Surgical Site Infection in Children with Neuromuscular Disorders after Laparoscopic Gastrostomy: A Propensity-Matched National Surgical Quality Improvement Program Pediatrics Database Analysis

Abstract

Background:

Prior studies have demonstrated that children with neuromuscular scoliosis have a higher incidence of infection after spine surgery. The purpose of the study is to determine whether children with neuromuscular disorders (NMDs) have higher rate of superficial surgical site infection (SSI) or increased hospital length of stay (LOS) compared with children without NMDs following laparoscopic gastrostomy creation, a common pediatric general surgery operation.

Patients and Methods:

We performed a retrospective propensity-matched analysis of laparoscopic gastrostomy creation in children from National Surgical Quality Improvement Program Pediatrics database (NSQIP-P) 2018–2019. Patients were stratified based on NMD status. We performed multivariable logistic regression and ordered logistic regression to estimate the odds ratio of superficial SSI within 30 days of surgery and increased LOS.

Results:

We screened 252,367 patients from the NSQIP-P 2018–2019 dataset. After applying inclusion and exclusion criteria and 1:1 propensity score-matching, there were 991 children with NMDs and 991 children without NMDs. Children with NMDs had higher prevalence of superficial SSI within 30 days of gastrostomy creation: 36 (3.63%) versus 18 (1.82%); p = 0.013. Children with NMDs had increased odds of having a superficial SSI within 30 days of laparoscopic gastrostomy tube (G-tube) placement compared with children without NMD (odds ratio [OR], 2.01; 95% confidence interval [CI], 1.13–3.58; p = 0.018). There was no difference in LOS based on NMD status.

Conclusion:

Children with NMDs have two-fold increased odds of superficial SSI after laparoscopic gastrostomy creation compared with children without NMDs. Children with NMDs should be the aim of targeted quality improvement initiatives to reduce infection risks.

Surgical site infections (SSIs) are responsible for up to 20% of health-care–acquired infections [1]. Although elevated body mass index (BMI) has been identified as a risk factor for SSI in pediatric general surgery patients, other independent risk factors have been understudied [2]. Specifically, the diagnosis of a neuromuscular disorder (NMD) has been understudied as a risk factor for SSI or other adverse infectious outcomes in children. Adult veterans with a diagnosis of paralysis have higher odds of becoming infected with methicillin-resistant Staphylococcus aureus (MRSA), although this association has not been reported in children [3]. It is important to understand whether children with NMDs have higher risk of adverse infectious outcomes so as to design interventions to reduce morbidity, mortality, and healthcare expenditures associated with complications of SSIs.

The study of infectious surgical outcomes for children with NMDs has focused on patients undergoing spinal surgery for scoliosis. In these studies, outcomes for children with NMDs with scoliosis are typically compared with other types of scoliosis and not to the general pediatric population, and therefore it remains unclear if NMDs are an independent risk factor for infectious surgical outcomes [4 –6]. The American College of Surgeons National Surgical Quality Improvement Program Pediatrics (NSQIP-P) database allows for large scale evaluation of peri-operative infection risks in select cohorts of children, including children with NMDs. To understand the impact of SSIs on children with NMDs, we used NSQIP-P to determine the rates of SSI and potential morbidity after laparoscopic gastrostomy tube placement, a common surgical procedure in children with NMDs.

The purpose of the study was to determine whether children with NMDs have higher rates of superficial SSI or increased length of stay (LOS) after laparoscopic gastrostomy tube (G-tube) placement. We hypothesized that patients with NMD would have higher rates of SSIs relative to patients without NMD.

Patients and Methods

National Surgical Quality Improvement Program Pediatrics Database

We performed a secondary analysis of data abstracted from NSQIP-P for the years 2018 and 2019. The NSQIP-P is a collaboration administered by the American College of Surgeons (ACS) to collect outcome data systematically from children younger than 18 years of age undergoing surgical procedures from hospitals across the United States [7]. The NSQIP-P contains more than 150 variables such as pre-operative risk factors, intra-operative variables, and 30-day post-operative mortality and morbidity outcomes. The NSQIP-P 2018 contains 119,486 cases from 127 sites and NSQIP-P 2019 contains 132,881 cases from 141 sites.

