R 10/60 [16.7] 30 (24–36) 34 (26–37) 1,002 2,170 n.r. n.r. n.r. n.r. 7 [70] 41 [84] # # (750–2,633) (970–2,875) Clements et al. (22) 2016 R 58/188 [30.8] 33 (r 24–40) 33 (r 23–42) 2,042 ± 1,165 1,993 ± 1,156 43.8 27.2 n.r. n.r. 27 [47] 68 [52] # # Prasad et al. (45) 2016 P 38/738 [5.1] 37 (34–38) 38 (36–39) 2,537 2,945 n.r. n.r. n.r. n.r. n.r. n.r. # # (1,955–3,265) (2,365–3,400) Bartz-Kurycki et al. (17) 2018 R 542/13,589 [3.9] n.r. n.r. n.r. n.r. n.r. n.r. 27 [4.9] 274 [2.1] n.r. n.r. # # Woldemicael et al. (60) 2018 P 43/319 [13.5] n.r. n.r. 2,121 ± 887 2,083 ± 1,082 7 (4–17) 3 (1–15) n.r. n.r. n.r. n.r. § # R, retrospective; PD, prospective database; P, prospective cohort study; n.r, not reported; , median (range); , median (IQR); r, range. Catania et al. Surgical Site Infection in Neonates TABLE 2b | Studies comparing SSI vs. no-SSI neonates (intra and postoperative data). References Age at surgery Operative time Number of Length of hospital (days) (minutes) procedures stay (days) SSI No-SSI SSI No-SSI SSI No-SSI SSI No-SSI § § Garcia et al. (24) n.r. n.r. 75 (20–240) 50 (10–300) n.r. n.r. n.r. n.r. Baird et al. (16) n.r. n.r. n.r. n.r. n.r. n.r. 95.9 (r 21–349) 41.6 (r 1–194) § § Rojo et al. (47) 21 (0–120) 12.5 (0–150) 100.8 ± 49.6 108 ± 51.6 n.r. n.r. n.r. n.r. # # # # Lejus et al. (34) 7 (2–14) 11 (0–20) 70 (64–123) 44 (22–79) n.r. n.r. n.r. n.r. # # # # # # Segal et al. (51) 85 (5–120) 11 (4–52) n.r. n.r. 2 (1–4) 1 (1–2) 79 (34–131) 25 (9–70) # # # # Battin et al. (18) 10 (2–81) 5 (2–12) 110 (60–134) 68 (53–96) n.r. n.r. n.r. n.r. Clements et al. (22) n.r. n.r. 108 ± 62 86 ± 58 2.44 ± 1.33 (r 1–6) 1.42 ± 0.73 (r 1–5) n.r. n.r. # # Prasad et al. (45) 5.5 (2–14.5) 5 (2–11) n.r. n.r. n.r. n.r. n.r. n.r. # # Bartz-Kurycki et al. (17) n.r. n.r. 78 (46–132) 64 (34–112) n.r. n.r. n.r. n.r. # # # # Woldemicael et al. (60) 8 (5–28) 6 (2–45) n.r. n.r. n.r. n.r. 40 (28–124) 26.5 (14–76) § # n.r., not reported; , median (range); median (IQR); r, range. comparison with those without SSI (SSI 93.1 ± 42.6 days vs. no TABLE 3 | Incidence of SSI according to the surgical district. SSI 45.8 ± 20.6; p < 0.00001, MD 36.45, 95% CI [31.21, 41.68], I Surgical districts SSI No-SSI p = 94%; Figure 10). (n) (n) Neck 6 78 p < 0.01 DISCUSSION Thorax 21 280 Abdomen 288 1,771 The overall rate of SSI in adult and pediatric patients is Pelvis 4 115 ∼ 2–5% and SSI are associated with increased morbidity, Perineum 3 31 mortality, healthcare costs, and length of hospital stay ( 3, 62). Not specified 624 13,221 Risk factors for SSI have been identified in predominantly Total 946 15,496 adult populations and include advanced age, hyperglycemia, malnutrition, co-morbidities, risk indices, patient frailty, prior infections, complexity of surgery, increased operative time, and increased blood loss during surgery (5, 45). With regard to difference between neonates with and without SSI for gestational children, certain surgical disciplines (cardiovascular, general age (34.2 ± 2.4 weeks vs. 34.7 ± 2.3; p < 0.00001, MD −1.02, surgery, neurosurgery, and orthopedics) were associated with 95% CI [−1.22, −0.82], I = 86%; Figure 2) and birth weight increased risk of developing an SSI (4). SSI development (2,171 ± 479 grams vs. 2,384 ± 411; p < 0.00001, MD −0.29, substantially increases the clinical and economic burden of 95% CI [−0.35, −0.23], I = 86%; Figure 3). Neonates with surgery, because of prolonged hospitalization of the patient, SSI were older at surgery compared to those without SSI (28.4 diagnostic tests, and treatment. Moreover, SSI negatively impact ± 24.4 days vs. 16.7 ± 14.3; p < 0.00001, MD 3.24, 95% CI on patient physical and mental health as well as on loss of [2.55, 3.93], I = 98%; Figure 4). The other main predictive earnings during recovery (63, 64). factors for the development of an SSI were length of surgical Our study shows that neonates undergoing abdominal surgery procedure (SSI 96.7 ± 11.2 min vs. no SSI 71.2 ± 20.8; p < are at high risk of SSI and that age at surgery and length of 0.00001, MD 15.82, 95% CI [14.06, 17.58], I = 85%; Figure 5), procedure are the main predictors of SSI in those admitted number of procedure per patient (SSI 2.3 ± 0.1 procedures vs. to NICU. Similarly, male gender and gestational age may be no SSI 1.3 ± 0.1; p < 0.00001, MD 1.00, 95% CI [0.79, 1.22], I associated to the development of SSI, but the present data are = 0%; Figure 6), length of preoperative hospital stay (SSI 21.3 not conclusive. ± 11.4 days vs. no SSI 21.0 ± 13.5; p < 0.00001, MD 3.17, 95% Although there is an abundance of literature on SSI in adults, CI [2.13, 4.21], I = 29%; Figure 7), and preoperative systemic there is a lack of studies having examined risk factors for SSI in infection (SSI 127/718 neonates, 17.7% vs. no SSI 384/13,526, neonates undergoing surgical interventions. 