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Malnutrition on admission to the paediatric cardiac intensive care unit increases the risk of mortality and adverse outcomes following paediatric congenital heart surgery: A prospective cohort study

  • Sibel Yilmaz Ferhatoglu
    Correspondence
    Corresponding author at: Department of Anesthesiology and Reanimation, stanbul Siyami Ersek Cardiothoracic Surgery Training and Research Hospital, Sahrayi Cedid Mh., Ataturk Cd., No: 36/11 Kadikoy, Istanbul, Turkey. Tel.: +905052600701.
    Affiliations
    University of Health Sciences, Istanbul Siyami Ersek Cardiothoracic Surgery Training and Research Hospital, Department of Anesthesiology and Reanimation, Istanbul, Turkey
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  • Okan Yurdakok
    Affiliations
    University of Health Sciences, Istanbul Siyami Ersek Cardiothoracic Surgery Training and Research Hospital, Department of Pediatric Cardiovascular Surgery, Istanbul, Turkey
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  • Nurgul Yurtseven
    Affiliations
    University of Health Sciences, Istanbul Siyami Ersek Cardiothoracic Surgery Training and Research Hospital, Department of Anesthesiology and Reanimation, Istanbul, Turkey
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Published:August 27, 2021DOI:https://doi.org/10.1016/j.aucc.2021.07.004

      Abstract

      Background

      Malnutrition is a common problem in children with congenital heart disease, and it increases the risk of adverse outcomes in the postoperative period.

      Objectives

      We aimed to assess the association between malnutrition and cardiac surgery outcomes in paediatric patients aged 0–36 months.

      Methods

      This prospective cohort study was performed in a hospital specialising in paediatric cardiothoracic surgery. Children aged 0–36 months admitted to the paediatric cardiac intensive care unit after elective cardiac surgery between January 2018 and July 2018 were included in the study. We evaluated the patients' demographics and clinical variables, nutritional status, adverse outcomes, and 30-day mortality rates.

      Results

      A total of 124 cases met the inclusion criteria. Results showed that the Risk Adjustment for Congenital Heart Surgery score ≥5, underweight status (weight-for-age Z score ≤−2), and stunting (length-for-age Z score ≤−2) were all indicators for increased mortality following congenital heart surgery. Underweight children also spent a prolonged stay in the intensive care unit. Stunting (length-for-age Z score ≤−2) was the most strongly associated variable with mortality.

      Conclusion

      The results confirm the impact of malnutrition on mortality, postoperative infection, and length of hospitalisation in children undergoing surgery for congenital heart disease.

      Keywords

      1. Introduction

      Malnutrition is defined as an imbalance between the consumption of nutrients and the cumulative energy/protein demand for maintenance and growth,
      • Iorember M.F.
      Malnutrition in chronic kidney disease.
      and it remains a significant health problem among children worldwide. Globally, one-third of children younger than 5 y are undernourished. In 2018, the United Nations Children's Fund reported that 155 million children younger than 5 y old were stunted and 52 million were underweight.

      Unicef. Levels and trends in child malnutrition. (May 2018 Edition). UN, SDG, UNICEF, WHO, World bank groups 2018. Available at: https://www.who.int/nutgrowthdb/estimates2017/en/.

      Congenital heart disease (CHD) is one of the most frequent congenital defects present at birth, with an incidence rate of 8–11 per 1000 live births,
      • Marwali E.M.
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      and has a high impact on neonatal morbidity and mortality.
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      Numerous studies have reported malnutrition to be a recognised cause of morbidity in children with CHD.
      • Peterson R.E.
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      ,
      • Vivanco-Munoz N.
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      • Peralta P.
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       Newborns and infants with CHD requiring surgical treatment face many obstacles in achieving good short- and long-term outcomes and ideal growth.
      • Dodge-Khatami A.
      Advances and research in congenital heart disease.
      The existence of additional chromosomal anomalies, cyanosis, and cardiac failure heightens the challenges after surgery.
      • Ross F.
      • Latham G.
      • Joffe D.
      • et al.
      Preoperative malnutrition is associated with increased mortality and adverse outcomes after pediatric cardiac surgery.
      Newborns/infants with cyanotic CHD are especially susceptible to acute or chronic starvation. Possible aetiologies involve insufficient intake (due to fatigue, oral aversion, dyspnoea, and/or early satiety), increased energy expenditure (including tachypnoea, and tachycardia), malabsorption (due to increased right-side heart pressure, lower cardiac output, and/or altered gastrointestinal function), and/or ineffective use of energy.
      • Kelleher D.K.
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      Thus, sufficient energy and protein intake are crucial for achieving normal growth and a strong immune system. Surgical trauma increases the metabolic/caloric need and increases metabolic stress in the malnourished newborn/infant as surgery drains their already-insufficient metabolic reserves.
      • Singer P.
      • Singer J.
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      As such, the probability of adverse outcomes and mortality after surgery increases. Optimal nutritional intake in the preoperative and postoperative phases can improve the metabolic stores of children with CHD, which is vital to prevent the adverse outcomes of surgical trauma.
      • Toole B.J.
      • Toole L.E.
      • Kyle U.G.
      • Cabrera A.G.
      • Orellana R.A.
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      Perioperative nutritional support and malnutrition in infants and children with congenital heart disease.