Patient selection and stratification

Patients were included for analysis if their principal operative procedure was laparoscopic G-tube placement as identified by the Current Procedural Terminology code 43653. Patients were excluded if they had a history of malignancy, presence of do-not-resuscitate order, or other existing wound infections. These exclusion criteria were selected to homogenize our cohort and to reduce the risk of confounding factors. Because details of surgical technique are not included in NSQIP-P, we did not stratify by different types of laparoscopic gastrostomy tube placement.

We stratified patients based on whether they had NMDs utilizing an existing NSQIP-P variable. The ACS labels a patient as having an NMD in NSQIP-P if they have a congenital or acquired degenerative neuromuscular disorder that results in a slow, progressive deterioration in motor function [8]. Examples of disorders that are designated as NMDs in NSQIP-P are neuromuscular scoliosis, degenerative disorders of gray and white matter (dystrophies), demyelinating disorders, and peripheral neuromuscular disorders [8].

Primary outcomes

The primary outcomes were the development of superficial SSI within 30 days of surgery and increased hospital LOS. We selected superficial SSI as a primary outcome because local G-tube site infection has been reported to be the most common adverse infectious outcome of G-tube placement [9,10]. The NSQIP-P does not include data about the location of the SSI, so it is not possible to determine whether the SSI occurred at the site where the laparoscope was inserted or at the gastrostomy site. All superficial SSI definitions and data are from NSQIP-P using routine data collection strategies. NSQIP-P defines a superficial SSI as an infection occurring within 30 days of the operation that involves only skin or subcutaneous tissue of the surgical incision [8]. Additionally, these infections must meet one of the following criteria: purulent drainage from the superficial incision; organisms isolated from an aseptically obtained culture of fluid or tissue from the superficial incision; incision deliberately opened by the surgeon because of pain, localized swelling, or redness; or diagnosis of superficial SSI by the physician or advanced practitioner [8]. Of note, NSQIP-P data collection methods do not stratify which clinician (i.e., surgeon, pediatrician, etc.) made the diagnosis of SSI.

Data analysis

Descriptive statistics were calculated for the NMD and non-NMD groups, with cohorts compared using standard differences. Propensity score-matching was used to control for confounding biases between the NMD and non-NMD groups. Comorbidity variables which may have affected the risk of SSI were selected a priori and included as covariates in the propensity score model, including age, asthma, American Society of Anesthesiologists (ASA) class, cardiac risk factors, nutritional support, ventilator dependance, steroid use, sepsis prior to surgery, inotrope usage, cardiopulmonary resuscitation (CPR) the week prior, and prior cardiac surgery [11]. The NSQIP-P defines the “sepsis use prior to surgery” variable as patients who meet criteria for systemic inflammatory response syndrome, sepsis, or septic shock within 48 hours prior to the primary surgery and “inotrope usage” variable as patients receiving intravenous agents used to increase myocardial contractility to aid in the correction of hemodynamic stability at the time of the operation [8]. Greedy nearest neighbor matching was performed with a caliper size of 0.01 and a ratio of 1:1 with the goal of bringing the standard difference of each variable of importance among the exposed and unexposed group below the threshold of 0.10 to ensure successful matching [12].

Both the unmatched and propensity score-matched cohorts were evaluated for an association between NMD and superficial SSI with the χ² test and for an association between NMD and hospital LOS with Wilcoxon rank sum. The odds of superficial SSI were estimated for both the unmatched and propensity score-matched cohorts by performing both univariable and multivariable logistic regression.

We also performed univariable and multivariable ordered logistic regression to determine the association between NMDs and stepwise increases in LOS. Variables included in the multivariable models were also selected a priori and included age at operation, asthma, ASA class, cardiac risk factors, history of lung malformations, nutritional support, ventilator dependance, steroids, sepsis prior to surgery, number of days inpatient before the operation, and inotrope usage.

