fluid may be seen as abnormally large amounts of fluid in the interlobar fissures, or Kerley A and B
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1 Archives of Disease in Childhood, 1982, 57, Delayed clearance of pulmonary fluid in the neonate S RIMMER AND J FAWCITT Departments of Radiology, St Mary's Hospital, Manchester and North Manchester General Hospital SUMMARY A consecutive series of 647 routine neonatal chest x-ray films taken at a known time within 48 hours of birth was reviewed; 48 % had been radiographed within 2 hours. Four hundred and twenty-seven had normal x-ray films, 147 showed evidence of delayed clearance of pulmonary fluid, and other diseases were present in 73. Excessive amounts of pulmonary fluid were not rare in neonates radiographed within 2 hours and were not necessarily associated with symptoms. Low birthweight and prematurity predisposed to delayed clearance of pulmonary fluid; with birthweights greater than 2 3 kg excess of pulmonary fluid was unlikely. Persistence of pleural fluid was more common in the right than the left lung. While radiologically there was no difference in the sex incidence of delayed clearance, symptoms were more common in boys. At birth the unventilated lung is not totally collapsed because the alveoli are partially distended with fluid.1 The volume of this fluid is about equivalent to the functional residual capacity, representing ml/kg of body weight. In the normal term fetus the lungs contain about ml of fluid.2 This fluid appears to be actively produced or modified by the lung as it differs both in total osmolarity and in its protein, urea, and bicarbonate concentrations compared with amniotic fluid.' It is said to be an ultrafiltrate of the plasma.3 Fawcitt et al.4 showed that aeration of the lungs was almost instantaneous in normally delivered infants. Therefore, the removal of fluid must be rapid. There are three main mechanisms of removal. Up to 20 ml of fluid is expressed through the nose and mouth as the thorax is squeezed while the fetus passes down the birth canal during a normal vertex delivery.5 f Fluid passes into the interstitial tissues and from there into the pulmonary lymphatics6 7 which are larger and more numerous in the fetal and newborn lung than in the adult.8 At the onset of ventilation there is a considerable increase in pulmonary lymph flow which in the mature fetal lamb increases at least 3-fold and drains 40% of the lung liquid within the first 2 hours of ventilation9 although removal is slower in the immature lung.' This Fig. 1 (Taken SO minutes after birth.) Shows interstitial fluid is also drawn into the pulmonary capillaries because of their higher osmotic pressure.' The radiological features of excessive amounts of pulmonary fluid have been described by Avery et al.,10 Kuhn et al.,1" Swischuck,12 and Wesenberg et al.'3 Increased pulmonary vascular markings are less sharply defined than normal, with haziness of the 63 hila and engorged vessels extending to the periphery of the lung fields. (In the normal neonatal chest sharply defined vessel markings are confined to the medial two-thirds.) Excessive amounts of interstitial fluid may be seen as abnormally large amounts of fluid in the interlobar fissures, or Kerley A and B intra-alveolar fluid and diffiuse opacities in both lungs; these are less pronounced at the periphery. An air bronchogram could be seen in the left upper lobe. More peripherally, congested vessels could be seen together with a Kerley B line at the right base and a trace of pleuralfluid. Thereafter films taken at 2-hourly intervals showed progressive improvement. At 3 hours the intra-alveolar fluid was no longfer visible
2 64 Riminer and Fawcitt ties that tend to coalesce and which may be associated with air bronchograms. Some of these features are shown in Figs I and 2. Clinical materials and methods Between 1956 and 1958 the radiographs of a consecutive series of 795 neonates admitted to the premature baby unit of Crumpsall Hospital, Manchester were collected. These are currently reviewed as they form a unique series of films, taken irrespective of the presence of abnormal clinical signs at a known time after birth. Of the 647 cases radiographed within 48 hours, 48 % had abnormal clinical signs within 2 hours of birth. Details of the Fig. 2 (Taken 30 minutes after birth.) A preterm but otherwise normal girl born at 37 weeks' gestation with no clinical evidence of respiratory distress. Excessive amounts ofpulmonary fluid are present with congested vessels extending up to the periphery of the lung fields. Kerley B lines are present at both bases; there is a Kerley A line in the right upper zone. in addition, there is an excessive amount offluid in the horizontal fissure. A small amount ofpleural fluid could be seen along the lower one-third of the righlt lateral chest wall. A further chest x-ray film taken at 27 hours was normal. lines