2.8%; p < 0.00001, OR 2.07, 95% CI [1.54, 2.78], I = 7%; In the present systematic review of the literature on more Figure 8). Conversely preoperative antibiotics prophylaxes were than 27,000 patients, we found an incidence of SSI of 5.5%. not significantly associated with a reduced development of SSI Interestingly, the overall rate of SSI in the neonatal age group (SSI 77/119 neonates, 64.7% vs. no SSI 243/505, 48.1%; p = 0.63, in our review is comparable to the rates reported in the older OR 1.12, 95% CI [0.70, 1.80], I = 53%; Figure 9). As expected, pediatric age group (51, 65, 66). This finding suggests that neonates with SSI showed a significant lengthened hospital stay in neonates may be less prone to SSI than it might be expected based Frontiers in Pediatrics | www.frontiersin.org 5 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 2 | Forest plot comparison of gestational age at birth of neonates with or without postoperative SSI. FIGURE 3 | Forest plot comparison of birth weight of neonates with or without postoperative SSI. FIGURE 4 | Forest plot comparison of age at procedure of neonates with or without postoperative SSI. FIGURE 5 | Forest plot comparison of length of procedure of neonates with or without postoperative SSI. Frontiers in Pediatrics | www.frontiersin.org 6 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 6 | Forest plot comparison of number of procedure per patient in neonates with or without postoperative SSI. FIGURE 7 | Forest plot comparison of preoperative hospital stay in neonates with or without postoperative SSI. FIGURE 8 | Forest plot comparison of preoperative systemic infection in neonates with or without postoperative SSI. FIGURE 9 | Forest plot comparison of preoperative antibiotic prophylaxis in neonates with or without postoperative SSI. on their alleged fragility, as they represent a special population of surgical intervention, the vast majority of infants underwent that is thought to be at higher risk for infection due to their gastrointestinal surgery (96%). In particular, abdominal surgery immature immune systems (6, 67, 68). was significantly associated with an increased risk of SSI (23, 54). According to our study, premature infants represent The most common type of surgical intervention described in a significant proportion of infants who require surgical the included articles was laparotomy for congenital abdominal interventions (51), and this is confirmed by the overall wall defects, necrotizing enterocolitis, or congenital bowel prevalence of SSI in this cohort (77%). When examining the type obstruction. This surgical procedure is known to compromise Frontiers in Pediatrics | www.frontiersin.org 7 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 10 | Forest plot comparison of length of hospital stay in neonates with or without postoperative SSI. TABLE 4 | Risk of bias assessment for individual studies using methodological index for nonrandomized studies (MINORS) (13). Item Garcia Bair et al. Rojo et al. Lejus Segal et al. Battin Clements Prasad et al. Bartz-Kurycki Woldemicael et al. (24) (16) (47) et al. (34) (51) (18) et al. (22) (45) et al. (17) et al. (60) 1. A clearly stated aim 2 2 2 2 2 2 2 2 2 2 2. Inclusion of consecutive 2 2 2 2 2 2 2 2 2 2 patients 3. Prospective collection of 0 2 0 0 0 0 0 2 0 2 data 4. Endpoints appropriate to the 2 2 2 2 2 2 2 2 2 2 aim of the study 5. Unbiased assessment of the 0 0 0 0 0 0 0 0 0 0 study endpoint 6. Follow-up period 0 0 0 0 0 0 0 0 0 0 appropriate to the aim of the study 7. Loss to follow-up less than 0 0 0 0 0 0 0 0 0 0 5% 8. Prospective calculation of 0 0 0 0 0 0 0 0 0 0 the study size 9. An adequate control group 2 2 2 2 2 2 2 2 2 2 10. Contemporary groups 2 2 2 2 2 2 2 2 2 2 11. Baseline equivalence of 1 2 1 2 2 2 2 2 2 2 groups 12. Adequate statistical 2 2 2 2 2 2 2 2 2 2 analyses Total score 13 16 13 14 14 14 14 16 14 16 the integrity of the gastrointestinal tract and to potentially result patients who developed SSI. Likewise, also a lower birth weight in bacterial translocation. Surgical wounds following a neonatal was associated with an increased risk of SSI in the included laparotomy are classified, at best, as clean-contaminated wounds, studies, even if the SSI group had an older age at the time which justify the highest prevalence of SSI in this sub-group (22). of their procedures compared to the group who neonates who The Canadian Pediatric Surgery Network recently reported an did not develop SSI. Moreover, this group also had a longer overall 15% incidence of SSI in infants with gastroschisis who preoperative length of stay and it likely required a greater number underwent immediate (<6 h after birth) or delayed closure (55). of invasive diagnostic and therapeutic procedures per patient, For this reason, to reduce time of visceral exposure, the authors as already reported by Garcia and Lejus (24, 34). In fact, this have proposed the gastroschisis sutureless closure, as it is also study confirmed a significant difference in number of surgical associated with a reduced risk of SSI (54). procedures between neonates with SSI and those without. This To define the risk factors that are to be considered by the figure may be related to the severity of illness, with sicker patients surgeon to estimate the risk of SSI at the time of neonatal surgery, being more likely to require additional procedures, although one we selected comparative studies that analyzed neonates with third of SSI did occur after a single or first procedure. A long or without SSI. Interestingly, we observed that neonates who preoperative admission is a risk factor for SSI, as it is proportional developed SSI had a younger GA compared to those who did to the severity of the underlying clinical conditions, the need for not. This was a validation of the results from the systematic invasive devices and treatments (included prolonged antibiotics), review that showed a high prevalence of prematurity among and it promotes nosocomial flora colonization. Furthermore, Frontiers in Pediatrics | www.frontiersin.org 8 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates neonates admitted to NICU are highly susceptible to nosocomial As a consequence, in our meta-analysis, none of the studies infections. As an expected consequence, the presence of a reached the gold standard cut-off on