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Pulmonary Neuroendocrine Cells in Hyaline Membrane Disease and Bronchopulmonary Dysplasia

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Pulmonary Neuroendocrine Cells in Hyaline Membrane Disease and Bronchopulmonary Dysplasia Pediatr. Res. 16: 446-454 (A82) Pulmonary Neuroendocrine Cells in Hyaline Membrane Disease and Bronchopulmonary Dysplasia DANA E. JOHNSON,'"' JAMES E. LOCK, ROBERT P. ELDE, THEODORE R. THOMPSON Departments of Pediatrics and Anatomy, University of Minnesota Medical School, Minneapolis, Minnesota, USA Summary munoreactivity (2). Bombesin, a 14 amino acid peptide, is a member of the continually expanding family of pep$des found in The number and distribution of bombesin immunoreactive pul- both the gut and the brain. This peptide is an active molecule monary neuroendocrine cells (PNEC) in fetuses and infants up to known to affect smooth muscle contraction of a number of organ 6 months of age was determined on postmortem lung specimens. systems, including the lung (3, 15, 34, 35). Individual cells and clusters of cells (neuroepithelial bodies) were The functional importance of these cells is undefined, but found in airways of all sizes, although greater than 95% of the preliminary evidence has suggested that PNEC may be chemore- positive cells were located in bronchioles, terminal bronchioles, ceptors contributing to the control of pulmonary vascular and/or and respiratory bronchioles. These infants were separated into airway tone in response to alterations in airway gas composition two groups. In control infants, who died primarily from noncardi- (20, 21, 24, 32). Despite their abundance in the neonatal lung, opulmonary causes, bombsin immunoreactive neuroendocrine cells little is known regarding the effect of acute and chronic neonatal were identified throughout the latter half of gestation. As gestation lung disease on these PNEC. The purpose of this study is to advanced, progressively more positive bronchioles/cm2 of lung describe the changes in the number of bombesin-immunoreactive tissue and cells/bronchiole were identified. In these control in- PNEC in two common neonatal pulmonary disorders where al- fants, the number of positive bronchioles/cm2 and cells/bronchiole terations in both pulmonary aeration and perfusion are known to were at the highest level at or near the time of delivery and then occur: hyaline membrane disease (HMD) and chronic broncho- gradually declined throughout the first 6 months of life. In contrast, pulmonary dysplasia (BPD). infants who died of acute hyaline membrane disease (1-7 days of life) or bronchiopulmonary dysplasia (2 wk to 6 months of life) demonstrated marked differences in the number of identifiable MATERIALS AND METHODS bombesin immunoreactive neuroendocrine cells when compared to Subjects. control infants. In early hyaline membrane disease, the number of Sixty-two hospitalized infants who died at the Univer- positive bronchioles/cm2 and cells/bronchiole was markedly de- sity of Minnesota Hospitals from 1956 through 1980 were used as creased. During the transition to chronic bronchopulmonary dys- the study population. Their ages at the time of death ranged from plasia, there appeared to be a marked increase in the number of birth to 6 months of age. Twenty-six of these infants had acute 26 bombesin immunoreactive cells. The peak number of cells occurred HMD or BPD (Table 1). These patients had required mechan- at 2-3 months of life, when substantially more bombesin-immu- ical ventilation and supplemental oxygen for most or all of their noreactive cells could be identified in children with bronchopul- lives. The diagnosis of both HMD and BPD were pathologically monary dysplasia than control infants of similar age. confirmed (29). Thirty-six fetuses and infants who died primarily from noncardiopulmonary causes were used as the control popu- lation (Table 26 and Ib). lthough a number of these infants had Speculation required short term mechanical ventilation before death, none This study demonstrates that a specific pulmonary cell type showed pathologic evidence of ventilator or oxygen toxicity to the containing bioactive molecules undergoes marked changes during lung. This study was approved by the Committee on the Use of acute and chronic neonatal lung disease. Anatomic and physiologic Human Subjects in Research at the University of Minnesota evidence suggests that these cells may be in an ideal position to Medical School. exert control on pulmonary vessel and airway tone either at the Tissue selection. Formalin-fixed, paraffin-embedded lung spec- local level or throughout the entire lung through vascular and imens were obtained from the University of Minnesota Hospitals neural connections. These data do not prove that alterations in Pathology file for each of the above infants. Autopsies had been this cell population are the cause of changes noted in airway and conducted in all cases within 24 h of death. An average of 2.07 in vascular resistance in infants with lung disease. They do identify, + 0.75 (S.D.) randomly chosen tissue blocks were examined per however, a