      1.1 Aim

      We aimed to explore the association between malnutrition and adverse outcomes in children aged 0–36 months undergoing surgery for CHD.

      2. Materials and methods

      2.1 Design

      This is a prospective cohort study.

      2.2 Setting

      This study was conducted in a 17-bed paediatric cardiac intensive care unit (PICU) in Turkey.

      2.3 Ethical approval

      All procedures performed in this study involving human participants follow the ethical standards of the institutional and/or national research committee and comply with the 1964 Helsinki Declaration and its later amendments. The institutional board approved the study protocol (28001928.501.01/25.05.2018), and written consent was obtained from the guardians of the children included in the study protocol.

      2.4 Recruitment and eligibility

      Children aged 0–36 months admitted to the PICU after elective cardiac surgery between January 2018 and July 2018 were included. Cases undergoing emergency cardiac surgery or subsequent surgeries during their hospitalisation were excluded.

      2.5 Assessed variables

      2.5.1 Demographic and clinical variables

      Age (days), gender, weight (grams), length (centimetres), prematurity (neonate at less than 37 weeks gestational age),

      Preterm Labor and Birth: Condition Information". National Institutes of Health. 3 November 2014. Archived from the original on 2 April 2015. Retrieved 7 March 2015.

      cyanotic heart disease,
      • Ossa Galvis M.M.
      • Bhakta R.T.
      • Tarmahomed A.
      • et al.
      Cyanotic heart disease. [Updated 2020 Oct 1].
      operative characteristics (cardiopulmonary bypass, duration on bypass, length of operation), mechanical circulation support
      • Ortuno S.
      • Delmas C.
      • Diehl J.L.
      • et al.
      Weaning from veno-arterial extracorporeal membrane oxygenation: which strategy to use?.
      (extracorporeal membrane oxygenation), sternal closure time (delayed due to myocardial oedema and/or bleeding or nondelayed),
      • Nelson-McMillan K.
      • Hornik C.P.
      • He X.
      • Vricella L.A.
      • Jacobs J.P.
      • Hill K.D.
      • et al.
      Delayed sternal closure in infant heart surgery-the importance of where and when: an analysis of the STS congenital heart surgery database.
      and Risk Adjustment for Congenital Heart Surgery (RACHS) scores
      • Jenkins K.J.
      • Gauvreau K.
      • Newburger J.W.
      • Spray T.L.
      • Moller J.H.
      • Iezzoni L.I.
      Consensus-based method for risk adjustment for surgery for congenital heart disease.
      (utilised to assess in-hospital mortality risk adjustment for paediatric cases undergoing cardiac surgery) were evaluated.
      Child development stages are as follows – Newborn: 0–1 months; Infant: 1–12 months; Toddler: 12–36 months.

      U.S. Department of Health & Human Services, Centers for disease control and prevention. Child Dev. https://www.cdc.gov/ncbddd/childdevelopment/positiveparenting/infants.html.

      World Health Organization, Newborn health in the Western Pacific, https://www.who.int/westernpacific/health-topics/newborn-health.

      • John M.
      Olssen, the newborn.

      2.5.2 Nutritional assessment

      The World Health Organization (WHO) growth standard charts were used for nutritional assessment. Length-for-age, weight-for-age, and weight-for-length Z scores were determined for every case using WHO standard charts (http://www.who.int/childgrowth/en/). Underweight was defined as weight-for-age Z score ≤−2, Stunting was defined as length-for-age Z score ≤−2, and Wasting was defined as weight-for-length Z score ≤ −2.