MINORS of 19.8 out of 24 systemic infection significantly influenced the SSI incidence in (Table 4). However, when independently assessed by two authors our study. using AMSTAR, the present systematic reviews and meta- Our present study also highlighted that the length of surgery analysis received a relevant score (Supplementary File 2) and the is another risk factor for SSI. Length of surgery was not identified PRISMA checklist was completed (Supplementary File 3). by all studies as a risk factor for SSI, and our meta-analysis confirmed the findings of Clements and coworkers who found a CONCLUSION longer operative time in patients developing SSI (22). Prolonged visceral exposure may negatively impact on surgical outcome In conclusion, SSI is a significant complication in neonates as consequence of skin contamination. Furthermore, the longer admitted to NICU that can negatively impact their outcome the operative time the deeper the surgical stress response, as the by prolonging hospital stay and increasing the risk for further invasiveness of surgery and the length of procedure significantly complications, such as potentially fatal sepsis. Younger and correlated to oxidative stress activation and cortisol response smaller neonates at birth, those requiring longer or multiple (69–71). The latter may have an impact on postoperative operative procedures, and those with prolonged preoperative outcome, such as the development of infectious complications, hospital stay and preoperative sepsis are at higher risk for SSI. including SSI. These patients require special attention with close monitoring This study did not show any difference in preoperative during their post-operative course. Given the lack of evidence in antibiotic administration between neonates who developed SSI the literature, well-designed prospective studies on large cohorts and those who did not. Whilst standardized preoperative of neonates may help setting up specific guidelines for the antibiotic protocols in the adult population have shown to prevention and treatment of SSI in this particular population. reduce the rate of SSI, a consensus is lacking among pediatric surgeons regarding preoperative antibiotic prophylaxis especially DATA AVAILABILITY in neonates (1, 4). The different definitions of antibiotic prophylaxis and antibiotic regimen used in the analyzed studies All datasets generated for this study are included in the may have led to our findings. The isolation of skin flora from manuscript and/or the Supplementary Files. a large number of wound cultures suggests that standardization of preoperative prophylaxis could potentially have an impact on the rate of SSI as has previously been demonstrated in pediatric AUTHOR CONTRIBUTIONS patients (72, 73). VC, AB, GL, FM, and AZ: conception and design, analysis and interpretation, drafting, final approval. VC, AB, and GL: data LIMITATIONS OF THE STUDY acquisition. VC, GL, FM, and AZ: quality assessment. GL, FM, Our study has some limitations. The first relates to the relative and AZ: revision. small number of studies available for the meta-analysis, with only two prospective cohort study and one national prospective FUNDING database included. Nonetheless, the population of neonates reported in the studies was not small, with more than 27,000 This work was supported by the Canadian Institute of Health neonates included. Research (CIHR) – SickKids Foundation New Investigator The second limitation is that we could not analyze important Research Grant (NI18-1270R). variables, such as the use of adequate antibiotic prophylaxis, as they were not reported in the few studies selected in our analysis. Finally, the third limitation is the relative heterogeneity SUPPLEMENTARY MATERIAL of the patient population: although we tried to limit the study to neonates, we included both patients with a post-conceptional The Supplementary Material for this article can be found age below 44 weeks and infants admitted in the NICU following online at: https://www.frontiersin.org/articles/10.3389/fped. abdominal, cervical, and thoracic surgery. 2019.00101/full#supplementary-material REFERENCES 3. Ban KA, Minei JP, Laronga C, Harbrecht BG, Jensen EH, Fry DE, et al. American college of surgeons and surgical infection society: surgical site 1. Vu LT, Vittinghoff E, Nobuhara KK, Farmer DL, Lee H. 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Woldemicael AY, Bradley S, Pardy C, Richards J, Trerotoli P, Giuliani S. be construed as a potential conflict of interest. Surgical site infection in a tertiary neonatal surgery centre. Eur J Pediatr Surg. (2018). doi: 10.1055/s-0038-1636916. [Epub ahead of print]. Copyright © 2019 Catania, Boscarelli, Lauriti, Morini and Zani. This is an open- 61. Wu Y, Lai W, Pei J, Zhao Y, Wang Q, Xiang B. Hyperglycemia and access article distributed under the terms of the Creative Commons Attribution its association with clinical outcomes in postsurgical neonates and small License (CC BY). The use, distribution or reproduction in other forums is permitted, infants in the intensive care unit. J Pediatr Surg. (2016) 51:1142–5. provided the original author(s) and the copyright owner(s) are credited and that the doi: 10.1016/j.jpedsurg.2016.01.001 original publication in this journal is cited, in accordance with accepted academic 62. Kulaylat AN, Engbrecht BW, Rocourt DV, Rinaldi JM, Santos MC, Cilley practice. No use, distribution or reproduction is permitted which does not comply RE, et al. Measuring surgical site infections in children: comparing clinical, with these terms. Frontiers in Pediatrics | www.frontiersin.org 11 March 2019 | Volume 7 | Article 101 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Frontiers in Pediatrics Pubmed Central

