Relationship among low baseline muscle mass, skeletal muscle quality and mortality in critically ill children

doi:10.21203/rs.3.rs-2097796/v1

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Relationship among low baseline muscle mass, skeletal muscle quality and mortality in critically ill children

https://doi.org/10.21203/rs.3.rs-2097796/v1

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Background: Adult studies have shown that low baseline muscle mass at ICU admission was associated with poor clinical outcomes. However, no information on the relationship between baseline muscle quality or mass and clinical outcomes in critically ill children was found. In this investigation, the aim was to ascertain the correlation among baseline muscle mass, muscle quality and clinical outcomes in severely ill children.

Methods: This is a retrospective observational study. A total of 3775 children were admitted to the PICU of the First Hospital of Jilin University in China during the research period from January 2019 to July 2021, of which 262 patients were eligible for inclusion. Abdominal computed tomography (CT) was performed before or within 72 hours of admission to the PICU to assess skeletal muscle mass and quality

Results:. BMI was greater in the normal SMI group than in the low SMI group (P=0.004), the length of PICU stay (P=0.02) was longer in the low SMI group than in the normal SMI group, and the in-PICU mortality rate (P=0.025) in the normal SMI group was superior tothat in the low SMI group. Children with low SMD had a higher in-PICU mortality rate, were younger and weighed less. Mortality was substantially greater in patients with lower SMD and prolonged hospital stay (log-rank, P=0.007). SMD was an independent predictor for length of PICU stay and in-PICU mortality.

Conclusions: Low baseline skeletal muscle quality in severely ill children is closely tied with a higher in-PICU mortality rate and longer length of PICU stay, and is an independent risk factor for unfavorable clinical outcomes. However, muscle mass did not show a similar strong association. Therefore, baseline muscle quality in severely ill children need more attention to avoid poor prognosis.

Trial registration: ChiCTR1800020196 (19/12/2018).

Computed tomography

Muscle quality

Muscle quantity

Children

Mortality

ICU-acquired muscle atrophy and weakness are closely related to poor clinical outcomes, such as an increased risk of mortality, high extubation failure rates and longer intensive care unit (ICU) stays, for critically ill adult and pediatric patients(1–3). Recently, several adult studies have shown that critically ill patients with low baseline muscle mass at ICU admission also have poor clinical outcomes. A retrospective study by Ariel(4) found that a large pectoralis muscle area (PMA) at admission was associated with high rates of 6-month survival, low in-PICU mortality, and more ICU-free days. Skylar et al. reported a strong relationship between prolonged mechanical ventilation and low baseline diaphragm muscle mass and mortality(5). In addition to muscle mass, muscle quality also has an essential impact on outcomes in ICU patients. Another retrospective study showed that a lower skeletal muscle quality at ICU admission is independently correlated with a high 6-month mortality rate in mechanically ventilated patients(6). Additionally, early interventions for patients with low baseline muscle mass and quality are also important for improving clinical prognosis. A prospective cohort study showed that (7) timely substantial protein intake is able to reduce mortality in ICU patients with lower skeletal muscle density and low area.

However, in reviewing the papers, no information on the relationship between baseline muscle quality or mass and clinical outcomes in critically ill children was found. Children have different metabolism rates and body compositions, suggesting that there are differences in skeletal muscle turnover compared to adults(8, 9). In addition, the types of critical illnesses that children experience differ from those of adults, especially regarding exposure and prevalence, so children may have better baseline muscle mass and quality. Therefore, it is unclear whether the conclusions of the abovementioned studies with adults are consistent with those of studies with children, so the ability to predict the clinical outcomes of critically ill children is limited and must be confirmed by corresponding studies with children.

In this investigation, the aim was to ascertain the correlation among baseline muscle mass, muscle quality and clinical outcomes in severely ill children. It was hypothesized that lower muscle quality and mass in severely ill children upon pediatric intensive care unit (PICU) admission were associated with poor clinical outcomes and were also independent risk factors for poor outcomes. This study also aimed to explore whether there are specific risk factors that predict and improve clinical outcomes in the pediatric population.