Secondary outcomes of interest included unplanned re-admission and death within 30 days of surgery. The association between these outcomes and NMDs were evaluated as described for the primary outcomes above. All data were analyzed using SAS 9.4 (SAS Institute, Cary, NC) and an alpha of 0.05 was selected a priori as the threshold for statistical significance. This study was determined exempt by the Duke Institutional Review Board (Pro00051486). We followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines (Supplementary eTable 1) for reporting observational studies [13].

Results

There were 252,367 patients in the NSQIP-P 2018–2019 dataset. Of these, 8,935 (3.5%) children underwent laparoscopic G-tube placement, including 1,567 (17.5%) with NMDs and 7,368 (82.5%) without NMDs. After applying inclusion and exclusion criteria as well as propensity score-matching, 1,982 patients remained (991 with NMDs and 991 without NMDs). The characteristics of the patients in the final matched dataset are similar (Table 1). All standard differences in both cohorts were less than 0.10 which demonstrates that propensity score-matching was performed successfully [12].

Table 1.

Characteristics of the Cohort Stratified by Neuromuscular Disorder Status before and after Propensity Score-Matching

	Before propensity score-matching, n (%)			After propensity score-matching, n (%)
Variables	NMD	No NMD	Standardized difference	NMD	No NMD	Standardized difference
Patients	1,038 (16.9%)	5,121 (83.1%)	—	991 (50%)	991 (50%)	—
Age, y^a	3.18	1.57	0.39	2.86	2.77	0.02
Gender
Female	503 (48.23%)	2,479 (48.22%)	0.00	478 (48.23%)	461 (46.52%)	0.03
Male	540 (51.77%)	2,662 (51.78%)	0.00	513 (51.77%)	530 (53.48%)	0.03
Sepsis
Sepsis	1 (0.10%)	4 (0.08%)	0.01	1 (0.10%)	0 (0%)	0.03
SIRS criteria	12 (1.15%)	56 (1.09%)	0.01	11 (1.11%)	12 (1.21%)	0.01
None	1030 (98.75%)	5,081 (98.83%)	0.01	979 (98.79%)	979 (98.79%)	0.00
Wound class
Clean	74 (7.09%)	407 (7.92%)	0.03	72 (7.27%)	82 (8.27%)	0.04
Clean-contaminated	963 (92.33%)	4,704 (91.50%)	0.03	913 (92.13%)	899 (90.72%)	0.05
Contaminated	6 (0.58%)	26 (0.51%)	0.01	6 (0.61%)	8 (0.81%)	0.03
Dirty	0 (0.00%)	4 (0.08%)		0 (0%)	2 (0.20%)
Cardiac risk factors
None	677 (64.91%)	2,460 (47.85%)	−0.35	633 (63.87%)	642 (64.78%)	0.02
Minor	154 (14.77%)	1,039 (20.21%)	0.14	152 (15.34%)	155 (15.64%)	0.01
Major	197 (18.89%)	1,344 (26.14%)	0.18	191 (19.27%)	182 (18.37%)	−0.02
Severe	15 (1.44%)	298 (5.80%)	0.24	15 (1.51%)	12 (1.21%)	−0.02
CPR prior to surgery	6 (0.58%)	15 (0.29%)	−0.04	4 (0.40%)	3 (0.30%)	−0.02
Inotrope support	2 (0.19%)	40 (0.78%)	0.08	2 (0.20%)	1 (0.10%)	−0.01
Previous cardiac surgery	77 (7.38%)	928 (18.05%)	0.33	75 (7.57%)	79 (7.97%)	0.01
Steroid use	57 (5.47%)	342 (6.65%)	0.05	56 (5.65%)	55 (5.55%)	0.00
Ventilator dependence	86 (8.25%)	257 (5.00%)	−0.13	69 (6.96%)	64 (6.46%)	0.02
Structural pulmonary abnormality	190 (18.22%)	962 (18.71%)	0.01	173 (17.46%)	177 (17.86%)	0.01
Nutritional support	612 (58.68%)	3,215 (62.54%)	0.08	579 (58.43%)	585 (59.03%)	0.01
Ostomy	25 (2.40%)	128 (2.49%)	0.01	23 (2.32%)	24 (2.42%)	0.01
History of chronic lung disease	151 (14.48%)	1,157 (22.51%)	0.21	142 (14.33%)	140 (14.13%)	−0.01
Hemo disorder	121 (11.60%)	903 (17.56%)	0.17	117 (11.81%)	149 (15.04%)	0.09
Esophageal/gastric/intestinal disease	424 (40.65%)	2,139 (41.61%)	0.02	414 (41.78%)	381 (38.45%)	−0.07
ASA
1–2	159 (15.32%)	1,012 (19.76%)	0.12	159 (16.04%)	165 (16.65%)	0.02
3	763 (73.51%)	3,473 (67.82%)	−0.13	732 (73.86%)	722 (72.86%)	−0.02
4–5	116 (11.18%)	636 (12.42%)	0.04	100 (10.09%)	104 (10.49%)	0.01
Asthma	69 (6.62%)	227 (4.42%)	−0.10	56 (5.65%)	58 (5.85%)	0.01