Risk Factors for Surgical Site Infection in Neonates: A Systematic Review of the Literature and Meta-Analysis

Frontiers in Pediatrics , Volume 7 – Mar 29, 2019

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Abstract

SYSTEMATIC REVIEW published: 29 March 2019 doi: 10.3389/fped.2019.00101 Risk Factors for Surgical Site Infection in Neonates: A Systematic Review of the Literature and Meta-Analysis 1 2 3 2 Vincenzo Davide Catania , Alessandro Boscarelli , Giuseppe Lauriti , Francesco Morini and Augusto Zani * Division of General and Thoracic Surgery, The Hospital for Sick Children, University of Toronto, Toronto, ON, Canada, Neonatal Surgery Unit, Department of Medical and Surgical Neonatology, Bambino Gesù Children’s Hospital, IRCCS, Rome, Italy, Department of Pediatric Surgery, Spirito Santo Hospital and G. d’Annunzio University of Chieti and Pescara, Chieti, Italy Purpose: Surgical site infections (SSI) contribute to postoperative morbidity and mortality in children. Our aim was to evaluate the prevalence and identify risk factors for SSI in neonates. Methods: Using a defined strategy, three investigators searched articles on neonatal SSI published since 2000. Studies on neonates and/or patients admitted to neonatal Edited by: Oliver J. Muensterer, intensive care unit following cervical/thoracic/abdominal surgery were included. Risk Johannes Gutenberg University factors were identified from comparative studies. Meta-analysis was conducted Mainz, Germany according to PRISMA guidelines using RevMan 5.3. Data are (mean ± SD) prevalence. Reviewed by: Maximilian Weniger, Results: Systematic review—of 885 abstracts screened, 48 studies (27,760 neonates) Massachusetts General Hospital and were included. The incidence of SSI was 5.6% (1,564 patients). SSI was more frequent in Harvard Medical School, United States males (61.8%), premature babies (77.4%), and following gastrointestinal surgery (95.4%). Ana Catarina Fragoso, Meta-analysis—10 comparative studies (16,442 neonates; 946 SSI 5.7%) showed that Universidade do Porto, Portugal predictive factors for SSI development were gestational age, birth weight, age at surgery, *Correspondence: Augusto Zani length of surgical procedure, number of procedure per patient, length of preoperative augusto.zani@sickkids.ca hospital stay, and preoperative sepsis. Conversely, preoperative antibiotic use was not significantly associated with development of SSI. Specialty section: This article was submitted to Conclusions: Younger neonates and those undergoing abdominal procedures are at Pediatric Surgery, higher risk for SSI. Given the lack of evidence-based literature, prospective studies may a section of the journal Frontiers in Pediatrics help determine the risk factors for SSI in neonates. Received: 06 January 2019 Keywords: newborn, wound infection, neonatal surgery, risk factors, systematic review, meta-analysis Accepted: 05 March 2019 Published: 29 March 2019 Citation: INTRODUCTION Catania VD, Boscarelli A, Lauriti G, Morini F and Zani A (2019) Risk Surgical site infections (SSI) are infections that occur postoperatively in the area of the body where Factors for Surgical Site Infection in the surgery took place. SSI can be superficial and involve the skin only, or more serious and Neonates: A Systematic Review of the involve other tissues, organs, or implanted material. SSI are among the most common hospital Literature and Meta-Analysis. acquired diseases and are an important cause of morbidity and mortality in all patients, including Front. Pediatr. 7:101. doi: 10.3389/fped.2019.00101 neonates and infants (1, 2). Frontiers in Pediatrics | www.frontiersin.org 1 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates TABLE 1 | Defined search strategy. Whilst the incidence and risk factors for SSI in adults and more recently in children have been defined and management Publication guidelines have been established (3, 4), yet little is known about SSI in neonates and infants. Sources PubMed, Medline, Cochrane Collaboration, The incidence of SSI is 2–5% in adult patients undergoing Embase, Web of Science, Ovid inpatient surgery (3). Risk factors associated with SSI included Language Any co-morbidities, advanced age, risk indices, patient frailty, and Date Since 2000 surgery complexity (5). Subject Human studies In children the rate of SSI ranged from 2.5 to 5.4% and Study type Retrospective dirty wounds, inpatient status, increased duration of surgery, Prospective or certain surgical disciplines (cardiovascular, general surgery, Case control neurosurgery, and orthopedics) were associated with increased Cohort risk of developing an SSI (4). Excluded Grey Literature Previous studies have shown that the incidence of SSI in Case reports neonates and infants can be as high as 17% (1, 2). In this Case series <10 patients population of patients, several conditions have been reported Letters to be associated with an increased risk of SSI, including Editorials admission to the neonatal intensive care unit (NICU), history Keywords Neonate, Neonatal, Newborn of prematurity, low birth weight, mechanical ventilation, Surgery central venous access, associated co-morbidities, prolonged Surgical site infection antibiotic administration, postsurgical hyperglycemia, and Surgical wound infection neutropenia (1, 2, 6, 7). In the present study, we aimed to establish the incidence of SSI in neonates and to identifyprognostic factors that