High IL-6/IL-10 ratios indicate sepsis in children with infectious diseases: A retrospective observational study

doi:10.21203/rs.3.rs-4997373/v1

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High IL-6/IL-10 ratios indicate sepsis in children with infectious diseases: A retrospective observational study

https://doi.org/10.21203/rs.3.rs-4997373/v1

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Background

The present study aims to investigate the levels of IL-6 and IL-10, and the ratio of IL-6 to IL-10 in children with or without sepsis, in order to explore the roles of these cytokines in pediatric sepsis.

Methods

A retrospective observational study was performed between January 1, 2018, and December 31, 2022. Children with infectious diseases were reviewed and assigned to the sepsis and non-sepsis groups, respectively. Information on the demographics, clinical characteristics, laboratory results on IL-6 and IL-10, and treatments were retrieved from the medical records, and compared between the two groups.

Results

A total of 122 children were analyzed, with 57 and 65 children in the sepsis and non-sepsis groups, respectively. Compared to children in the non-sepsis group, children in the sepsis group had higher IL-6 and IL-10 levels, and IL-6/IL-10 ratios on the first day of hospital admission (p < 0.05). The further multivariate logistic regression analysis confirmed the statistically significant association between the IL-6/IL-10 ratio, and the presence of sepsis.

Conclusions

Sepsis children present with higher IL-6 and IL-10 levels, and IL-6/IL-10 ratios, when compared to non-sepsis children. This can be used to evaluate the disease severity in this children population.

sepsis

interleukin-6

interleukin-10

pediatrics

Sepsis, particularly severe sepsis, is a significant contributor to mortality in the pediatric population. In infected children, the early identification of high-risk factors for sepsis and prompt treatment are essential to save their lives, and decrease morbidity.

Sepsis is multi-organ dysfunction caused by infection [1]. During the pathogenesis of sepsis, immune dysregulation contributes to the deterioration and unfavorable prognosis of sepsis [2]. Inflammatory mediators are involved in modulating the immune reaction. Both anti-inflammatory and pro-inflammatory cytokines are released to collectively contribute in maintaining the immune homeostasis, and facilitating infection control. However, the excessive release of these inflammatory cytokines can trigger a cytokine storm, and lead to multi-organ dysfunction. Therefore, conducting studies on these cytokine releases can help to better understand the pathogenesis of sepsis, and recognize patients with a high risk to develop severe illnesses [3, 4].

The cytokine interleukin-6 (IL-6) has pro-inflammatory activities [3, 4]. Elevated levels of IL-6 are associated to high risk of unfavorable prognosis in sepsis patients [3]. Although interleukin-10 (IL-10) serves as a crucial anti-inflammatory mediator, high IL-10 level is a risk factor for poor outcomes in sepsis patients [3, 5]. Several studies have reported the correlation between IL-6/IL-10, and suggested that the IL-6/IL-10 ratio can be used to predict the severity and prognosis of septic patients [6, 7]. A recent publication revealed that the IL-6/IL-10 ratio can indicate the disease severity in pediatric sepsis patients with gram-negative infection in the intensive care unit (ICU)[8]. However, it remains unknown whether IL-6 and IL-10 can be applied to differentiate sepsis children from non-sepsis children in clinic.

Therefore, the present retrospective study was conducted to investigate the significance of IL-6 and IL-10, and the IL-6/IL-10 ratio in pediatric patients with infections, in order to provide a useful clinical tool to facilitate the early identification and management of pediatric sepsis.

Study design and participant selection

The present retrospective observational study was conducted for children with infectious diseases, who were admitted in Xinhua Hospital Affiliated to Shanghai Jiaotong University School of Medicine, China, between January 1, 2018 and December 31, 2022. The study protocol was approved by the hospital ethics committee (Ethics approval number: XHEC-D-2024-136).

The inclusion criteria were, as follows: (1) children ≤ 18 years old, and (2) children with an infectious disease, as detailed in the following paragraph. The exclusion criteria were, as follows: (1) children with a history of immunodeficiency; (2) children with malignancy; (3) children with autoimmune diseases; (4) children undergoing long-term glucocorticoid or immunosuppressant therapy; (5) children who received immunotherapy in the past three months; (6) children who have incomplete medical records. If the same child was admitted more than once, all admissions were included in the analysis.

Definition of infection

Sepsis was defined with reference to the Sepsis-III criteria [1]. The Sequential Organ Failure Assessment (SOFA) score of children was based on the standard proposed by Matics et al [9]. The diagnostic criteria for pneumonia, bacterial enteritis, appendiceal abscess, upper urinary tract infection, and cellulitis were established based on the 2005 publication of the ICU infection diagnostic criteria [10].