NMD = neuromuscular disorders; SIRS = systemic inflammatory response syndrome; CPR = cardiopulmonary resuscitation; ASA = American Society of Anesthesiologists.

Values presented are medians.

Primary outcomes

In the unmatched cohort, the prevalence of superficial SSI 30 days after surgery was not different between the NMD and non-NMD groups: 37 (3.6%) and 171 (3.6%), respectively; p = 0.718 (Table 2). However, after propensity score-matching, the prevalence of superficial SSI within 30 days of surgery was higher for the NMD group than for the non-NMD group: 36 (3.6%) and 18 (1.8%), respectively; p = 0.013 (Table 2).

Table 2.

Association between Neuromuscular Disorder Status and Development of Superficial Surgical Site Infection, Death, or Unplanned Re-Admission within Thirty Days of Gastrostomy Tube Placement

	Cohort	NMD, n (%)	No NMD, n (%)	p
Superficial SSI	Unmatched	37 (3.55%)	171 (3.55%)	0.7178
Superficial SSI	Propensity score-matched	36 (3.63%)	18 (1.82%)	0.0130
Death within 30 days	Unmatched	7 (0.67%)	24 (0.47%)	0.3943
Death within 30 days	Propensity score-matched	7 (0.71%)	5 (0.50%)	0.5625
Unplanned re-admission	Unmatched	99 (9.49%)	488 (9.49%)	0.9996
Unplanned re-admission	Propensity score-matched	95 (9.59%)	81 (8.17%)	0.2689

p Values generated using χ² test.

NMD = neuromuscular disorders; SSI = surgical site infection.

Before propensity score-matching, the average post-operative LOS for patients with NMDs was 5.30 days (95% confidence interval [CI], 4.91–5.70). The average post-operative LOS for patients without NMDs was 6.44 days (95% CI, 6.26–6.62), which was longer than for patient without NMDs (p < 0.0001). However, after propensity score-matching, the post-operative LOS was not different between the NMD and non-NMD groups: 5.33 (95% CI, 4.92–5.73) and 5.85 (95% CI, 5.43–6.28) respectively; p = 0.5110 (Table 3).

Table 3.

Mean Days from Operation to Discharge Stratified by Neuromuscular Disorder Status before and after Propensity Score-Matching

	NMD status	Mean	Lower 95% CI	Upper 95% CI	p
Unmatched	NMD	5.30	4.91	5.70	< 0.0001
Unmatched	No NMD	6.44	6.26	6.62	< 0.0001
Propensity score-matched	NMD	5.33	4.92	5.73	0.5110
Propensity score-matched	No NMD	5.85	5.43	6.28	0.5110

p Value generated using Wilcoxon rank sum test.