may be present. Small amounts of pleural fluid may be seen in either the costophrenic angle or as a lamellar effusion situated along the lower lateral chest wall. There is generalised hyperinflation and mild cardiomegaly. In addition, if neonates have x-ray films taken early before all the pulmonary fluid has been displaced into the interstitial spaces, intra-alveolar fluid produces fluffy ill-defined densi- Table 1 Principal clinicalfeatures present at time of initial chest x-ray Cases (n =647) % Birthweight >2500 g <2500 g No abnormal signs Birth asphyxia 54 8 Tachypnoea Cyanosis and tachypnoea Apnoeic attacks Congenital heart defect Hypothermia 15 2 Cerebral damage 21 3 Unrelated abnormality Table 2 x-rayed before 48 hours of age Distribution of radiological findings in infants Radiological findings No of infants (n = 647) Normal radiographs 427 Excess pulmonary fluid 147 Other lesions 73 In 180 M Normal =Retained pulmonary fluid 140 u 100 -Io- Fig. 3 Distribution ofpatients with fl60 0 retained pulmonary fluid up to 48 hours. n0 60 E I 20 J Time ( hours)
3 maturity, birthweight, clinical condition at birth, subsequent course, and if applicable, necropsy results, were available. Table 1 records the major clinical features present on admission at the time of the initial chest x-ray film. 30 a U a Fig Bilateral Right Left Distribution ofpleural fluid. o 0 Normal A -. Retained pulmonary fluid tn20 u~~~~~~~~~~~~~ E lo u' 0_../..;0,..0 0 A' Weight (g) Fig. 5 Distribution of cases according to weight. 40 o - o Normal 30 * * Retained pulmonary fluid Delayed clearance ofpulmonary fluid in the neonate 65 Results Table 2 shows the distribution of abnormalities in the neonates radiographed before 48 hours of age; excess pulmonary fluid was present in 147 cases and was more common than any other abnormality. Fig. 3 demonstrates the diminution in the number of patients with evidence of retained pulmonary fluid with increasing time after birth. Of a total of 147 patients with excess pulmonary fluid, only 27 had excess fluid after 2 hours. Analysis of the distribution of pleural fluid (Fig. 4) showed bilateral pleural fluid in 26 patients; 44 patients had pleural fluid on the right and 14 had pleural fluid on the left. This increased incidence of pleural fluid on the right was statistically significant at the 1 % level using the x2 test (P<0 01). Fluid seen in the horizontal fissure was excluded as this would have produced a bias towards the right side. Fig. 5 demonstrates the effects of birthweight on clearance of fluid. There were no neonates between 600 mg and 1 kg with normal chest radiographs, but 5 showed excess pulmonary fluid. At the upper end of the scale there were 14 neonates with birthweights greater than 2.3 kg with excess pulmonary fluid compared with 43 with normal chest radiographs, thus suggesting that low birthweight predisposes to delayed clearance. Similarly, Fig. 6 shows the relationship between maturity and excess pulmonary fluid. There were no normal chest radiographs before 29 weeks and an excess of abnormal x-ray films up to 31 weeks. The incidence of delayed clearance had fallen considerably by term. As transient respiratory distress of the newborn appears to be more common in boys we looked at the sex distribution of the group. Of 147 neonates in whom excess pulmonary fluid was present, the gender was known for 118. Fig. 7 shows the number of patients plotted against time. It is apparent that 20 o A"'j\is \. Fig. 6 Distribution of cases according to E,' / *\', a maturity. 10~~~~~~~~~~ 0..A Ȧ,A A Maturity (weeks)
4 66 Rimmer and Fawcitt 80 Boys Boys o Retained pulmonary fluid o o Total A A Girls ATotal 60 \A Girls. A Retained pulmonary fluid Ci) U L0 E < > < Fig. 7 Distribution of boys and girls. E 20 A\ \ Z ~~~ A~ A %% A--A -A Time (hours) the total distribution of boys and girls was similar; the distribution of boys and girls who retained pulmonary fluid was also similar, although there were fewer girls in each group. There was no statistically significant difference between the relative distribution of the two genders. In order to attempt to explain the sex difference in transient respiratory distress of the newborn, we looked for the presence of symptoms, and found that out of a total of 69 boys, 35 (52 %) were symptomatic and out of a total of 49 girls, 13 (33-3%) were symptomatic. These findings were statistically significant at the 5 % level using the x2 test (P <0 05). Discussion Avery et al.10 described a series of 8 cases of neonatal respiratory distress which did not follow the typical pattern of the idiopathic respiratory distress syndrome and which she ascribed to delayed clearance of this pulmonary fluid and called transient tachypnoea of the newborn. The condition has also been called transient respiratory distress of the newborn,12 wet lung disease,'3 neonatal disseminated atelectasis,14 respiratory distress syndrome