new area of potential investigation in these disease patient. The precise region of the lung from which tissue was states. taken was known for only a minority of specimens. Six patients had only one tissue block available for study. Zmrnunohistochemistry. The localization of bombesin imuno- A distinct population of granulated cells posessing both endo- reactivity was accomplished on 5 p tissue sections using the crine and neural characteristics has been recognized in the respi- unlabeled antibody-peroxidase-antiperoxidase technique of Stern- ratory epithelium for over thirty years (8, 10). These pulmonary berger, et al. (3 1) Rabbit antibombesin (Immunonuclear Corp., neuroendocrine cells (PNEC) are identified in greatest numbers Stillwater, MN), raised in response to a synthetic amphibian during the neonatal period (19, 24) and are situated near both bombesin, was used at a dilution of 1:200 in phosphate buffered pulmonary vessels and nerves (8, 10, 20, 23, 28). saline (PBS) (pH 7.2) with 0.5% Triton X-100 (Research Products Recent work has demonstrated that the secretory granules of International, Elk Grove Village, IL). Sections mounted on gelatin these cells contain biologically active molecules such as serotonin coated slides were incubated overnight at 3O with the primary (Is), as well as peptides with bombesin (36) and calcitonin im- antiserum. Sections were then incubated sequentially for 1 h at PULMONARY NEUROENDOCRINE CELLS 447 Table 1. Clinical data on infants with respiratory distress syndrome tion of individual cells was difficult, only nucleated immunoreac- and bronchopulmonary dysplasia tive cells were ennumerated. Differentiation between hyperplasia of individual PNEC and hyperplasia of cells within NEB was Mechani- Age at Oxygen extremely difficult using these techniques and was not attempted. Birth Gestational age cal death weight requirements Two measurements were made from each slide: (1) the total ventilation number of airways in any plane of section (cross, longitudinal, or 30 wk 1 day I day tangenital) (Fig. 6 and 7) exhibiting bombesin-immunoreactive I day 27 wk I day 1 day cells (expressed as airways/cm2), and (2) the total number of 36 wk I day 1 day Table 2a. Control term infants-clinical data (Age at Death I day- 32 wk 3 days 3 days 6 months) 3 days 34 wk 3 days 3 days 36 wk' 3 days 3 days Age at death Diagnosis Mesoblastic nephroma 28 wk 7 days 7 days I day Massive hemolysis (? etiology) 7 days 32 wk 7 days 7 days Massive hemolsis (G-6-PD deficiency) 31 wk 7 days 7 days Myelodysplasia-gram negative sepsis 30 wk 2 wk 2 wk 3 days Renal vein thrombosis 2 wk 40 wk2 2 wk 2 wk Birth asphyxia 30 wk 2 wk 2 wk Intestinal perforation-gram negative sepsis 32 wk 3 wk 3 wk 7 days Omphalocele-gram negative meningitis 3 wk 30 wk 3 wk 3 wk Myelodysplasia-gram-negative sepsis 35 wk 3 wk 3 wk E. coli Septicemia 29 wk 2 months 2 months 2 wk Myelodysplasia-gram negative sepsis 2 months 32 wk 2 months 2 months No pathologic diagnosis (? SIDS) 23 wk 5 wk3 2 months Myelodysplasia-gram negative meningitis 34 wk 3 months 3 months 3 wk Hyperammonemia syndrome 3 months 32 wk 3 months 3 months Cerebral trauma 32 wk 3 months 3 months Peritonitis-gram negative sepsis 32 wk Last 6 wk Last 6 wk 2 months Sudden infant death syndrome (SIDS) 4 months 36 wk 3 wk 4 months Cerebral trauma 30 wk 6 wk 4 months H. Injluenzae meningitis 30 wk 6 months 6 months 3 months 6 months Reye's syndrome 32 wk 3 months 6 months ' Infant of diabetic mother. Meningiococcemia Meconium aspiration syndrome. 4 months Lactic acidosis (? inborn error of metabolism) Nasal CPAP until death. Myelodysplasia, recurrent seizures E. coli sepsis room temperature with sheep anti-rabbit IgG (Cappel Laborato- 5 months Acute subdural hematoma ries, Cochranville, PA) diluted 1:200 in borate buffered saline (pH 8.5) with 1% normal sheep serum (NSS) (Antibodies, Inc., D&, S. Pneumoniae meningitis CA) and rabbit peroxidase-antiperoxidase (PAP) (Cappel Labo- 6 months H. Influenzae meningitis ratories, diluted 1:500 in BBS with 1% NSS). Peritonitis-gram negative sepsis The specificity of bombesin localization was tested by incubat- ing varying concentrations of peptides with the primary immune sera for 1 h at room temperature before its application to tissue sections. Localization of bornbesin-immunoreactive cells in the Table 26. Controlpreterm infants-clinical data (age at death <I2 lung was prevented by 0.1 pg of bombesin per ml diluted antisera hl (1:200). The addition of 50 pg of litorin, eledoisin, substance P, Gestational Birth weight Time of death somatostatin, neurotensin or met-enkephalin did not prevent the age (wk) (8) (diagnosis) staining of bombesin-immunoreactive cells in the bronchiolar Second trimester 19 200 Stillborn epithelium. All peptides for absorption controls were obtained 23 477 1 h (Respiratory in- from Penninsula Laboratories, San Carlos, CA. No immunoreac- tive cells were demonstrated when nonimmune rabbit sera was sufficiency) substituted for the primary antibody or when BBS was substituted 25 590 9 h (Respiratory in- for sheep anti-rabbit IgG or rabbit PAP.
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