      2.5.3 Nutritional support

      Enteral nutrition is preferred as the method of nutrition support in our PICU, and we start enteral nutrition as soon as possible following PICU admission (except significant upper gastrointestinal bleeding, presence or high risk of necrotising enterocolitis, postoperative ileus, intestinal obstruction).
      The nutritional plan is decided for each patient according to age, medical history, and nutritional status with a dietitian. We prepared a nutritional support program based on the Baylor College of Medicine Guidelines for Neonatal Nutrition,
      • Whitfield J.M.
      • Charsha D.S.
      Neonatal care at Baylor University Medical Center: you've come a long way, baby!.
      the Schofield prediction equation,
      • Sion-Sarid R.
      • Cohen J.
      • Houri Z.
      • Singer P.
      Indirect calorimetry: a guide for optimizing nutritional support in the critically ill child.
      and the 2017 American Society for Parenteral and Enteral Nutrition guidelines.
      • Mehta N.M.
      • Skillman H.E.
      • Irving S.Y.
      • et al.
      Guidelines for the provision and assessment of nutrition support therapy in the pediatric critically ill patient: society of critical care medicine and American Society for parenteral and enteral nutrition.
      Because a significant proportion of the patients were malnourished and there was a prediction of requirement for long-time mechanical ventilation support, high energy and protein intake were planned as 90 kcal/kg/day and 3 g/kg/day, respectively. At the same time, stress factors were considered while calculating energy and protein intake. Enteral nutrition was delivered through a nasogastric tube by continuous infusion, starting at a low rate (5–10 ml/h according to the weight of the child), and gradually increased until entire requirements were delivered. Following any interruption other than feeding intolerance, feeding is restarted according to previously established feeding schedules and advanced as tolerated. We initiated parenteral nutrition in patients with malnutrition, low birth weight, or hypermetabolism if fasting is anticipated for 3 days or more.
      A separate wing of the hospital was made available for breastfeeding mothers to stay. Thus, mothers could feed their babies, aged 0–24 months, either directly breastfeeding or via expressing milk. Mother's milk was given enterally for mechanical ventilated patients. Patients aged 24–36 months with spontaneous breathing were fed orally, while those on a mechanical ventilator were fed through a nasogastric tube.

      2.5.4 Patient follow-up

      All patients were followed up for 30 days following surgery. If patients were discharged before this time, outpatient clinic visits were scheduled for the 30th day after the operation. In each case, the duration of mechanical ventilation, the instance of postoperative infection, length of PICU stay, hospitalisation time, and 30-day mortality were evaluated. Urinary tract infection, ventilator-associated pneumonia (developing 48–72 h after endotracheal intubation),
      • Chughtai M.
      • Gwam C.U.
      • Mohamed N.
      • et al.
      The epidemiology and risk factors for postoperative pneumonia.
      mediastinitis (deep sternal wound infection), and sepsis
      • Mathias B.
      • Mira J.C.
      • Larson S.D.
      Pediatric sepsis.
      were deemed postoperative infections.

      2.6 Statistical analysis

      The NCSS 2007 (Utah, USA) program for statistical analysis was used. Descriptive statistical methods (mean, standard deviation, median, first quarter, third quarter, frequency, percentage, minimum, maximum) were used to evaluate the study data. The Shapiro–Wilk test and graphical examinations were applied to test the suitability of quantitative data for normal distribution. Binary logistic regression analysis was used for univariable and multivariable evaluations of factors affecting mortality, cardiac arrest, and infection. Generalised linear models were used for univariable and multivariable assessments of factors affecting mechanical ventilation, length of PICU stay, and hospitalisation time. Statistical significance was accepted as p < 0.05.