The diagnosis of bacterial meningitis required the fulfillment of all the following criteria: (1) fever with rectal temperature of > 38.5°C or axillary temperature of > 38.0°C; (2) meningeal irritation, headache, or altered mental status; (3) severe leukocytosis of > 100×10⁶ cells/L or moderate leukocytosis of 10–100×10⁶ cells/L, but with a decreased glucose level or an elevated protein of > 100 mg/dL in the cerebrospinal fluid (CSF) examination [11]. Viral encephalitis was diagnosed according to the clinical presentation of persistent altered mental status for > 24 hours, excluding encephalopathy due to other etiology. The diagnosis required meeting at least three of the following six criteria: (1) fever > 38°C within 72 hours before or after hospital admission; (2) seizures not fully explained by pre-existing epilepsy; (3) CSF white blood cell count of ≥ 5× 10^6/L; (4) new focal neurological signs; (5) new abnormalities in the neurological imaging examination; (6) electroencephalogram suggesting encephalitis [12].

Cryptococcal meningitis was diagnosed based on the guidelines provided by the Chinese Society of Infection, affiliated with the Chinese Medical Association, with the main criterion being the identification of cryptococcus in the CSF [13].

Data collection

The hospital medical records were reviewed to retrieve the following necessary information: demographics, pediatric risk mortality (PRISM) score, SOFA score, etiology, and treatments.

The IL-6 and IL-10 levels were measured on the first day of admission to the pediatric ICU. Then, the serum concentrations of IL-6 and IL-10 were determined using the MesoScale Discovery method (Meso QuickPlex SQ 120, USA) and human cytokines kit (BD, USA), respectively, according to manufacturer’s instructions in the hospital laboratory.

Statistical analysis

Eligible children were categorized into two groups: sepsis and non-sepsis groups. Continuous data were presented in mean ± standard deviation or median with interquartile range (IQR), and compared by Student t-test or Mann-Whitney test, depending on the normality test results. Categorical data were presented in numbers with percentages, and compared by Chi-square test. Then, multivariate logistic regression analysis was performed to identify the risk factors for sepsis. All statistical analyses were performed using SPSS version 22.0 (SPSS, IBM, NY, USA). A p-value of < 0.05 was considered statistically significant.

Characteristics of the study participants

A total of 412 pediatric patients were admitted during the study period. Among these patients, 185 patients had infections. After excluding 63 pediatric patients, 122 patients were included for the final analysis. These patients had a median age of 32.4 months old (IQR: 16.9 months old, 63.2 months old), and 54.9% (67/122) of these pediatric patients were boys. The participant selection flowchart is presented in Fig. 1. Among these pediatric patients, 18 patients had the following underlying diseases (8 patients from the non-sepsis group and 10 patients from the sepsis group): epilepsy (two cases), congenital esophageal atresia (IIIa) (two cases), cerebral hypoplasia (six cases), methylmalonic acidemia (three cases), asthma (one case), Gaucher disease (one case), bronchopulmonary dysplasia (one case), congenital megacolon (one case), and Reye’s syndrome (one case).

There were no statistically significant differences in gender, age, number of underlying diseases, and length of hospital and ICU stays between the two groups. Sepsis children had higher disease severity (higher SOFA and PRISM scores), when compared to non-sepsis children. Furthermore, compared to non-sepsis children, sepsis children received more frequent mechanical ventilation, hemodialysis/hemofiltration, glucocorticoids, and vasopressors (p < 0.001, Table 1).

Table 1

Comparison of baseline characteristics and treatments between the two groups.
Characteristics		Non-sepsis group (n = 65)	Sepsis group (n = 57)	p
Gender, n (%)	Male	36.00 (55.40%)	31.00 (54.40%)	0.912
Age, months		36.30 (17.60, 60.60)	27.00 (15.50, 80.20)	0.851
Underlying diseases, n (%)	Yes	8 (12.30%)	10 (17.50%)	0.452
Infectious diseases, n				0.767
	Pneumonia	39	31
	Viral encephalitis	15	16
	Bacterial meningitis	4	2
	Cryptococcal encephalitis	1	1
	Bacterial enteritis	3	6
	Appendiceal abscess	1	0
	Upper urinary tract infection	1	0
	Cellulitis	1	1
Disease severity
SOFA		1 (0, 1)	6 (2, 10)	< 0.001
PRISM		0 (0, 2)	9 (1, 16)	< 0.001
Medical treatments, n (%)
Invasive mechanical ventilation	Yes	4 (6.20%)	31 (54.40%)	< 0.001
Hemodialysis/hemofiltration	Yes	14 (21.50%)	31 (54.40%)	< 0.001
Glucocorticoids	Yes	24 (36.90%)	41 (71.90%)	< 0.001
Vasopressors	Yes	0 (0.00%)	41 (71.90%)	< 0.001
Survival, n (%)	Yes	65 (100.00%)	40 (17.20%)	< 0.001
Length of hospital stay, days		17 (11.00, 25.00)	19 (8.50, 30.00)	0.882
Length of intensive care unit stay, days		7 (5.00, 12.00)	9 (5.50, 19.50)	0.112

