Prevalence and factors associated with thoracic alterations in infants born prematurely

Prevalência e fatores associados às alterações torácicas em lactentes nascidos prematuros

ORIGINAL ARTICLE

Prevalence and factors associated with thoracic alterations in infants born prematurely

Prevalência e fatores associados às alterações torácicas em lactentes nascidos prematuros

Josy Davidson^I; Kessey Maria B. Garcia^II; Liu C. Yi^III; Ana Lucia Goulart^IV; Amelia Miyashiro N. dos Santos^V

^IPhD, Physiotherapist, Department of Pediatrics, Neonatal Division of Medicine, Universidade Federal de São Paulo (UNIFESP), SP, São Paulo, SP, Brazil

^IIMSc, Physiotherapist, Department of Pediatrics, Neonatal Division of Medicine, UNIFESP, São Paulo, SP, Brazil

^IIIPhD, Physiotherapist, Professor of Musculoskeletal Physiotherapy Section, UNIFESP, São Paulo, SP, Brazil

^IVAdjunct Professor, Department of Pediatrics, Neonatal Division of Medicine, UNIFESP, São Paulo, SP, Brazil

^VAssociate Professor, Department of Pediatrics, Neonatal Division of Medicine, UNIFESP, São Paulo, SP, Brazil

^{Correspondence to}

SUMMARY

OBJECTIVE: To determine the prevalence of thoracic musculoskeletal alterations and associated factors in infants born prematurely.

METHODS: This was a cross sectional study with infants in the first year of age, born prematurely with birth weight < 2,000 g, who were followed up at the Premature Clinic from February, 2007 to December, 2008. Exclusion criteria were: maj or congenital malformations as defined by the Centers for Disease Control and Prevention (CDC), grade III/IV intraventricular hemorrhage, or periventricular leucomalacia. Physical examinations performed independently by two physiotherapists were used to assess shoulder elevation and thoracic retractions. Comparisons between groups were performed using the chi-squared test or Fisher's exact test for categorical variables, and Mann-Whitney's test or Student's t-test were used for continuous variables. Interobserver reliability between the two physiotherapists was assessed by the kappa coefficient. Variables associated with these thoracic musculoskeletal alterations were studied by univariate and multiple logistic analyses. Statistical differences were considered significant when p < 0.05. This study was approved by the ethical committee of the institution, and parents/guardians signed an informed consent.

RESULTS: 121 infants with a gestational age of 31.1 ± 2.8 weeks and birth weight of 1,400 ± 338 g were included. Thoracic alterations were detected by Physiotherapist 1 in 81 (66.9%) infants, and in 83 (68.6%) by Physiotherapist 2 (kappa coefficient = 0.77). By multivariate logistic regression analysis, factors associated with thoracic musculoskeletal alterations were: respiratory distress syndrome (odds ratio [OR] = 3.246, 95% confidence interval [CI]: 1.237-8.732), bronchopulmonary dysplasia (OR = 11.138, 95% CI: 1.339-92.621), and low length/age ratio (OR = 4.571, 95% CI: 1.371-15.242).

CONCLUSION: The prevalence of thoracic alterations was high in infants born prematurely, and was associated with pulmonary disease and low length/age ratio.

Keywords: Child; physiotherapy; infant; premature; posture; chest.

RESUMO

OBJETIVO: Determinar a prevalência e os fatores associados às alterações torácicas musculoesqueléticas em lactentes nascidos prematuros.

MÉTODOS: Estudo transversal com lactentes no primeiro ano de vida, nascidos prematuros com peso < 2000 g e acompanhados em um ambulatório de seguimento de prematuros, de fevereiro/2007 a dezembro/2008. Foram excluídas crianças com malformações maiores definidas pelo CDC ou com hemorragia peri-intraventricular grau III/IV ou leucomalácia periventricular. Duas fisioterapeutas realizaram o exame físico, avaliando, de modo independente, a elevação de ombros e as retracões da caixa torácica. O estudo foi aprovado pelo Comitê de Ética em Pesquisa da Instituição, sendo solicitada assinatura do Termo de Consentimento pelos pais. As variáveis numéricas foram comparadas pelo teste t ou Mann-Whitney. O grau de concordância entre as avaliações das fisioterapeutas foi obtido pelo coeficiente kappa e as variáveis associadas às alterações torácicas foram estudadas por regressão logística univariada e múltipla. Considerou-se significante p < 0,05.