may studies, and opinion articles were excluded. The full text of help stratify which neonates are at increased risk to develop the potentially eligible studies was retrieved and independently this complication. A better understanding of the causes leading assessed for eligibility by the same three investigators. Any to SSI could reduce their incidence, help define guidelines, and disagreement over the eligibility of particular studies was eventually improve outcome. resolved through discussion with the other two authors (FM and AZ). Outcome measures included demographic data, METHODS type and district of surgery, SSI development, preoperative systemic infection, preoperative antibiotic prophylaxis, length of To investigate the incidence and risk factors of SSI in neonates, procedure, and number of procedure per patient. Risk factors of we conducted a systematic review of the literature and SSI were identified from comparative studies. complemented it with a meta-analysis of comparative studies. Both the systematic review and the meta-analysis Statistical Analysis were drafted according to the Preferred Reporting Items Data were analyzed using GraphPad Prism 6.2 Macintosh for Systematic Reviews and Meta-Analyses (PRISMA) Version (10). Data were compared using Fisher’s exact test and statement (8). The protocol for this systematic review are expressed as mean ± SD. When median and range were was registered on PROSPERO—international prospective reported, mean± SD were estimated, as previously reported (11). register of systematic reviews (registration number: The meta-analysis was conducted with RevMan 5.3 (12), using CRD42017069003) (9). Using a defined search strategy, the fixed-effects model to produce risk ratio (RR) for categorical three investigators (VDC, AB, and GL) independently variables and mean differences (MD) for continuous variables, searched scientific databases (PubMed, Medline, Cochrane along with 95% confidence intervals (CI). We produced I values Collaboration, Embase, Web of Science, Ovid) using a to assess homogeneity and quantify the dispersion of effect sizes. combination of keywords (Table 1). MeSH headings and terms used were “neonate OR newborn” AND “surgery OR Quality Assessment surgical” AND “wound infection OR surgical site infection” Risk of bias for individual studies was assessed in duplicate (VDC (Supplementary File 1). and GL) using the methodological index for non-randomized All gray literature publications (i.e., reports, theses, conference studies (MINORS) (13). Differences between the two reviewers proceedings, bibliographies, commercial documentations, were resolved through consensus and discussion with another and official documents not published commercially) were author (AZ). The total score for this 12-item instrument ranges excluded. Only studies on neonates (<44 wks gestational 0–24 points with a validated “gold standard” cut-off of 19.8. age) and/or neonates admitted to the NICU following Two authors (FM and AZ) independently evaluated cervical/thoracic/abdominal surgery published since 2,000 were the present systematic reviews and meta-analysis using A included. Case reports, case series with <10 patients, animal Measurement Toll to Assess Systematic Reviews (AMSTAR) Abbreviations: SSI, surgical site infection; NICU, neonatal intensive care unit. (14). The PRISMA checklist of our study was then completed (8). Frontiers in Pediatrics | www.frontiersin.org 2 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 1 | Diagram of workflow in the systematic review and meta-analysis. RESULTS database (16). No randomized studies were included. The papers included reported 946 cases of SSI out of 16,442 patients (5.7%). Systematic Review The distribution of surgical districts is significantly different Of the 885 abstracts analyzed, 48 full articles, for a total of between patients who developed SSI and those who did not 27,760 patients (16,517 males, 59.5%) met our inclusion criteria (Table 3). SSI development was significantly associated with (2, 15–61) (Figure 1). The overall incidence of SSI was 5.6% (n abdominal surgery (288/2,059 cases, 13.9%) in comparison with = 1,564) with a slight prevalence of male gender (61.8%) and other surgical districts. In 13,845 patients the surgical district premature babies (77.4%, gestational age at birth: 33 ± 7 weeks). was not specified. When reported, the most common type of The majority of neonates with SSI had gastrointestinal and/or abdominal surgery was laparotomy for congenital abdominal wall colorectal surgery (95.4%), followed by thoracic (3.0%), and other defect (601 cases), necrotizing enterocolitis (133), malrotation (1.6%) procedures. (33), small bowel atresia (34), volvulus (17), or not specified congenital bowel obstruction (418). Comparative Studies We analyzed 10 comparative studies (Tables 2a,b) (16–18, 22, 24, Meta-Analysis 34, 45, 47, 51, 60). Among these articles, there were only two The meta-analysis of the 10 comparative studies (16–18, 22, 24, prospective cohort studies (45, 60) and one national prospective 34, 45, 47, 51, 60) showed that there was a slight albeit significant Frontiers in Pediatrics | www.frontiersin.org 3 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates Frontiers in Pediatrics | www.frontiersin.org 4 March 2019 | Volume 7 | Article 101 TABLE 2a | Studies comparing SSI versus no-SSI neonates (preoperative data). References Year Type of SSI (No.) [%] Gestational age Birth weight (grams) Preoperative hospital Preoperative sepsis Preoperative study (weeks) stay (days) (No.) [%] antibiotics