Pneumonia was the most common infection in both groups of children, followed by viral encephalitis and bacterial meningitis (Table 1). Furthermore, pathogenic microorganisms were isolated from 58 of 122 children, which included viruses in 15 cases, bacteria in 33 cases, Mycoplasma pneumoniae in seven cases, and fungi in three cases (Table 2).

Table 2

Distribution of pathogenic microorganisms in the two groups of children.
Pathogen identified, n		Non-sepsis group	Sepsis group
Virus
	Cytomegalovirus	1	3
	Epstein-Barr virus	1	3
	Adenovirus	2	1
	Enterovirus	1	1
	Parainfluenza virus	0	1
	SARS-CoV-2 virus	0	1
Bacteria
	Escherichia coli	1	2
	Klebsiella pneumoniae	1	3
	Haemophilus influenzae	3	5
	Pseudomonas aeruginosa	1	1
	Streptococcus pneumoniae	1	6
	Staphylococcus aureus	2	6
	Salmonella .	0	1
Others
	Mycoplasma pneumoniae	4	3
	Cryptococcus	1	1
	Candida albicans	0	1
Pathogen not detected		46	18

Differences in inflammatory cytokine levels between groups

The concentrations of IL-6 and IL-10 in both groups of children are presented in Table 3. The median levels of IL-6 and IL-10 were significantly higher in the sepsis group, when compared to the non-sepsis group. Similarly, the median IL-6/IL-10 ratio was significantly higher in the sepsis group, when compared to the non-sepsis group. Next, a multivariate logistic regression analysis was further performed, with sepsis as the dependent variable, and demographics, underlying diseases, disease severity, IL-6, IL-10, and the IL-6/IL-10 ratio as independent variables. The association among IL-6, IL-10, and the occurrence of sepsis had no statistical significance in the multiple regression analysis (Tables S1 and S2), while the high IL-6/IL-10 ratio was associated to sepsis occurrence in children with infectious diseases (Table 4).

Table 3

Comparison of cytokine levels between the two groups.
Cytokines	Non-sepsis group (n = 65)		Sepsis group (n = 57)		p
Cytokines	IQR	P₅₀	IQR	P₅₀	p
IL-6 (pg/ml)	12.00, 116.00	44.60	13.00, 66.03	89.90	0.020
IL-10 (pg/ml)	6.80, 39.90	20.10	10.80, 227.50	58.90	< 0.001
IL-6/IL-10	0.70, 5.20	1.40	0.90, 8.20	2.40	0.020

Table 4

Results for the multivariate logistic regression analysis.
Variables	β	S.E.	Wald	df	p	Exp(β)	95% EXP(β)
Variables	β	S.E.	Wald	df	p	Exp(β)	Lower	Upper
Gender (male)	1.888	1.580	1.427	1	0.232	6.604	0.298	146.248
Have underlying diseases	6.428	3.014	4.549	1	0.033	619.013	1.683	227,614.702
Age (months)	-0.007	0.020	0.137	1	0.711	0.993	0.954	1.032
SOFA	1.822	0.642	8.062	1	0.005	6.182	1.758	21.736
IL-6/IL-10	0.441	0.232	3.605	1	0.040	1.147	1.214	2.450
Constant	-11.361	4.312	6.941	1	0.008	0.000
Notes: Dependent variable: sepsis occurrence or no sepsis occurrence. Exp(β) = 1.147, 95% confidence interval = 1.214–2.450. SOFA, Sequential Organ Failure Assessment.

Children with sepsis carry a high mortality rate. In the present study, it was found that children with sepsis had higher levels of IL-6 and IL-10, when compared to children without sepsis. In addition, the ratio of IL-6 to IL-10 was notably higher in sepsis children, when compared to non-sepsis children. These results show that the increase in IL-6/IL-10 ratio can indicate the presence of sepsis in children with infectious diseases.

In the present study participants, the most common infection sites included pneumonia, and the central nervous system, which is consistent with the findings of a previous study [14].