Participants:

This study retrospectively analyzed patients (aged from 1 to 18 years) admitted to the PICU of the First Hospital of Jilin University in China from January 2019 to July 2021. The current research was approved by the hospital’s institutional ethics committee. The parents or guardians of the registered children were aware of the protocols for which they presented a letter of satisfaction and were given an information sheet.

All participants were required to be admitted to the PICU for more than 3 days, and an abdominal computed tomography (CT) scan was used for diagnosis or treatment before or within 72 hours of admission to the PICU.

The exclusion criteria included the following: patients for whom the abdominal CT scan quality was too low for analysis; patients who underwent previous surgical treatment of the lumbar 3-segment plane to remove the muscle; and patients whose guardians or parents refused to participate in the study.

Procedures

All eligible data included sample characteristics (sex, age, height, weight, body mass index (BMI), diagnosis at admission, Pediatric Critical Illness Score (PCIS)), muscle index (muscle quality and mass), and clinical outcomes (length of PICU stay, in-PICU mortality).

Abdominal CT scans were used for diagnosis or treatment before or within 72 hours of admission to the PICU. CT was performed using our HI speed 64-slice spiral CT machine (PHILIPS, Netherlands). All scanned images of the participants were imported into Neusoft Fat analysis image postprocessing software (AVW 2.0.36.1237, China) for analysis by two professionals.

We selected the cross-sections of the muscles at L3 for qualitative and quantitative analysis. The reason for choosing this segment is that the muscle mass at this level has a good correlation with the muscle mass of the whole body, which can determine the muscle condition of the whole body[1–4]. Muscle tissue was identified by using Hounsfield unit dimensions set from − 29 to + 150 and intermuscular adipose tissue (IMAT) dimensions set from − 190 to 150[2]. Muscle mass at the L3 level in cm² was appraised by delineating the muscle boundaries, which have been marked in red, and the IMAT is shown in blue (Fig. 1.1 and 1.2). Due to the characteristics of the children, we corrected the measurement results with the skeletal muscle index (SMI), which was evaluated by normalizing the assessed muscle area to the square height of the patient (cm²/m²)[5]. Muscle quality was evaluated by measuring skeletal muscle density (SMD), which was evaluated through skeletal muscle radiation attenuation (SM-RA) of the muscles visible at the L3 level, assessed in Hounsfield units (HUs)[6].

Statistical Analysis

Assessments were executed by employing IBM SPSS Statistics for Windows, Version 22 (IBM Corp, Armonk, NY). Continuous variables are defined as the median or mean ± SD (interquartile range) based on whether the distribution was nonnormal or normal. Categorical variables are presented as n (%). A thorough comparison was made between continuous variables and the Mann–Whitney U test or Student’s t test was used. Considering the size of the sample, categorical variables were compared with Fisher’s exact test or the chi-squared test. ROC curve assessment was employed to explain the SMI and SMD cutoff values that best fit to estimate hospital mortality separately. All patients were categorized into different groups based on the cutoff values separately. Logistic regression or multivariate linear assessment was performed to evaluate the factors that were considerably correlated with in-PICU mortality or length of PICU stay. Kaplan–Meier curve assessment was conducted to assess the relationship between the different SMI or SMD groups and mortality. A p value ≤ 0.05 was regarded as statistically meaningful.

A total of 3775 children were admitted to the PICU during the research period, of which 654 patients were eligible for inclusion. During the CT image analysis, 301 children were excluded due to poor CT scan image quality, 49 children were excluded because their guardians or parents refused participation, and 42 children were excluded due to missing CT data. Ultimately, 262 children met the criteria and were included in the study, with a mean SMI of 37.75 ± 9.32 cm2/m2. Subgroup analysis was performed for 203 of these children with SMD data, with a mean SMD of 41.71 ± 6.83 HU. Figure 2 shows the flow chart of this study.

The cutoff values that best fit to estimate hospital mortality were 30.96 cm2/m2 for the SMI and 41.21 HUs for SMD. All patients were categorized into a normal SMI group (n = 209) and a low SMI group (n = 53) based on the cutoff value of the SMI. A total of 204 patients were categorized into a low SMD group (n = 86) and a normal SMD group (n = 117) based on the cutoff value of SMD.