prophylaxis (No.) [%] SSI No-SSI SSI No-SSI SSI No-SSI SSI No-SSI SSI No-SSI § § § § Garcia et al. (24) 2005 R 125/279 [44.8] 38 (26–41) 36 (24–40) 2,700 2,108 2 (1–119) 2 (1–105) 77 [61.6] 72 [46.7] n.r. n.r. § § (625–4,200) (700–4,200) Baird et al. (16) 2012 PD 48/395 [12.1] 36 (r 30–40) 36 (r 25–41) n.r. n.r. n.r. n.r. n.r. n.r. n.r. n.r. § § § § Rojo R (47) 2012 R 40/90 [44.4] 32 (25–40) 34 (24–40) 2,121 ± 945 2,546 ± 1,179 3 (0–90) 0.25 (0–120) 20 [50] 20 [40] 36 [90] 40 [80] # # Lejus et al. (34) 2013 R 11/286 [3.8] 37 (35–38) 38 (37–39) 2,530 3,000 n.r. n.r. 3 [27.3] 18 [6.6] 7 [63.6] 94 [34.2] # # (2,340–3,115) (2,719–3,500) Segal et al. (51) 2014 R 31/498 [6.2] 33 ± 6 33 ± 6 2,190 ± 1,127 2,152 ± 1,158 n.r. n.r. n.r. n.r. n.r. n.r. # # Battin M (18) 2016 R 10/60 [16.7] 30 (24–36) 34 (26–37) 1,002 2,170 n.r. n.r. n.r. n.r. 7 [70] 41 [84] # # (750–2,633) (970–2,875) Clements et al. (22) 2016 R 58/188 [30.8] 33 (r 24–40) 33 (r 23–42) 2,042 ± 1,165 1,993 ± 1,156 43.8 27.2 n.r. n.r. 27 [47] 68 [52] # # Prasad et al. (45) 2016 P 38/738 [5.1] 37 (34–38) 38 (36–39) 2,537 2,945 n.r. n.r. n.r. n.r. n.r. n.r. # # (1,955–3,265) (2,365–3,400) Bartz-Kurycki et al. (17) 2018 R 542/13,589 [3.9] n.r. n.r. n.r. n.r. n.r. n.r. 27 [4.9] 274 [2.1] n.r. n.r. # # Woldemicael et al. (60) 2018 P 43/319 [13.5] n.r. n.r. 2,121 ± 887 2,083 ± 1,082 7 (4–17) 3 (1–15) n.r. n.r. n.r. n.r. § # R, retrospective; PD, prospective database; P, prospective cohort study; n.r, not reported; , median (range); , median (IQR); r, range. Catania et al. Surgical Site Infection in Neonates TABLE 2b | Studies comparing SSI vs. no-SSI neonates (intra and postoperative data). References Age at surgery Operative time Number of Length of hospital (days) (minutes) procedures stay (days) SSI No-SSI SSI No-SSI SSI No-SSI SSI No-SSI § § Garcia et al. (24) n.r. n.r. 75 (20–240) 50 (10–300) n.r. n.r. n.r. n.r. Baird et al. (16) n.r. n.r. n.r. n.r. n.r. n.r. 95.9 (r 21–349) 41.6 (r 1–194) § § Rojo et al. (47) 21 (0–120) 12.5 (0–150) 100.8 ± 49.6 108 ± 51.6 n.r. n.r. n.r. n.r. # # # # Lejus et al. (34) 7 (2–14) 11 (0–20) 70 (64–123) 44 (22–79) n.r. n.r. n.r. n.r. # # # # # # Segal et al. (51) 85 (5–120) 11 (4–52) n.r. n.r. 2 (1–4) 1 (1–2) 79 (34–131) 25 (9–70) # # # # Battin et al. (18) 10 (2–81) 5 (2–12) 110 (60–134) 68 (53–96) n.r. n.r. n.r. n.r. Clements et al. (22) n.r. n.r. 108 ± 62 86 ± 58 2.44 ± 1.33 (r 1–6) 1.42 ± 0.73 (r 1–5) n.r. n.r. # # Prasad et al. (45) 5.5 (2–14.5) 5 (2–11) n.r. n.r. n.r. n.r. n.r. n.r. # # Bartz-Kurycki et al. (17) n.r. n.r. 78 (46–132) 64 (34–112) n.r. n.r. n.r. n.r. # # # # Woldemicael et al. (60) 8 (5–28) 6 (2–45) n.r. n.r. n.r. n.r. 40 (28–124) 26.5 (14–76) § # n.r., not reported; , median (range); median (IQR); r, range. comparison with those without SSI (SSI 93.1 ± 42.6 days vs. no TABLE 3 | Incidence of SSI according to the surgical district. SSI 45.8 ± 20.6; p < 0.00001, MD 36.45, 95% CI [31.21, 41.68], I Surgical districts SSI No-SSI p = 94%; Figure 10). (n) (n) Neck 6 78 p < 0.01 DISCUSSION Thorax 21 280 Abdomen 288 1,771 The overall rate of SSI in adult and pediatric patients is Pelvis 4 115 ∼ 2–5% and SSI are associated with increased morbidity, Perineum 3 31 mortality, healthcare costs, and length of hospital stay ( 3, 62). Not specified 624 13,221 Risk factors for SSI have been identified in predominantly Total 946 15,496 adult populations and include advanced age, hyperglycemia, malnutrition, co-morbidities, risk indices, patient frailty, prior infections, complexity of surgery, increased operative time, and increased blood loss during surgery (5, 45). With regard to difference between neonates with and without SSI for gestational children, certain surgical disciplines (cardiovascular, general age (34.2 ± 2.4 weeks vs. 34.7 ± 2.3; p < 0.00001, MD −1.02, surgery, neurosurgery, and orthopedics) were associated with 95% CI [−1.22, −0.82], I = 86%; Figure 2) and birth weight increased risk of developing an SSI (4). SSI development (2,171 ± 479 grams vs. 2,384 ± 411; p < 0.00001, MD −0.29, substantially increases the clinical and economic burden of 95% CI [−0.35, −0.23], I = 86%; Figure 3). Neonates with surgery, because of prolonged hospitalization of the patient, SSI were older at surgery compared to those without SSI (28.4 diagnostic tests, and treatment. Moreover, SSI negatively impact ± 24.4 days vs. 16.7 ± 14.3; p < 0.00001, MD 3.24, 95% CI on patient physical and mental health as well as on loss of [2.55, 3.93], I = 98%; Figure 4). The other main predictive earnings during recovery (63, 64). factors for the development of an SSI were length of surgical Our study shows that neonates undergoing abdominal surgery procedure (SSI 96.7 ± 11.2 min vs. no SSI 71.2 ± 20.8; p < are at high risk of SSI and that age at surgery and length of 0.00001, MD 15.82, 95% CI [14.06, 17.58], I = 85%; Figure 5), procedure are the main predictors of SSI in those admitted number of procedure per patient (SSI 2.3 ± 0.1 procedures vs. to NICU. Similarly, male gender and gestational age may be no SSI 1.3 ± 0.1; p < 0.00001, MD 1.00, 95% CI [0.79, 1.22], I associated to the development of SSI, but the present data are = 0%; Figure 6), length of preoperative hospital stay (SSI 21.3 not conclusive. ± 11.4 days vs. no SSI 21.0 ± 13.5; p < 0.00001, MD 3.17, 95% Although there is an abundance of literature on SSI in adults, CI [2.13, 4.21], I = 29%; Figure 7), and preoperative systemic there is a lack of studies having examined risk factors for SSI in infection (SSI 127/718 neonates, 17.7% vs. no SSI 384/13,526, neonates undergoing surgical interventions. 