type 11,15 and diffuse primary alveolar atelectasis.'6 The condition presents by the age of 4 hours with symptoms similar to those of idiopathic respiratory distress syndrome, but they are generally less severe and usually resolve within 48 hours. Avery et al.10 reported that minimal cyanosis might be present but that alveolar ventilation was normal as measured by blood ph and Pco2 although Sundell et al.'5 described the presence of mild hypercarbia, hypoxia, and acidosis at 2-6 hours. The excessive amounts of pulmonary fluid are thought to result in splinting of the lung with reduced pulmonary compliance and therefore normal inflation and deflation is hindered producing respiratory distress, pulmonary congestion, and generalised overaeration. Causes of delayed clearance which have been postulated are hypoproteinaemia'3 17 and hypervolaemia due to excessive milking of the cord.'8 Although the condition was originally described as affecting mainly term infants, this series together with that of Wesenberg et al.13 demonstrate a higher incidence in the preterm neonate. The incidence of retained pulmonary fluid found in this series is high, but these neonates had been admitted to the premature baby unit. This higher incidence might have been expected since experiments on animals have shown decreased pulmonary lymph flow in the premature,7 and preterm neonates are also hypoproteinaemic compared with term ones.19 The radiographic features of intra-alveolar or interstitial fluid tend to be particularly pronounced in the right lung, and in keeping with this is our observation that there is a statistically significant increased incidence of pleural fluid on the right. According to reports transient respiratory distress of the newborn is more common in the male. This series shows that although the radiological features of the condition are present in an equal proportion of boys and girls, they are associated with symptoms in a significantly greater number of males. References Strang L B. Uptake of liquid from the lungs at the start of breathing. In: de Reuk A V S, Porter R, eds. Development of the lung. Edinburgh: Churchill, 1967: Karlberg P. The adaptive changes in the immediate post-natal period, with particular reference to respiration. J Pediatr 1960; 56: Adams F H, Fujiwara T, Rowshan G. The nature and origin of the fluid in the fetal lamb lung. J Pediatr 1963; 63: Fawcitt J, Lind J, Wegelius C. The first breath: a preliminary communication describing some methods of investigation of the first breath of a baby and the results obtained from them. Acta Paediatr Scand [Suppl] 1960; 49: Supplement 123, 5-17.
5 Delayed clearance ofpulmonary fluid in the neonate 67 5 Karlberg P, Adams F H, Geubelle F, Wallgren G. Alteration of the infant's thorax during vaginal delivery. Physiological studies. Acta Obstet Gynecol Scand 1962; 41: Aherne W, Dawkins M J R. The removal of the fluid from the pulmonary airways after birth in the rabbit and the effect on this of prematurity and prenatal hypoxia. Biol Neonate 1964; 7: Boston R W, Humphreys P W, Reynolds E 0 R, Strang L B. Lymph-flow and clearance of liquid from the lungs of the foetal lamb. Lancet 1965; ii: Davis J, Dobbing J. Scientific foundations of paediatrics. London: Heinemann, 1974: Humphreys P W, Normand I C S, Reynolds E 0 R, Strang L B. Pulmonary lymph flow and the uptake of liquid from the lungs of the lamb at the start of breathing. J Physiol 1967; 193: Avery M E, Gatewood 0 B, Brumley G. Transient tachypnea of newborn. Possible delayed resorption of fluid at birth. Am J Dis Child 1966; 111: Kuhn J P, Fletcher B D, De Lemos R A. Roentgen findings in transient tachypnea of the newborn. Radiology 1969; 92: Swischuck L E. Transient respiratory distress of the newborn (TRDN): a temporary disturbance of a normal phenomenon. AJR 1970; 108: Wesenberg R L, Graven S N, McCabe E B. Radiological findings in wet lung disease. Radiology 1971; 98: Kottler R E, Malan A F, Heese H de V. Respiratory distress syndrome in the newborn. S Afr J Radiol 1964; 2: Sundell H, Garrott J, Blankenship W J, Shepard F M, Stahlman M T. Studies on infants with type 11 respiratory distress syndrome. J Pediatr 1971; 78: Fawcitt J. Radiological findings in the lungs of premature infants. Arch Dis Child 1956; 31: Steele R W, Copeland G A. Delayed resorption of pulmonary alveolar fluid in the neonate. Radiology 1972; 103: Burnard E D, James L S. Atrial pressures and cardiac size in the newborn infant. Relationships with degree of asphyxia and size of placental transfusion. J Pediatr 1963; 62: Hardie G, Kench J S. Anti-IgG agglutinins in idiopathic respiratory distress syndrome of the newborn. Atch Dis Child 1969; 44: Correspondence to Dr S Rimmer, Department of Diagnostic Radiology, University of Manchester, Stopford Building, Oxford Road, Manchester M13 9PT. Received 9 February 1981
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