      3. Results

      A total of 124 children met the inclusion criteria for the study. The gender distribution was 46/124 (37%) female and 78/124 (63%) male, with ages ranging between 0 and 36 months. Underweight and wasting were seen more frequently in infants (35/51 [68.6%] and 20/51 [39.2%], respectively), while stunting was observed most commonly in newborns (30/41 [73.2%]). Demographics and operational characteristics are shown in Table 1.
      Table 1Patient and operative characteristics.
      CharacteristicsMean ± SD, median (IQR) or n(%)
      Age (months), mean ± SD, median (Q1, Q3)9.08 ± 10.4, 5 (0.66, 16)
      Female/male, n (%)46/78 (37/63)
      Weight (grams), mean ± SD, median (Q1, Q3)6145.06 ± 3344.42, 4700 (3250, 8200)
      Length (centimetres), mean ± SD, median (Q1, Q3)62.72 ± 14.52, 59 (50, 71)
      Prematurity, n (%)20 (16.1)
      Cyanotic hearth disease, n (%)14 (11.2)
      Major noncardiac anomaly, n (%)5 (4)
      Preoperative mechanical ventilation, n (%)24 (19.3)
      Cardiopulmonary bypass, n (%)109 (87.9)
      Duration on bypass (minutes), mean ± SD, median (Q1, Q3)148.22 ± 127.07, 130 (90, 1080)
      Delayed sternal closure, n (%)
      Yes50 (40.3)
      No74 (59.7)
      Cardiac arrest, n (%)5 (4)
      ECMO: extracorporeal membrane oxygenation.
      ECMO, n (%)
      19 (15.3)
      Mortality (with in 30 days of surgery), n (%)10 (8)
      Postoperative infection15 (12.1)
      Duration of mechanical ventilation (postoperative) (days), mean ± SD, median (Q1, Q3)9.2 ± 10.2, 7 (3,12)
      Duration of PICU
      RACHS: Risk Adjustment for Congenital Heart Surgery.
      (days), mean ± SD, median (Q1, Q3)
      14.2 ± 13.2, 10 (5, 18)
      Hospital stay (days), mean ± SD, median (Q1, Q3)19.8 ± 14.7, 16 (10,24)
      RACHS: Risk Adjustment for Congenital Heart Surgery.
      RACHS score, n (%)
      115 (12.1)
      225 (20)
      343 (34.6)
      419 (15.3)
      510 (8)
      612 (9.7)
      Growth and development indices, n (%)
      Weight-for-age, Z score ≤−2
      All patients (n = 124)85 (59.7)
      Newborn (n = 41)24 (58.5)
      Infant (n = 51)35 (68.6)
      Toddler (n = 32)14 (43.7)
      Length-for-age, Z score ≤−2
      All patients (n = 124)88 (70.9)
      Newborn (n = 41)30 (73.2)
      Infant (n = 51)29 (56.8)
      Toddler (n = 32)15 (46.8)
      Weight-for-length, Z score ≤−2
      All patients (n = 124)43 (34.6)
      Newborn (n = 41)14 (34.1)
      Infant (n = 51)20 (39.2)
      Toddler (n = 32)9 (28.1)
      PICU: paediatric cardiac intensive care unit; SD: standard deviation.
      a RACHS: Risk Adjustment for Congenital Heart Surgery.
      b ECMO: extracorporeal membrane oxygenation.