RESULTADOS: Foram estudados 121 lactentes com idade gestacional de 31,1 ± 2,8 semanas e peso ao nascer de 1400 ± 338 g. A fisioterapeuta 1 detectou alterações torácicas em 81 (66,9%) lactentes e a fisioterapeuta 2 em 83 (68,6%) (coeficiente kappa = 0,77). Os fatores associados às alterações musculoesqueléticas foram: síndrome do desconforto respiratório no período neonatal (OR=3,246; IC 95%: 1,237-8,732), ter apresentado displasia broncopulmonar (OR=11,138; IC 95%: 1,339-92,621) e relação comprimento para a idade alterada (OR=4,571; IC 95%: 1,371-15,242).

CONCLUSÃO: A prevalência de alterações torácicas foi alta em lactentes nascidos prematuros e associou-se a doença pulmonar no período neonatal e baixa relação comprimento/idade.

Unitermos: Criança; fisioterapia; prematuro; postura; caixa torácica.

INTRODUCTION

Immaturity of the lungs, rib cage, and central nervous system frequently require prolonged mechanical ventilation and oxygen therapy in preterm infants. These therapies may be associated with lung injuries such as bronchopulmonary dysplasia, increasing morbidity and prolonging hospitalization^1,2.

Recent studies have demonstrated that airway trapping in infants with bronchopulmonary dysplasia persists until adulthood³. This could increase the effort required to breathe, thus causing biomechanical alterations during childhood and adulthood, suggesting that preterm infants should be routinely examined until adulthood.

To the authors' knowledge, there are no studies on the prevalence of thoracic musculoskeletal abnormalities stemming from premature birth and associated factors in preterm infants after discharge from neonatal intensive care units (NICUs).

Thus, the purpose of this study was to assess the frequency and the factors associated with such abnormalities during the first year of life in infants born prematurely.

METHODS

This is a cross-sectional study with infants aged 1 to 12 months, born before 37 weeks of gestation, and with a birth weight < 2,000g who were regularly examined at the Premature Clinic between February, 2007 and December, 2008. The study was approved by the ethics committee of the institution, and the parents signed an informed consent.

Preterm infants included in the study received routine care from a team of physiotherapists who performed daily bronchial hygiene, positioning, and stretching during their NICU stay. After discharge from the NICU, and before inclusion in the study, the parents received routine general recommendations regarding stimulation of their children's motor development.

Exclusion criteria for this study were major congenital malformations identified according to the Center for Diseases Control and Prevention (2012)⁴ guideline, grade III/IV intraventricular hemorrhage or periventricular leukomalacia diagnosed by cranial ultrasound and/or magnetic resonance^5,6, or presence of acute respiratory tract infections in the previous two weeks.

Infants in the study underwent physical examination followed by a review of their medical charts for birth conditions and clinical evolution. Since physical examination is a subjective tool for detecting thoracic abnormalities, it was independently performed by two physiotherapists, in order to improve reliability (Physiotherapist 1 had ten years of experience in evaluating premature infants, Physiotherapist 2 had four years of experience). All infants were placed in the supine position, without clothes. Based on the established frequencies of clinical alterations observed in adults and children with chronic pulmonary disease, two abnormalities were specifically evaluated:

- Fixed elevation of the shoulders (positioning of the rib cage in the inhalation phase when the child was in the exhalation phase), or muscle tension in the neck and shoulders at rest.

- Retraction in the rib cage (anterolateral region of the thorax between the inframamillary region and lower anterior ribs) was recorded when there was a local depression during inhalation and exhalation.

STATISTICAL ANALYSIS

Statistical analysis was performed using the Statistical Package for the Social Sciences (SPSS) for Windows

(v. 17.0 - Chicago, IL, USA). Comparisons between groups were performed with the chi-squared test or Fisher's exact test for categorical variables, and Student's t-test for continuous variables. Inter-observer reliability between the two physiotherapists was assessed by the kappa coefficient. Univariate analysis identified independent clinical factors associated with the presence of thoracic alterations (dependent variable). Significant clinical and statistical variables identified in the univariate analysis were further included in a multivariate logistic regression model (backward stepwise). Differences were considered significant when p-values were < 0.05.