Sample characteristics

The characteristics of all children are given in Table 1. Comparing the group characteristics, the following were shown: BMI was superior in the normal SMI group compared to the low SMI group (18.07 ± 4.44 vs. 15.99 ± 4.51, P = 0.004), and length of PICU stay (13.00 [7.50–20.00] vs. 16.00[8.50–32.50], P = 0.02) and in-PICU mortality (10.00% vs. 22.6%, P = 0.025) were greater in the low SMI group.

Table 1

Sample Characteristics comparsion between normal and low SMI group
Characteristics	Normal SMI group (n = 209)	Low SMI group (n = 53)	P
Age, mon, IQR	84(18–156)	76(49–119)	0.694
Height, cm, IQR	120(88.75-159.75)	120(105–143)	0.715
Weight, kg, IQR	26(13.63–51.5)	20(14.5–31)	0.186
Sex, %	68.75%	53.48%	0.195
BMI, kg/m2, (mean ± SD)	18.07 ± 4.44	15.99 ± 4.51	0.004
SMI, cm²/m², (mean ± SD)	40.36 ± 8.55	27.40 ± 2.59	༜0.001
PCIS, (mean ± SD)	86.95 ± 9.74	87.21 ± 6.55	0.821
Length of PICU stay, day, IQR	13.00(7.5–20)	16.00(8.5–32.5)	0.02
Hospital mortality, %	10.0(21/209)	22.6(12/53)	0.025
Admission diagnosis, %
Respiratory	10.0 (21/209)	5.6 (3/53)
Neurologic	23.9 (50/209)	22.6 (12/53)
Post-surgery	2.8 (6/209)	3.7 (2/53)
Hematology	11.5(24/209)	18.9 (10/53)
Sepsis	11.5(24/209)	9.4(5/53)
Cardiovascular	3.8(8/209)	5.6(3/53)
Trauma	18.2(38/209)	7.5(4/53)
Other	18.2(38/209)	26.4(14/53)
BMI = body mass index, SMI = skeletal muscle index, PCIS = pediatric critical illness score

Subgroup analysis showed that children with low SMD had a higher in-PICU mortality rate (25.6% vs. 7.7%, P < 0.001), were younger (36.00[12.00-120.00] vs. 84.00[47.50-147.50], P < 0.001) and had lower weights (16.40[10.93–37.25] vs. 23.00[16.00–45.00], P = 0.006). No discrepancy was detected between the two groups in the length of PICU stay (Table 2).

Table 2

Sample Characteristics comparsion between normal and low SMD group
Characteristics	Normal SMD group (n = 117)	Low SMD group (n = 86)	P
Age, mon, IQR	84 (47.5-147.5)	36(12–120)	< 0.001
Height, cm, IQR	120 (104–157)	104.5 (79.5-139.7)	0.001
Weight, kg, IQR	23 (16–45)	16.4 (10.9–37.2)	0.006
Sex male, %	53.0 (62/117)	55.8 (48/86)	0.776
BMI, kg/m2, (mean ± SD)	17.3 ± 4.1	18.6 ± 5.1	0.053
PCIS, (mean ± SD)	87.3 ± 9.4	85.5 ± 10.2	0.199
Length of PICU stay, day, IQR	16.3 (14.8–18.9)	17.1 (15.2–20.4)	0.065
Hospital mortality, %	7.7(9/117)	25.6(22/86)	༜0.001
BMI = body mass index, PCIS = pediatric critical illness score, SMD = skeletal muscle density

Relationship between muscle condition and clinical outcomes

The Kaplan–Meier curve analysis of the SMI and SMD is shown in Figs. 3 and 4. The analysis results indicated that mortality was considerably greater in patients with a low SMD and prolonged hospital stay (log rank test P = 0.007). However, a trend was not found between the low SMI and normal SMI groups (log rank test P = 0.902).

The comparison of characteristics between survivors (n = 172) and nonsurvivors (n = 31) showed that nonsurvivors had a lower SMD (37.53 ± 8.09 vs. 42.47 ± 6.32, P < 0.001), a longer length of PICU stay (25.00[17.00–41.00] vs. 13.00[8.00-19.75], P < 0.001) and more severe illness (PCIS 78.48 ± 18.9 vs. 88.08 ± 5.96 P < 0.001) (Table 3).