2.8%; p < 0.00001, OR 2.07, 95% CI [1.54, 2.78], I = 7%; In the present systematic review of the literature on more Figure 8). Conversely preoperative antibiotics prophylaxes were than 27,000 patients, we found an incidence of SSI of 5.5%. not significantly associated with a reduced development of SSI Interestingly, the overall rate of SSI in the neonatal age group (SSI 77/119 neonates, 64.7% vs. no SSI 243/505, 48.1%; p = 0.63, in our review is comparable to the rates reported in the older OR 1.12, 95% CI [0.70, 1.80], I = 53%; Figure 9). As expected, pediatric age group (51, 65, 66). This finding suggests that neonates with SSI showed a significant lengthened hospital stay in neonates may be less prone to SSI than it might be expected based Frontiers in Pediatrics | www.frontiersin.org 5 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 2 | Forest plot comparison of gestational age at birth of neonates with or without postoperative SSI. FIGURE 3 | Forest plot comparison of birth weight of neonates with or without postoperative SSI. FIGURE 4 | Forest plot comparison of age at procedure of neonates with or without postoperative SSI. FIGURE 5 | Forest plot comparison of length of procedure of neonates with or without postoperative SSI. Frontiers in Pediatrics | www.frontiersin.org 6 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 6 | Forest plot comparison of number of procedure per patient in neonates with or without postoperative SSI. FIGURE 7 | Forest plot comparison of preoperative hospital stay in neonates with or without postoperative SSI. FIGURE 8 | Forest plot comparison of preoperative systemic infection in neonates with or without postoperative SSI. FIGURE 9 | Forest plot comparison of preoperative antibiotic prophylaxis in neonates with or without postoperative SSI. on their alleged fragility, as they represent a special population of surgical intervention, the vast majority of infants underwent that is thought to be at higher risk for infection due to their gastrointestinal surgery (96%). In particular, abdominal surgery immature immune systems (6, 67, 68). was significantly associated with an increased risk of SSI (23, 54). According to our study, premature infants represent The most common type of surgical intervention described in a significant proportion of infants who require surgical the included articles was laparotomy for congenital abdominal interventions (51), and this is confirmed by the overall wall defects, necrotizing enterocolitis, or congenital bowel prevalence of SSI in this cohort (77%). When examining the type obstruction. This surgical procedure is known to compromise Frontiers in Pediatrics | www.frontiersin.org 7 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates FIGURE 10 | Forest plot comparison of length of hospital stay in neonates with or without postoperative SSI. TABLE 4 | Risk of bias assessment for individual studies using methodological index for nonrandomized studies (MINORS) (13). Item Garcia Bair et al. Rojo et al. Lejus Segal et al. Battin Clements Prasad et al. Bartz-Kurycki Woldemicael et al. (24) (16) (47) et al. (34) (51) (18) et al. (22) (45) et al. (17) et al. (60) 1. A clearly stated aim 2 2 2 2 2 2 2 2 2 2 2. Inclusion of consecutive 2 2 2 2 2 2 2 2 2 2 patients 3. Prospective collection of 0 2 0 0 0 0 0 2 0 2 data 4. Endpoints appropriate to the 2 2 2 2 2 2 2 2 2 2 aim of the study 5. Unbiased assessment of the 0 0 0 0 0 0 0 0 0 0 study endpoint 6. Follow-up period 0 0 0 0 0 0 0 0 0 0 appropriate to the aim of the study 7. Loss to follow-up less than 0 0 0 0 0 0 0 0 0 0 5% 8. Prospective calculation of 0 0 0 0 0 0 0 0 0 0 the study size 9. An adequate control group 2 2 2 2 2 2 2 2 2 2 10. Contemporary groups 2 2 2 2 2 2 2 2 2 2 11. Baseline equivalence of 1 2 1 2 2 2 2 2 2 2 groups 12. Adequate statistical 2 2 2 2 2 2 2 2 2 2 analyses Total score 13 16 13 14 14 14 14 16 14 16 the integrity of the gastrointestinal tract and to potentially result patients who developed SSI. Likewise, also a lower birth weight in bacterial translocation. Surgical wounds following a neonatal was associated with an increased risk of SSI in the included laparotomy are classified, at best, as clean-contaminated wounds, studies, even if the SSI group had an older age at the time which justify the highest prevalence of SSI in this sub-group (22). of their procedures compared to the group who neonates who The Canadian Pediatric Surgery Network recently reported an did not develop SSI. Moreover, this group also had a longer overall 15% incidence of SSI in infants with gastroschisis who preoperative length of stay and it likely required a greater number underwent immediate (<6 h after birth) or delayed closure (55). of invasive diagnostic and therapeutic procedures per patient, For this reason, to reduce time of visceral exposure, the authors as already reported by Garcia and Lejus (24, 34). In fact, this have proposed the gastroschisis sutureless closure, as it is also study confirmed a significant difference in number of surgical associated with a reduced risk of SSI (54). procedures between neonates with SSI and those without. This To define the risk factors that are to be considered by the figure may be related to the severity of illness, with sicker patients surgeon to estimate the risk of SSI at the time of neonatal surgery, being more likely to require additional procedures, although one we selected comparative studies that analyzed neonates with third of SSI did occur after a single or first procedure. A long or without SSI. Interestingly, we observed