CI = confidence interval; NMD = neuromuscular disorder.

A multivariable logistic regression was performed to estimate the odds ratio (OR) of superficial SSI for patients with NMDs compared with patients without NMDs (Table 4). After propensity score-matching, the adjusted odds of superficial SSI within 30 days of surgery were two-fold higher for patients with NMDs (OR, 2.05; 95% CI, 1.14–3.66; p = 0.0161). Results of all logistic regressions are presented in Table 4.

Table 4.

Logistic Regression Models Evaluating Odds Ratio of Superficial Surgical Site Infection, Death, and Unplanned Readmission within Thirty Days of Operation for Patients with Neuromuscular Disorders

Pathogen	Statistical test	OR	Lower 95% CI	Upper 95% CI	p
Superficial SSI	Unmatched univariable	1.08	0.75	1.55	0.6898
	Unmatched multivariable	1.16	0.80	1.68	0.4385
	Propensity score-matched univariable	2.04	1.15	3.61	0.0149
	Propensity score-matched multivariable	2.05	1.14	3.66	0.0161
Death within 30 d	Unmatched univariable	1.44	0.62	3.36	0.3957
	Unmatched multivariable	1.82	0.72	4.63	0.2094
	Propensity score-matched univariable	1.40	0.44	4.44	0.5644
	Propensity score-matched multivariable	1.57	0.48	5.19	0.4820
Unplanned re-admission	Unmatched univariable	0.99	0.79	1.24	0.9299
	Unmatched multivariable	1.02	0.81	1.29	0.8690
	Propensity score-matched univariable	1.19	0.87	1.63	0.2690
	Propensity score-matched multivariable	1.19	0.87	1.63	0.2834

OR = odds ratio; CI = confidence interval; SSI = surgical site infection.

A multivariable ordered logistic regression was performed to evaluate the adjusted effect of NMDs on post-operative LOS. The odds of extending post-operative length of stay by one week were not significantly different based on NMD status (OR, 0.924; 95% CI, 0.743–1.150; p = 0.4806).

Secondary outcomes

Neither death within 30 days of surgery nor unplanned re-admission were different between children with or without NMDs before or after propensity score-matching (Table 2). Additionally, neither the adjusted and unadjusted odds of death within 30 days of surgery nor the odds of unplanned re-admission were different between cohorts (Table 4).

Discussion

Although SSI is less common in children than adults after most surgical procedures, certain groups of children may be at increased risk for SSIs. Prior studies have demonstrated that children with scoliosis associated with a neuromuscular etiology have a higher incidence of infection after spine surgery [5,6,14 –16]. Given the high case frequency and relative lack of prior evaluation of SSI after G-tube placement in children with NMDs, there exists an opportunity for study. We found that there is a higher rate of SSI for children with NMDs after G-tube placement, suggesting that these children may be at higher risks for other types of SSIs.

Our finding that children with NMDs have two-fold higher odds of superficial SSI after laparoscopic G-tube placement suggests that NMDs are an important independent risk factor for adverse infectious outcomes after surgery. Although the reasons for this increased risk of SSIs are not addressed by our study, it may be possible that as children with NMDs often develop soft-tissue infections associated with pressure ulcers, the use of antimicrobial therapy to treat prior surgical infections may have provided selection pressure for multi-drug–resistant organisms (MDROs) [17,18]. Given that this population has increased odds of SSI, interventions should be designed that can prevent SSI and reduce the probability of selection for future MDROs.

Children with NMDs may be especially vulnerable to SSIs for a variety of other reasons. Their medical complexity and frequent interactions with health care providers may lead to increased exposure to pathogens and increased probability of colonization with pathogens such as MRSA, a known cause of superficial SSI [19]. Pediatric patients with prior MRSA colonization have been shown to have higher risk of developing superficial postoperative MRSA infection at G-tube sites [20]. Additionally, it would be useful to evaluate whether there were differences among children with NMDs and those without in other factors that could contribute to SSI incidence such as prior antibiotic usage or prior healthcare exposures. Understanding exposures such as these would help to adjust future studies to evaluate whether it is the NMD in and of itself that confers increased odds of superficial SSI or if it is the exposures common to children with NMDs that confer increased odds. These factors have not been well-studied and further studies should be conducted to evaluate the etiology of SSIs and possible associations with MDROs to support targeted quality improvement initiatives.