Table 3

The comparsion of characteristics between survivors and non- survivors
Characteristics	survivors (n = 172)	non- survivors (n = 31)	P
Age, mon, IQR	65.5(24.2–132.0)	84.0(24.0-132.0)	0.655
Height, cm, IQR	113 (93.2-152.2)	120 (78–157)	0.79
Weight, kg, IQR	20.5 (13.5-40.75)	21.3 (10.7–47)	0.975
Sex male, %	55.8 (96/172)	45.2 (14/31)	0.329
BMI, kg/m2, (mean ± SD)	17.3 ± 4.1	18.6 ± 5.1	0.053
PCIS, (mean ± SD)	88.1 ± 5.9	78.4 ± 18.9	༜0.001
Length of PICU stay, day, IQR	13.0(8.0-19.7)	25.0(17.0–41.0)	༜0.001
SMD, HU, (mean ± SD)	42.47 ± 6.32	37.53 ± 8.09	༜0.001
SMI, cm²/m², (mean ± SD)	38.29 ± 9.66	34.98 ± 8.75	0.76
BMI = body mass index, SMI = skeletal muscle index, PCIS = pediatric critical illness score, SMD = skeletal muscle density

The factors we included in logistic regression analysis were sex, age, BMI, SMD, the SMI, and the PCIS, and the results showed that SMD (95% CI, 0.79–0.92; OR, 0.85) and the PCIS (95% CI, 0.83–0.94; OR, 0.88) were independent predictors for in-PICU mortality, which indicated that for every 1 HU decrease in SMD, the in-PICU mortality increased by 15% (Fig. 5).

Multivariate linear regression analysis demonstrated that age (β = 0.08, P = 0.002), SMD (β=-0.54, P = 0.005) and BMI (β=-0.73, P = 0.025) were considerably correlated with in-PICU mortality (Table 4).

Table 4

Linear regression analysis of risk factors associated with Length of PICU stay
Factors	Length of PICU stay
Factors	B	95% CI	P
SMD	-0.544	-0.919 to -0.169	0.005
SMI	-0.072	-0.396 to -0.251	0.659
BMI	-0.731	-1.370 to -0.093	0.025
PCIS	-0.108	-0.356 to -0.141	0.395
Age	0.081	0.030 to 0.132	0.002
Sex	-1.02	-6.008 to 3.968	0.687
BMI = body mass index, SMI = skeletal muscle index, PCIS = pediatric critical illness score, SMD = skeletal muscle density

In this retrospective study, we showed that lower skeletal muscle quality at PICU admission is significantly correlated with higher hospital mortality and a longer PICU stay, and is an independent risk factor for length of PICU stay and in-PICU mortality in severely ill children. However, this relationship was not found for muscle mass in our study. In addition, consistent with adult studies[7–10], BMI and illness severity were also associated with hospital mortality in the present research.

This is the first investigation to explore the association between muscle quality and mass at PICU admission and outcomes in critically ill children. It is becoming increasingly difficult to ignore the association between decreased skeletal muscle mass and poor clinical outcomes. Ong et al.[11] found that a decrease in muscle in critically ill children was associated with poor mobility. In addition, recent studies using ultrasound or other methods have found that muscle atrophy progresses rapidly and is common in critically ill children[12–14]. However, a lack of exploration of the relationship between muscle mass and clinical outcomes has existed thus far. A strength of our study is that the CT scan method was used to evaluate the skeletal muscle condition of critically ill children, which is more accurate than other methods and can better reflect the whole-body muscle condition. In addition, the starting time of observation in our study was before or within 72 hours of the children entering the PICU, which may help to identify high-risk children at an earlier stage to carry out rehabilitation and nutritional intervention sooner to reduce the occurrence of adverse outcomes.