      3.1 Factors affecting mortality

      Increased age and weight were associated with decreased mortality rates (p = 0.02 and p = 0.01, respectively). On the other hand, prematurity, longer cardiopulmonary bypass duration, RACHS score ≥5, underweight (weight-for-age Z score ≤−2), and stunting (length-for-age Z score ≤−2) were all associated with increased mortality rates (p = 0.04; p = 0.03; p = 0.01; p = 0.04; p = 0.04, respectively). Details of factors affecting mortality are shown in Table 2.
      Table 2Determination of factors affecting mortality, ICU LOS, hospital LOS, duration of mechanic ventilation, and postoperative infection.
      Mortality
      Logistic regression analysis.
      ICU LOS
      Linear regression analysis.
      Hospital LOS
      Linear regression analysis.
      Duration of mechanical ventilation
      Linear regression analysis.
      Postoperative infection
      Logistic regression analysis.
      OR (95% CI)pBeta (95% CI)pBeta (95% CI)pBeta (95% CI)pOR (95% CI)p
      Age (days)0.908 (0.995,1.001)0.02
      p < 0.05.
      −0.005 (−0.014, 0.003)0.221−0.002 (−0.012, 0.009)0.766−0.003 (−0.01, 0.004)0.375−0.997 (0.001,- 0.004)0.004
      p < 0.05.
      Gender (male)1.480 (0.351, 6.239)0.594−2.30 (−9.255, 4.639)0.510−3.59 (−11.476, 4.296)0.3670.103 (−4.393, 4.6)0.9641.045 (0.413,2.642)0.926
      Weight (gr)0.802 (1.001, 1.004)0.01
      p < 0.05.
      −0.002 (−0.003,-0.001)0.011
      p < 0.05.
      23.424 (15.918,30.93)0.137−0.001 (−0.002,-0.001)0.012
      p < 0.05.
      −1.002 (−0.003,-0.001)<0.001
      p < 0.05.
      Length (cm)0.949 (0.892, 1.009)0.096−0.228 (−0.429,-0.027)0.027
      p < 0.05.
      −0.137 (−0.374, 0.099)0.252−0.178 (−0.327,-0.028)0.020
      p < 0.05.
      −0.928 (−0.108,-0.045)<0.001
      p < 0.05.
      Prematurity1.909 (0.059, 4.408)0.04
      p < 0.05.
      3.668 (−2.084, 9.42)0.2082.794 (−3.106, 8.695)0.3481.623 (−3.255, 6.501)0.5093.131 (0.788,12.44)0.105
      Cyanotic hearth disease2.143 (0.378, 12.16)0.390−1.464 (−9.327, 6.399)0.7123.211 (−8.782, 15.204)0.5957.885 (−4.556, 20.326)0.2111.676 (0.387, 7.257)0.490
      CBP
      CPB: cardiopulmonary bypass; Mec.Vent.: mechanical ventilation; RACHS: Risk adjustment for congenital heart surgery; ECMO: extracorporeal membrane oxygenation.
      0.467 (0.082, 2.648)0.3900.08 (−8.242, 8.402)0.9850.815 (−6.429, 8.06)0.823−2.124 (−9.736, 5.489)0.5801.013 (0.25, 4.106)0.985
      Duration of CPB
      CPB: cardiopulmonary bypass; Mec.Vent.: mechanical ventilation; RACHS: Risk adjustment for congenital heart surgery; ECMO: extracorporeal membrane oxygenation.
      (min)
      1.999 (0.993, 1.006)0.03
      p < 0.05.
      −0.006 (−0.019, 0.008)0.385−0.005 (−0.019, 0.009)0.491−0.009 (−0.02, 0.001)0.0820.999 (0.995, 1.003)0.570
      Noncardiac anomaly
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      0.999−6.779 (−12.496, −1.063)0.021
      p < 0.05.
      −10.23 (−17.636, −2.824)0.076.354 (−9.697, −3.01)<0.001
      p < 0.05.
      0.381 (0.033, 4.389)0.439
      Preoperative Mec.Vent.
      CPB: cardiopulmonary bypass; Mec.Vent.: mechanical ventilation; RACHS: Risk adjustment for congenital heart surgery; ECMO: extracorporeal membrane oxygenation.
      1.964 (0.443, 8.713)0.3741.016 (−5.034, 7.066)0.7392.776 (−5.595, 11.148)0.5117.879 (−0.15, 15.907)0.0544 (1.027,15.57)0.046
      p < 0.05.
      RACHS
      CPB: cardiopulmonary bypass; Mec.Vent.: mechanical ventilation; RACHS: Risk adjustment for congenital heart surgery; ECMO: extracorporeal membrane oxygenation.
      (5–6)
      5.750 (1.248, 36.522)0.01
      p < 0.05.
      2.629 (−8.075, 13.332)0.026
      p < 0.05.
      2.229 (−8.293, 12.751)0.67412.049 (−3.629, 27.727)0.1301.06 (0.221, 5.092)0.942
      Weight-for-age, Z score ≤−21.675 (0.398,7.049)0.04
      p < 0.05.
      2.587 (−4.697, 9.87)0.043
      p < 0.05.
      1.811 (−6.057, 9.68)0.048
      p < 0.05.
      5.887 (1.658, 10.115)0.007
      p < 0.05.
      3.712 (1.398, 9.86)0.008
      p < 0.05.
      Length-for-age, Z score ≤−26.075 (0.727, 50.757)0.04
      p < 0.05.
      3.22 (−3.523, 9.963)0.044
      p < 0.05.
      −0.067 (−7.64, 7.506)0.9864.452 (0.066, 8.839)0.047
      p < 0.05.
      4.156 (1.58, 10.934)0.004
      p < 0.05.
      Weight-for length, Z score ≤−23.286 (0.838,12.884)0.0882.8 (−2.541, 8.141)0.3000.887 (−5.224, 6.999)0.7735.298 (0.089, 10.507)0.046
      p < 0.05.
      3.354 (1.204, 9.346)0.021
      p < 0.05.
      Weight-for-age0.787 (0.465, 1.33)0.371−1.737 (−3.42, −0.054)0.043
      p < 0.05.
      −1.063 (−2.984, 0.859)0.024
      p < 0.05.
      −1.875 (−3.019, −0.732)0.002
      p < 0.05.
      0.540 (0.365, 0.801)0.245
      Length-for-age0.849 (0.503, 1.435)0.542−1.574 (−3.452, 0.303)0.099−0.538 (−2.557, 1.482)0.047
      p < 0.05.
      −1.499 (−2.896, −0.101)0.036
      p < 0.05.
      0.534 (0.357, 0.799)0.062
      Weight-for- length0.667 (0.4, 1.111)0.1200.386 (−1.862, 2.633)0.7331.088 (−1.407, 3.583)0.388−0.94 (−3.158, 1.278)0.4010.668 (0.456, 0.979)0.090
      Delayed sternal closure
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      −9.199 (−15.584, −2.815)0.005
      p < 0.05.
      −10.002 (−17.174, −2.83)0.007
      p < 0.05.
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      ECMO
      CPB: cardiopulmonary bypass; Mec.Vent.: mechanical ventilation; RACHS: Risk adjustment for congenital heart surgery; ECMO: extracorporeal membrane oxygenation.
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      6.892 (−7.021, 20.806)0.32712.244 (−3.528, 28.016)0.126
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      Postop infection
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      7.172 (1.724, 12.621)0.011
      p < 0.05.
      9.283 (3.316, 15.251)0.003
      p < 0.05.
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      The OR or beta value could not be calculated because the affecting determinant was not observed.
      CI: confidence interval; ICU: intensive care unit; LOS: length of stay; OR: odds ratio.
      a Logistic regression analysis.
      b Linear regression analysis.
      c p < 0.05.
      d The OR or beta value could not be calculated because the affecting determinant was not observed.
      e CPB: cardiopulmonary bypass; Mec.Vent.: mechanical ventilation; RACHS: Risk adjustment for congenital heart surgery; ECMO: extracorporeal membrane oxygenation.