The organisms causing SSIs after G-tube placement in children with NMD are assumed to be the same as their peers, however, these pathogens are unidentified in the NSQIP-P dataset. Of note, it has been shown that polymicrobial or extended spectrum β-lactamase gram-negative organisms are more likely to cause SSI in patients with neuromuscular scoliosis undergoing spinal surgery [16]. Future modifications of NSQIP-P should consider including culture data to aid in understanding whether certain groups of children are at risk of developing infections caused by specific bacteria or MDROs in general given their importance to the Global Health Security Agenda [21].

Although our study found no difference in LOS, unplanned re-admission, or 30-day mortality, there likely exists an impact that was not captured by the variables provided by NSQIP-P. For example, superficial SSIs were most likely treated with antibiotic prescriptions, but this was not captured in the dataset. This would be important to know because increased use of antibiotics could provide selection pressure for MDROs in the future. Also, the effect of increased odds of superficial SSI could have an impact on hospitalization cost. However, NSQIP-P does not include data about cost so we could not evaluate this. Finally, there is likely an increased toll on the patients' caregivers from discovering that the child has been diagnosed with an infection after surgery or by having to administer antibiotic agents after discharge. The NSQIP-P does not capture all adverse clinical outcomes though they likely exist.

Our study suggests that targeted infection reduction programs improve the outcomes of children with NMDs undergoing G-tube placement, similarly to programs to reduce SSI in children with neuromuscular scoliosis undergoing spine surgery [16,22]. These programs focused on tailoring antimicrobial prophylaxis and implementing intra-operative interventions such as betadine wash or vancomycin powder application. Similar tailored programs may be valuable for children with NMDs undergoing common general surgery operations such as G-tube placement. At our hospital, we have implemented a program that standardized operating room skin preparation and pre-operative prophylactic antibiotic selection among hospitalized children undergoing surgery that is different from the methods we utilize with outpatients. We have seen a reduction in SSI incidence with this strategy and will likely be publishing the results of this quality improvement initiative at a later date. Given increased SSI incidence among children with NMDs, we will consider expanding this program to this vulnerable population. Prospective studies are needed to confirm our findings and further investigate the morbidity of SSIs in this vulnerable population.

Limitations

Our findings are generated from two years of a surgical database created by one surveillance program. Moving forward, our findings should be validated through queries of other large databases and through prospective studies. Additionally, there may be heterogeneity in the determination of superficial SSI diagnosis between hospitals that we can neither evaluate nor address given the retrospective nature of NSQIP-P data. There could also be differences in laparoscopic G-tube placement techniques, but these cannot be determined from NSQIP-P in its present form. This study is meant to be hypothesis-generating and represents the first step to understanding whether children with NMDs have increased likelihood of adverse infectious outcomes in surgery and beyond. Reliance on a large retrospective database includes inherent bias, which we acknowledge in this analysis, but hope to address in subsequent prospective work on this topic.

Conclusions

We found that children with NMDs have two-fold higher odds of developing superficial SSI after laparoscopic G-tube placement compared with children without NMDs. In conjunction with prior studies of increased risks of SSIs following spine surgery in children with NMDs, our data suggest that children with NMDs may be at higher risk for adverse peri-operative infectious outcomes compared with the general pediatric population. Our study suggests that children with NMDs are especially vulnerable to SSI and that further study of this group of patients is warranted to develop effective prevention strategies.

Funding Information

The authors have no funding to report.

Footnotes

Author Disclosure Statement

The authors have no conflicts of interest to report.

Supplementary Material

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Supplementary Material

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