RESULTS

During the study period, 162 infants aged 1 to 12 months were examined at the Premature Clinic. Of these, 27 (16.7%) were excluded: 17 with major malformations, five with grade III/IV intraventricular hemorrhage and/or periventricular leukomalacia, and five due to parental refusal. Of the 135 infants who met the eligibility criteria, 14 (10.4%) missed evaluation appointments. 121 (89.6%) infants were included, with a mean gestational age at birth of 31.1 ± 2.8 weeks (25.0-36.9 weeks), birth weight of 1,400 ± 338 g (715-1,990g), median first minute Apgar score of 8 (range: 2-9), and median fifth minute Apgar score of 9 (range: 6-10). Fifty-seven (47.1%) of the selected infants were males. On enrollment, the infants had a mean age of 5.3 ± 2.4 months (median of 5.3, range: 0.6 days to 11.7 months). The post-conceptual age at study entry was of 3.3 ± 2.4 months (median of 3, range: -0.7 to 10.3 months).

On physical examination, Physiotherapist 1 identified 81 (66.9%) infants with musculoskeletal alterations: 22 (18.2%) with elevated shoulders, 32 (26.4%) with thoracic retraction, and 27 (22.3%) with both abnormalities. Physiotherapist 2 identified 83 (68.6%) infants with musculo skeletal abnormalities: 16 (13.2%) with elevated shoulders, 43 (35.5%) with thoracic retraction, and 24 (19.8%) with both abnormalities. There was agreement between the two observers in 109 cases (90.1%) with elevated shoulders and/or thoracic retraction, in 106 cases (87.6%) with elevated shoulders, and in 109 cases (90.1%) with thoracic retraction. This corresponds to kappa coefficients of 0.77 (standard error = 0.06), 0.74 (standard error = 0.06), and 0.80 (standard error = 0.05), respectively.

Analysis of the prevalence of thoracic alterations and associated factors was performed on the physical examination results reported by Physiotherapist 1, because of her greater professional experience.

Demographic and clinical characteristics of the studied infants are shown in Table 1. Regardless of the presence of thoracic alterations, infants in the study exhibited similar nutritional status (weight/age ratio, length/age ratio, weight/length ratio, and body mass index, according to the World Health Organization [WHO] Child Growth Standards)⁷, frequency of bronchiolitis and/or pneumonia (18.5% versus 10.3%, p = 0.30), sibilance (18.5% versus 12.8%, p = 0.43), and need for hospitalization after discharge from the neonatal unit (14.8% versus 7.5%, p = 0.38). Likelihood ratios of the independent variables for the occurrence of thoracic alterations studied by univariate analysis are shown in Table 2.

The following statistically significant variables derived from the univariate analysis were included in the multivariate model: gestational age, presence of respiratory distress syndrome, patent ductus arteriosus (with clinical signs and symptoms and/or echocardiography alterations), bronchopulmonary dysplasia (stated as a need for supplemental oxygen therapy after 28 days of life), clinical sepsis, number of days on mechanical ventilation, length of NICU stay, and low length/age ratio. After adjustment for variables included in the model, the multivariate logistic regression analysis demonstrated that the chance of presenting thoracic alterations was higher in infants who developed respiratory distress syndrome and/or bronchopulmonary dysplasia during their NICU stay and in infants with a low length/age ratio in the first year of life (Table 3).

DISCUSSION

To the authors' knowledge, this is the first study assessing thoracic musculoskeletal abnormalities in infants born prematurely. Although there are no data for comparison, the prevalence of thoracic abnormalities found in this study appears to be high, especially considering that the infants included in this study received routine physiotherapy in the neonatal unit for the prevention or rehabilitation of cardiopulmonary impairment.

In premature infants, some factors could explain the high prevalence of musculoskeletal alterations found in this study. The immaturity of the lungs and rib cage favors an increase in the effort required to breathe, in case of acute respiratory illness. Under these conditions, accessory respiratory muscles, such as the trapezius and sternocleidomastoid, are recruited, thus increasing thoracoabdominal asynchronism. Successive increases in respiratory work during the neonatal period can alter respiratory muscles and, in the long-term, rib cage configuration. Studies evaluating chest radiographs of children with bronchopulmonary dysplasia showed that these patients have significantly flatter chests than children without any respiratory diseases².

Studies of adolescents with asthma also indicate that the increased respiratory work that is caused by airway obstruction could permanently alter the rib cage configuration⁸. In patients with chronic obstructive pulmonary disease, the hyperinflation caused by parenchymal destruction could increase the rib cage diameter. The resulting altered diaphragm position, and reduced muscle contraction and tidal volume, cause the recruitment of accessory muscles of the neck and upper rib cage in order to to maintain ventilatory demand, thereby causing typical postural abnormalities in the long-term^9,10.