      3.2 Factors affecting the duration of mechanical ventilation

      There was an inverse association between decrease in weight and length and longer duration of mechanical ventilation (Beta [95% confidence interval {Cl}]: −0.178 [−0.327, −0.028], p = 0.012; Beta [95% Cl]: −0.001 [−0.002, −0.001], p = 0.02, respectively). The duration of mechanical ventilation was longer in patients who were underweight and short.
      Other factors related to extended mechanical ventilation were underweight, stunting, wasting, low weight-for-age Z score, and shorter length-for-age Z score (Table 2). Additionally, increase in length-for-age Z score in the Toddler group was associated with a decrease in mechanical ventilation time (Beta [95% Cl]: −7.127 [−12.763, −1.491], p = 0.017).

      3.3 Factors affecting postoperative infection

      There was an inverse association between age, length, weight, and postoperative infection rates (odds ratio [OR] [95% Cl]: −0.997 [0.001, −0.004], p = 0.004; OR [95% Cl]: −0.928 [−0.108, −0.045], p < 0.001; OR [95% Cl]: −1.002 [−0.003, −0.001], p < 0.001, respectively). Postoperative infection rates were higher in younger, shorter, and less weighted patients. Additionally, underweight (weight-for-age Z score ≤−2), stunting (length-for-age Z score ≤−2), and wasting (weight-for-length Z score≤−2) were other factors related to postoperative infection rates (p = 0.008; p = 0.004; p = 0.001, respectively) (Table 2).

      3.4 Factors affecting the length of stay in the PICU

      Being shorter, of less weight, and underweight had an inverse association with prolonged ICU stay (p = 0.011; p = 0.027; p = 0.043, respectively). Other factors associated to prolonged PICU stay were the RACHS score ≥5, underweight (weight-for-age Z score ≤−2), delayed sternal closure, and postoperative infection (Table 2).

      3.5 Factors affecting the length of stay in hospital

      There was a relationship between underweight patients and an increased length of hospital stay (p = 0.048).