The present study revealed that in children with infectious diseases, both IL-6 and IL-10 were associated to sepsis, which is consistent to the reports of previous studies [3–5]. As an important proinflammatory factor, the high level of IL-6 was found to be a risk factor for poor outcomes in sepsis patients. Thus, IL-6 can be used as a valuable biomarker for sepsis diagnosis [15]. Compared to non-sepsis patients, the level of IL-6 can be significantly higher in sepsis patients at disease onset [16, 17]. In addition, it was reported that IL-6 can be applied to indicate the severity of sepsis, and predict the sepsis prognosis. Among sepsis patients, patients with septic shock presented with significantly higher IL-6 levels, when compared to patients without septic shock[16]. Furthermore, among sepsis patients, patients with elevated levels of IL-6 presented with a significant increase in mortality within 28 days [17]. The presence of a ≥ 86% reduction in IL-6 levels within the initial 24 hours of ICU admission would indicate a favorable prognosis [18]. The level of IL-6 upon discharge can be applied to predicate the all-cause mortality in sepsis patients [19].

As an anti-inflammatory cytokine, IL-10 is a risk factor for severe sepsis and unfavorable prognosis in sepsis patients [5]. It was reported that IL-10 is a valuable biomarker to diagnose neonatal sepsis at its early stage [20]. A higher level of IL-10 can predict the severity of infection in patients with febrile neutropenia [21]. The persistent elevated levels of IL-10 in septic shock patients might inhibit the release of pro-inflammatory factors, and induce immunosuppression [22, 23], finally contributing to the pathogenesis of multiple organ failure (MOF) [24].

The findings of the present study suggest that elevated IL-6/IL-10 ratios might contribute to sepsis development in pediatric patients with infectious diseases, which is consistent with the reports of previous studies [6, 24–26]. Loisa et al. reported that a high IL-6/IL-10 ratio might be involved in MOF development in patients with severe sepsis [24]. In patients with Pneumocystis pneumonia, the severe and non-survival groups presented with high IL-6/IL-10 ratios [25]. In the present study, it was found that the IL-6/IL-10 ratio can indicate the presence of sepsis in children with infectious diseases. The IL-6/IL-10 ratio can be used to assess the relationship between pro-inflammatory and anti-inflammatory states, with alterations in this relationship closely associated to patient outcomes and disease severity. The early mortality of sepsis patients primarily stems from the exaggerated pro-inflammatory response, resulting in organ dysfunction. During this stage, the body exhibits a hyper-inflammatory state [27]. An elevated IL-6/IL-10 ratio suggests that the body is experiencing a strong inflammatory reaction, which might contribute to MOF and death.

The present study investigated the correlation between IL-6/IL-10 and disease severity, primarily during the stages of the disease. The dynamic balance between anti-inflammatory and pro-inflammatory responses may vary over time. Therefore, the clinical implications of IL-6/IL-10 during the course of sepsis might change with its management. Further studies to monitor the dynamic changes of IL-6/IL-10 are required.

For children with infectious diseases, high IL-6 and IL-10 levels, and IL-6/IL-10 ratio can indicate the presence of sepsis, requiring prompt management. These present study findings offer novel insights for assessing the severity of infectious diseases in pediatric patients.

IL-6：interleukin-6；IL-10：interleukin-10；ICU：intensive care unit;

SOFA: Sequential Organ Failure Assessment; CSF: cerebrospinal fluid; PRISM: pediatric risk mortality; IQR：interquartile range; MOF: multiple organ failure

Ethics approval and consent to participate:

Ethical approval was provided by the Xinhua Hospital Affiliate, Shanghai Jiao Tong University School of Medicine (XHEC-D-2024-136)

Consent to participate:

Written informed consent for publication of their clinical details and/or clinical

images were obtained from the guardian of the patient. A copy of the consent form is available for review by the Editor of this journal.

Consent for publication: NOT applicable

Availability of data and materials:

The datasets generated during and analyzed during the current study are not publicly available now because the follow-up observation test is still in progress; but are available from the corresponding author or first author on reasonable request.

Competing interests

The authors declare that they have no competing interests

Funding source: No Funding.

Authors' contributions:

LL C, program design, implementation, data collection and analysis, writing manuscript; YQ R, specimen detection and analysis; L Z, specimen collection, storage and sample preprocessing; PP W, case admission, specimen collection, data collection; XD Z: case admission, data collection; YN Z: quality control, review and editing the manuscript. All authors have read and agreed to the published version of the manuscript.

Acknowledgements: We sincerely thank the children and their parents who participated in this study.

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No competing interests reported.

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You are reading this latest preprint version

High IL-6/IL-10 ratios indicate sepsis in children with infectious diseases: A retrospective observational study

Status:

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Background

Materials and Methods

Study design and participant selection

Definition of infection

Data collection

Statistical analysis

Results

Characteristics of the study participants

Differences in inflammatory cytokine levels between groups

Discussion

Conclusions

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1