Due to differences in study populations, the results of this study are somewhat inconsistent with those of the adult studies. We were in agreement with an investigation by Looijaard et al.[15] investigating the relationship between baseline muscle quality and clinical outcomes, which found that mortality was substantially greater in patients with lower muscle quality and that lower skeletal muscle quality at ICU admission was independently correlated with higher 6-month mortality and a longer PICU stay in critically ill patients. A strong relationship between SMD and poor clinical outcomes has been reported in other recent studies[16, 17]. The biggest difference between our findings and studies with adults is the association of skeletal muscle quantity with clinical outcomes. Previous studies on critically ill patients have found that low baseline skeletal muscle quantity is closely associated with poor clinical outcomes (increased mortality and length of PICU stay) and is an independent risk factor for hospital mortality[18–20], which is not in accordance with our study. The results of this study found no significant association between low muscle quantity and poor clinical outcomes, which was not as good of an association as that with muscle quality. The main reasons for the difference are as follows: First, there are differences in muscle development at the L3 level in children of different ages. Some younger children were included in the study, and they had incomplete abdominal muscle development. Second, there is no uniform method for the correction of muscle area measurement in pediatric patients, which may affect the calculation of muscle area. Third, because the characteristics of children's spine development are different from those of adults, some studies with children have selected other spinal planes or other parts of the spine as landmarks.[21–23], and the selection criteria are not uniform. The relationship between the muscle area of the L3 level and the whole body muscle area in children is not clear. Therefore, it is limiting to predict mortality in critically ill children by calculating the muscle quantity currently assessed by CT.

There were a few limitations to this study. First, children under 12 months of age were not included in the study because of their thin abdominal muscles, resulting in unclear visualization of the abdominal muscle area at the L3 level, so the study results are not representative of the infant population. Second, due to the proportions between the trunk, head, and limbs of developing children vary, the choice of cross-sections for muscle analysis in CT images may also have some impact on the results. There is a need for CT image localization methods that are more applicable to the pediatric population in the future. Third, the clinical outcomes of the study only observed mortality during PICU hospitalization, the follow-up time was short, and the long-term clinical information of severely ill children was not followed up. Finally, although CT scans have good accuracy in assessing the condition of skeletal muscle in children, they are not reproducible and are radioactive, so they are difficult to use as a routine examination in children. Limited studies have performed consistent analyses of CT scans and other methods for assessing muscle[24], and more research may be needed in the future.

This paper has provided an account that low baseline skeletal muscle quality in critically ill children is correlated with greater in-PICU mortality and a longer length of PICU stay, and is an independent risk factor for length of PICU stay and in-PICU mortality in critically ill children. However, muscle quantity did not show a strong association with poor clinical outcomes. Therefore, muscle quality in children may be a better predictor. Further studies need to pay more attention to critically ill children with low muscle quality at PICU admission, and an earlier nutritional and rehabilitation intervention may be needed.

CT: computed tomography; PICU: pediatric intensive care unit; BMI: body mass index; SMI: skeletal muscle index; SMD: skeletal muscle density; PCIS: pediatric critical illness score; PMA: pectoralis muscle area; IMAT: intermuscular adipose tissue; SM-RA: skeletal muscle radiation attenuation; HU: hounsfield units

Ethics approval and consent to participate

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the first hospital of Jilin university’s institutional ethics committee. Written informed consent was obtained from the parents.

Consent for publication

Not applicable.

Availability of data and materials:

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding：This study was supported by the National Nature Science Foundation of China(81973054), Science and Technology Planning Project of Guangdong Province(2018B030335001), Jilin Provincial Key Laboratory of Medical imaging & big data(20200601003JC), Radiology and Technology Innovation Center of Jilin Province(20190902016TC), Jilin Provincial International Joint Research Center for Medical Artificial Intelligence Precision Diagnosis and Treatment(20210504008GH)

Authors' contributions: YX: analysis and interpretation of data, drafting the article, and investigation. TT, YM: analysis data and drafting the article (tables).JF: supervising, editing, and clinical trial registration. LZ, SZ: acquisition of data. LD: concept and design, revising the article critically for important intellectual content, final approval of the version to be published, and funding acquisition. All authors contributed to the article and approved the submitted version.

Acknowledgements

We thank all pediatric critical care fellows and nurses for their clinical assistance. We also thank Professor Du for reviewing our manuscript.

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No competing interests reported.

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Relationship among low baseline muscle mass, skeletal muscle quality and mortality in critically ill children

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