that neonates who preoperative admission is a risk factor for SSI, as it is proportional developed SSI had a younger GA compared to those who did to the severity of the underlying clinical conditions, the need for not. This was a validation of the results from the systematic invasive devices and treatments (included prolonged antibiotics), review that showed a high prevalence of prematurity among and it promotes nosocomial flora colonization. Furthermore, Frontiers in Pediatrics | www.frontiersin.org 8 March 2019 | Volume 7 | Article 101 Catania et al. Surgical Site Infection in Neonates neonates admitted to NICU are highly susceptible to nosocomial As a consequence, in our meta-analysis, none of the studies infections. As an expected consequence, the presence of a reached the gold standard cut-off on MINORS of 19.8 out of 24 systemic infection significantly influenced the SSI incidence in (Table 4). However, when independently assessed by two authors our study. using AMSTAR, the present systematic reviews and meta- Our present study also highlighted that the length of surgery analysis received a relevant score (Supplementary File 2) and the is another risk factor for SSI. Length of surgery was not identified PRISMA checklist was completed (Supplementary File 3). by all studies as a risk factor for SSI, and our meta-analysis confirmed the findings of Clements and coworkers who found a CONCLUSION longer operative time in patients developing SSI (22). Prolonged visceral exposure may negatively impact on surgical outcome In conclusion, SSI is a significant complication in neonates as consequence of skin contamination. Furthermore, the longer admitted to NICU that can negatively impact their outcome the operative time the deeper the surgical stress response, as the by prolonging hospital stay and increasing the risk for further invasiveness of surgery and the length of procedure significantly complications, such as potentially fatal sepsis. Younger and correlated to oxidative stress activation and cortisol response smaller neonates at birth, those requiring longer or multiple (69–71). The latter may have an impact on postoperative operative procedures, and those with prolonged preoperative outcome, such as the development of infectious complications, hospital stay and preoperative sepsis are at higher risk for SSI. including SSI. These patients require special attention with close monitoring This study did not show any difference in preoperative during their post-operative course. Given the lack of evidence in antibiotic administration between neonates who developed SSI the literature, well-designed prospective studies on large cohorts and those who did not. Whilst standardized preoperative of neonates may help setting up specific guidelines for the antibiotic protocols in the adult population have shown to prevention and treatment of SSI in this particular population. reduce the rate of SSI, a consensus is lacking among pediatric surgeons regarding preoperative antibiotic prophylaxis especially DATA AVAILABILITY in neonates (1, 4). The different definitions of antibiotic prophylaxis and antibiotic regimen used in the analyzed studies All datasets generated for this study are included in the may have led to our findings. The isolation of skin flora from manuscript and/or the Supplementary Files. a large number of wound cultures suggests that standardization of preoperative prophylaxis could potentially have an impact on the rate of SSI as has previously been demonstrated in pediatric AUTHOR CONTRIBUTIONS patients (72, 73). VC, AB, GL, FM, and AZ: conception and design, analysis and interpretation, drafting, final approval. VC, AB, and GL: data LIMITATIONS OF THE STUDY acquisition. VC, GL, FM, and AZ: quality assessment. GL, FM, Our study has some limitations. The first relates to the relative and AZ: revision. small number of studies available for the meta-analysis, with only two prospective cohort study and one national prospective FUNDING database included. Nonetheless, the population of neonates reported in the studies was not small, with more than 27,000 This work was supported by the Canadian Institute of Health neonates included. Research (CIHR) – SickKids Foundation New Investigator The second limitation is that we could not analyze important Research Grant (NI18-1270R). variables, such as the use of adequate antibiotic prophylaxis, as they were not reported in the few studies selected in our analysis. Finally, the third limitation is the relative heterogeneity SUPPLEMENTARY MATERIAL of the patient population: although we tried to limit the study to neonates, we included both patients with a post-conceptional The Supplementary Material for this article can be found age below 44 weeks and infants admitted in the NICU following online at: https://www.frontiersin.org/articles/10.3389/fped. abdominal, cervical, and thoracic surgery. 2019.00101/full#supplementary-material REFERENCES 3. Ban KA, Minei JP, Laronga C, Harbrecht BG, Jensen EH, Fry DE, et al. American college of surgeons and surgical infection society: surgical site 1. Vu LT, Vittinghoff E, Nobuhara KK, Farmer DL, Lee H. 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Kulaylat AN, Engbrecht BW, Rocourt DV, Rinaldi JM, Santos MC, Cilley practice. No use, distribution or reproduction is permitted which does not comply RE, et al. Measuring surgical site infections in children: comparing clinical, with these terms. Frontiers in Pediatrics | www.frontiersin.org 11 March 2019 | Volume 7 | Article 101

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