The thoracic alterations observed in this study could be explained by physiological and anatomical factors. The development of shoulder elevation reflects the use of neck and upper thorax muscles, such as the trapezius, sternocleidomastoid, and pectoral muscles, as imposed by increased respiratory effort. Thoracic retraction occurs due to thoracoabdominal asynchronism, causing depression of the rib and sternum¹¹.

According to the univariate analysis, every one-week decrease in gestational age increased the probability of having such abnormalities by 1.3-fold, and every 10g decrease in birth weight increased such a chance by 10fold. This suggests that lower gestational age and lower birth weight represent a greater probability of morbidity and need for life support, particularly, mechanical ventilation and oxygen therapy. Further, the univariate analysis demonstrated that all variables related to respiratory illness and the need for life support increased the probability of thoracic abnormalities in the first year of life (Table 2). Respiratory distress syndrome, patent ductus arteriosus, and bronchopulmonary dysplasia are interrelated and significantly contribute to the occurrence of thoracic musculoskeletal alterations. The presence of patent ductus arteriosus is known to contribute to the development of bronchopulmonary dysplasia¹², whose clinical consequences may persist into adolescence¹³. Similarly, the length of stay in the NICU represents the extent of clinical evolution during the neonatal period, and thus showed an association with thoracic abnormalities. The final model of the multivariate logistic regression analysis indicated that the presence of respiratory distress syndrome, bronchopulmonary dysplasia, and impaired growth as measured by length/age ratio were associated with thoracic abnormalities. This reinforces the hypothesis that thoracic alterations detected in the first year of life could be related to neonatal lung diseases.

Bronchopulmonary dysplasia may be followed by obstructive impaired lung function in the first years of life^11,13, and may cause biomechanical alterations and recruitment of all respiratory muscles, including the accessory muscles, over a long period, leading to thoracic alterations. Data shown in the present study corroborates this hypothesis.

The association between thoracic alterations and low length/age ratio found in the univariate and multivariate regression analysis appears to be a consequence of the high caloric consumption caused by increased respiratory effort, rather than a true cause of thoracic abnormality. Factors such as intensive care intervention, poor nutrition, increased respiratory effort, and infections during the neonatal period appear to contribute to impaired growth. Children with bronchopulmonary dysplasia showed smaller weight and length increments than children born prematurely who did not have any respiratory diseases during the first year of life^14,15. This minimal gain in weight and height may persist until adulthood¹⁶.

It would be expected that the occurrence of bronchiolitis and pneumonia after discharge from the neonatal unit would increase the chance of thoracic alterations^17,18. However, the number of infants with bronchiolitis or pneumonia in this study did not provide the necessary statistical power to demonstrate this association.

A limitation of this study was that the prevalence of observed musculoskeletal alterations might have been affected by the fact that approximately 10% of the eligible infants were not included. A physical examination is a qualitative and subjective tool, and is dependent on the examiner's experience¹⁹; this could also be mentioned as a limitation of this study. However, in the present study, physical examinations were performed by skilled professionals and showed good inter-rater reliability, thereby justifying its use as a reference standard for the assessment of musculoskeletal alterations. Moreover, in a recent study describing a new objective tool for the detection of thoracic abnormalities based on photogrammetry, the researchers found a good correlation between shoulder elevation detected by physical examination and the measurement of the manubrium/acromion/trapezius angle (intraclass correlation coefficient > 0.9), and between thoracic retraction and measurement of the deep thoracic retraction (intraclass correlation coefficient > 0.8)²⁰.

As the presence of thoracic alterations was found to be associated with neonatal pulmonary diseases, a new study assessing pulmonary function in infants born prematurely is already underway in this institution to investigate whether these alterations are truly related to impaired pulmonary function, as has been previously described^21,22.

CONCLUSIONS

The prevalence of thoracic alterations was high in infants born prematurely, and may also have compromised the growth rate of these infants during the first year of life. If evidence of thoracic musculoskeletal alterations in infants born prematurely is confirmed by new studies, it will have implications for follow-up protocols after NICU discharge.

Submitted on: 12/01/2011

Approved on: 07/10/2012

Financial support: Josy Davidson was supported by a Brazilian Government Scholarship from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) as a postgraduate student

Conflict of interest: None.

Study conducted at the Department of Pediatrics, Neonatal Division of Medicine, Universidade Federal de São Paulo, SP, Brazil

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Publication Dates

• Publication in this collection
  13 Dec 2012
• Date of issue
  Dec 2012

History

• Received
  12 Jan 2011
• Accepted
  07 Oct 2012