      4. Discussion

      The study highlights the negative impact of malnutrition on mortality in patients aged 0–36 months who undergo cardiac surgery, and stunting has the most noticeable effect.
      Hypercatabolism, following cardiac surgery, consumes the limited amounts of hepatic glycogen and adipose tissue reserves that are present in newborns, infants, or toddlers. Therefore, deficiency in these metabolic stores is associated with an increased risk of mortality among the youngest children undergoing cardiac surgery.
      • Ross F.
      • Latham G.
      • Joffe D.
      • et al.
      Preoperative malnutrition is associated with increased mortality and adverse outcomes after pediatric cardiac surgery.
      ,
      • Shan Lim C.Y.
      • Boon Lim J.K.
      • Moorakonda R.B.
      • et al.
      The impact of preoperative nutritional status on outcomes following congenital heart surgery.
      In the study, more than half of the children were underweight, a sign of acute malnutrition, and more than 70% had stunting, considered an indication of chronic malnutrition. This supports previous studies that indicate a particularly high rate of malnutrition in children with CHD who live in developing countries. The malnutrition rates reported in the literature for children who undergo surgery for CHD range from 27% to 90.4%.
      • Mehrizi A.
      • Drash A.
      Growth disturbance in congenital heart disease.
      ,
      • Tokel K.
      • Azak E.
      • Ayabakan C.
      • Varan B.
      • Aslamaci S.A.
      • Mercan S.
      Somatic growth after corrective surgery for congenital heart disease.
      The 1962 study by Mehrizi and Dash described a 27% rate,
      • Mehrizi A.
      • Drash A.
      Growth disturbance in congenital heart disease.
      while more recent research from Turkey puts this number at a much higher to 85%;
      • Tokel K.
      • Azak E.
      • Ayabakan C.
      • Varan B.
      • Aslamaci S.A.
      • Mercan S.
      Somatic growth after corrective surgery for congenital heart disease.
      and in Nigeria, the rate is reported to be 90.4%.
      • Okoromah C.A.
      • Ekure E.N.
      • Lesi F.E.
      • Okunowo W.O.
      • Tijani B.O.
      • Okeiyi J.C.
      Prevalence, profile and predictors of malnutrition in children with congenital heart defects: a case-control observational study.
      When investigating mortality rates of children undergoing cardiac surgery, the link between age/weight/length and mortality is a well-documented concept.
      • Ross F.
      • Latham G.
      • Joffe D.
      • et al.
      Preoperative malnutrition is associated with increased mortality and adverse outcomes after pediatric cardiac surgery.
      ,
      • Toole B.J.
      • Toole L.E.
      • Kyle U.G.
      • Cabrera A.G.
      • Orellana R.A.
      • Coss-Bu J.A.
      Perioperative nutritional support and malnutrition in infants and children with congenital heart disease.
      ,
      • Jenkins K.J.
      • Gauvreau K.
      • Newburger J.W.
      • Spray T.L.
      • Moller J.H.
      • Iezzoni L.I.
      Consensus-based method for risk adjustment for surgery for congenital heart disease.
      ,
      • Oyarzun I.
      • Claveria C.
      • Larios G.
      • Le Roy C.
      Nutritional recovery after cardiac surgery in children with congenital heart disease.
      Inevitably, paediatric candidates for cardiac surgery often have complicated comorbidities and severe physiological variations. There may be difficulties related to immature organ development and the immune system, while cardiopulmonary bypass can cause severe pathophysiological outcomes in patients with such a small volume of intravascular blood. In the study, stunting, a marker for foetal undernutrition, had a substantial impact on mortality, increasing the risk by 6.075 times. This result was in line with previous studies.
      • Cameron J.W.
      • Rosenthal A.
      • Olson A.D.
      Malnutrition in hospitalized children with congenital heart disease.
      • Marino L.V.
      • Magee A.
      A cross-sectional audit of the prevalence of stunting in children attending a regional pediatric cardiology service.
      • Gupta R.
      • Misra A.
      • Pais P.
      • Rastogi P.
      • Gupta V.P.
      Correlation of regional cardiovascular disease mortality in India with lifestyle and nutritional factors.
      Although the results did not show any relation between stunting and length of hospital stay, associations were seen between stunting and an increase in the length of PICU stay, duration of mechanical ventilation, and risk of postoperative infection.
      Recent studies have shown that, in cases where the Glenn procedure is used, a higher weight-for-age Z score correlates to a shorter hospitalisation time.
      • Zaloga G.P.
      • Roberts P.R.
      • Marik P.
      Feeding the hemodynamically unstable patient: a critical evaluation of the evidence.
      Also, in patients awaiting the Norwood procedure, successful preoperative enteral nutrition is associated with a shorter transition to full enteral feeding.
      • Li J.
      • Zhang G.
      • Herridge J.
      • et al.
      Energy expenditure and caloric and protein intake in infants following the Norwood procedure.
      Institutions have varying approaches to dealing with malnourished infants, such as which to treat with nasogastric feeding, which can be breastfed, and the exact time to start enteral nutrition via gastric tube.
      • Jenkins K.J.
      • Gauvreau K.
      • Newburger J.W.
      • Spray T.L.
      • Moller J.H.
      • Iezzoni L.I.
      Consensus-based method for risk adjustment for surgery for congenital heart disease.
      Although many institutions discharge patients with a nasogastric feeding tube in place, some prefer to use a surgically placed percutaneous gastric tube, which is the most reliable way of delivering nutrients to maintain nutritional support.
      • Cameron J.W.
      • Rosenthal A.
      • Olson A.D.
      Malnutrition in hospitalized children with congenital heart disease.
      According to the protocol we followed, malnourished newborns/infants who have undergone cardiac surgery are fed with formula via a nasogastric tube, while those with a healthy sucking reflex are assigned formula + breastfeeding.
      Feeding difficulties in newborns and infants undergoing cardiac surgery are a common problem, although the actual mechanism causing this remains unclear.
      • Medoff-Cooper B.
      • Naim M.
      • Torowicz D.
      • Mott A.
      Feeding, growth, and nutrition in children with congenitally malformed hearts.
      Some newborns completely resist sucking, whereas others lose their sucking reflex shortly after surgery.
      • Bourin P.F.
      • Puech M.
      • Woisard V.
      Pediatric aspect of dysphagia.
      In fact, swallowing begins in the 16th gestational week and is expected to be a normal functioning reflex at birth in healthy newborns.
      • Abdallah Y.
      • Namiiro F.
      • Nankunda J.
      • et al.
      Mortality among very low birth weight infants after hospital discharge in a low resource setting.
      However, laryngopharyngeal dysfunction, which inescapably leads to problematic feeding, is often seen in newborns undergoing major cardiac surgery. Despite optimal medical care, weight gain is less than expected in these children.
      • Licht D.J.
      • Shera D.M.
      • Clancy R.R.
      • et al.
      Brain maturation is delayed in infants with complex congenital heart defects.
      ,
      • Jadcherla S.R.
      • Vijayapal A.S.
      • Leuthner S.
      Feeding abilities in neonates with congenital heart disease: a retrospective study.
      The percentage of patients with stunting, which indicates chronic undernutrition, was 70.9% in our study group. It is likely that chronic malnutrition, which begins in the intrauterine period and continues into the extrauterine period, has a negative impact on mortality after major cardiac surgery. Our results showed that mortality rate, duration in the PICU, duration of mechanical ventilation, and postoperative infection were higher in stunted patients.
      The delay of sternal closure is also of importance. Delaying sternal closure helps the patient to settle down haemodynamically by providing space for the dilated, dysfunctional ventricle or poorly compliant lungs to expand.
      • Ozker E.
      • Saritas B.
      • Vuran C.
      • et al.
      Delayed sternal closure after pediatric cardiac operations; single-center experience: a retrospective study.
      The advantages of delayed sternal closure are more significant in paediatric cardiac surgery because of a larger cardiac size relative to the thoracic cavity. Besides this, postsurgery cardiac oedema causes diastolic restriction and leads to a tamponade-like condition of the right ventricle.
      • Kundan S.
      • Tailor K.
      • Radhakrishnan H.B.
      • et al.
      Elective delayed sternal closure portends better outcomes in congenital heart surgery: a retrospective observational study.
      We observed that children who underwent delayed sternal closure had prolonged PICU stay and hospitalisation. The haemodynamically unstable condition of children undergoing cardiac surgery explains the longer PICU and hospital stays.
      The interrelation between undernutrition and adverse postoperative outcomes demonstrated may force our institution as well as other paediatric cardiac surgery centres to place more emphasis on preoperative nutritional support before complex cardiac surgery. Despite the extraordinary efforts taken in most paediatric cardiac surgery institutions, a standardised nutritional care protocol for neonates or infants with CHD, which could lead to improved nutritional status, is lacking. Further investigations are needed to assess the possible impact of an optimised preoperative enteral nutrition program on postoperative outcomes.

      5. Limitations

      There are several limitations to consider. The primary constraint is that the cohort was from a single institution with a relatively small number of cases. The short follow-up period is a second limitation. Unlike many previous studies,
      • Nelson-McMillan K.
      • Hornik C.P.
      • He X.
      • Vricella L.A.
      • Jacobs J.P.
      • Hill K.D.
      • et al.
      Delayed sternal closure in infant heart surgery-the importance of where and when: an analysis of the STS congenital heart surgery database.
      ,
      • Yıldız O.
      • Kasar T.
      • Öztürk E.
      • Tüzün B.
      • Altın H.F.
      • Onan İ.S.
      • et al.
      Analysis of congenital heart surgery results: a comparison of four risk scoring systems.
      ,
      • Padley J.R.
      • Cole A.D.
      • Pye V.E.
      • et al.
      Five-year analysis of operative mortality and neonatal outcomes in congenital heart disease.
      children with a high RACHS score (RACHS score: 4-5-6) were included in this study, and this may have influenced the resulting rate of prolonged PICU hospitalisation. This issue was not investigated further as the focus of the study was the link between the children's preoperative nutritional status and its postoperative effects.
      Indeed, evaluating the association between the RACHS score and hospital/PICU stay is a separate topic. We recommend that multicentre studies conducted with larger sample sizes and provision for long-term follow-up are needed to confirm our findings.
      Data about daily nutritional plan were not used in the study. We think that these data would not contribute to the purpose of our study but may clarify the nutrition of critically ill patients in the intensive care unit. Thus, it would be better if these data could be included the study.

      6. Conclusions

      We assessed the association between malnutrition present on admission to the PICU and postoperative outcomes in patients who underwent surgery for CHD. Our research confirms the impact of malnutrition on mortality in children having surgery for CHD and poor postoperative outcomes, including postoperative infection and extended length of hospital stay. We believe international guidelines on the identification, management, and treatment of malnourished paediatric cases should be established with the aim of reducing mortality rates and preventing adverse surgical outcomes. In addition, in the light of these international guidelines, each paediatric cardiac surgery institution should determine their own strategies for managing newborns/infants who are malnourished before surgery.

      Funding

      The authors have received no funding related to this study.

      Conflict of Interest

      The authors declare no conflict of interest.

      CRediT authorship contribution statement

      Sibel Yilmaz Ferhatoglu: Conceptualisation, Methodology, Software, Validation, Formal analysis, Investigation, Resources, Data curation, Writing – original draft, Writing – review & editing, Visualisation, Project administration; Okan Yurdakok: Resources; Nurgul Yurtseven: Supervision.

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