- Email: [email protected]
Meconium contamination of the neonatal middle ear
M e c o n i u m contamination of the neonatal middle ear Jorge Piza E., MD, Mario Gonzalez P., MD, Clarinda C. Northrop, BA, and Roland D. Eavey, MD From the Department of Pathology, Hospital Nacional de Nifios, Escuela de Medicina, Universidad d e Costa Rica, San Jos~, Costa Rica, and the Department of Otology and Laryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston The n e o n a t a ! middle ear and mastoid cavity are frequently c o n t a m i n a t e d by
cells a n d hair of the amniotic fluid. This a m n i o t i c fluid cellular content provokes a foreign b o d y inflammatory reaction that c a n persist for months. To e v a l u a t e w h e t h e r clinical and postmortem findings might correlate with the amount of a m n i o t i c fluid cellular content in the middle ear, we c o m p a r e d t e m p o r a l bones of nine patients born through m e c o n i u m - c o n t a m i n a t e d amniotic fluid with those of 40 patients born through clear amniotic fluid. All patients were e x a m i n e d at l e s s than 47 days postpartum and p r o v i d e d 37 temporal bones for histologic analysis. The volume of c o n t a m i n a n t was quantified for e a c h patient. The c a s e s w e r e arranged a c c o r d i n g to volume of c o n t a m i n a n t in the middle ear and c o m p a r e d with clinical information and autopsy findings. Patients with larger volumes of contaminant in the middle e a r w e r e born through thick, meconiumstained amniotic fluid (1.9-38 mm3; a v e r a g e 9.3 mm3). Conversely, patients with l e s s e r volumes of c o n t a m i n a n t in the middle e a r w e r e born through unstained amniotic fluid (none to 3.2 mma; a v e r a g e 0.9 mma). We speculate that patients b o r n t h r o u g h thick, meconium-stained amniotic fluid may be at g r e a t e r risk of s e q u e l a e such as otitis media from this foreign b o d y inflammatory reaction in t h e m i d d l e e a r and mastoid cavity. (J PEDIATR1989,145:910-4)
Previous histologic studies of neonatal temporal bones have demonstrated that most middle ear and mastoid cavities contain varying amounts Of amniotic fluid cellular content. 1-1l Depending on tile amount of such material, a foreign body inflammatory reaction Or even inflammatory polyps may be f0rmed,! 3 possibly predisposing the middle ear and mastoid to clinical otitis media. This theoretical predisposition has been suggested since early in this Century, 1! but proof is lacking. In clinical studies an association between neonatal otitis
Presented in part as a" poster at a meeting of the" Society for Pedi9 ..~2,,~ atrlc Pathology, Feb. 27, 1988, Washington, D.C. Submitted for publication April 7, 1989; accepted June 5, 1989. Reprint requests: Mario Gonzalez, MD, PO Box 1654-1000, Hospital Nacional de Nifios, San Jos~, Costa Rica.
9/20/14488
910
media and amniotic fluid has been suggested by Cioce and Canubi 12 and by Pestalozza. 13 Perinatal meconium aspiration and prolonged membrane rupture were correlated with a higher incidence of otitis media. Epidemiologic studies have stressed ttge high frequency of otitis media that starts during the first year of life. 1 4 ; 1 5 The earlier the first episode, the more likely that the infant is to be "otitis prone." 15 Contamination of the amniotic fluid with meconium presumably increases the concentration of desquamated epithelial cells. 16 Therefore more of these cells migh t be expected in the middle ear and mastoid cavities of neonates born .through meconium-stained amniotic fluid) In this study we wanted to determine whether clinical or autopsy findings, especially meconium-stainedananiotic fluid, might correlate with a more voluminous middle ear inocuium. A quantitative study of temporal bones of neonates born at 34 weeks of gestatio n or more was undertaken, and the amount of amniotic fluid cellular contents in the middle ear was compared with 35 clinical factors.
Volume 115 Number 6
M e c o n i u m contamination o f neonatal m i d d l e ear
METHODS
T a b l e . Volume of amniotic fluid cellular content in
Temporal bones have been collected for the past 10 years in the pathology department at the Hospital Nacional de Nifios, San Jos6, Costa Rica. Between 1984 and 1987 an effort was made to review neonatal cases of infants born at a minimum of 34 weeks of gestation with meconium staining of the amniotic fluid. (Meconium staining is unusual in fetuses at less than 34 weeks of gestation. 16-~9) Forty-two temporal bones without removal artifact, taken from 22 patients at birth to 16 days postpartum, who were at least 34 weeks of gestational age at birth, were available for study. All the temporal bones were fixed in 10% formaldehyde and processed with the routine celloidin method described by Schuknecht. 2~The blocks were cut at 20 ~zm in the horizontal plane, from the superior canal ampulla to the posterior canal ampulla; every tenth section was stained with hematoxylin and eosin, making approximately 40 slides per ear, 200 ~m apart. In each ear the volume of amniotic fluid cellular content and the volume of space of the middle ear and mastoid cavity were measured. Amniotic fluid cellular content was defined as desquamated keratinized and nonkeratinized epithelial cells and hair. Every third slide (600 #m apart) was projected at x 27.5 and drawn onto graph paper by use of a camera lucida type of image made with a Tri-Simplex projector (Bausch & Lomb Inc., Rochester, N.Y. ). We calculated the volume of the cellular content and of the middle ear and mastoid by computing the area for each of the 11 projected sections, averaging the areas, and then computing the distance between each section. Some infants had a larger volume of inoculum in one ear than in the other. Therefore, for standardization, the ear with the larger volume of cellular content in the middle ear was used for analysis in each case. In all cases, information about pregnancy, labor; and delivery was gathered from the mothers' charts. The clinical histories of the neonates were reviewed. The circumstances evaluated included maternal age, number of prior pregnancies, bleeding during pregnancy, hypertension or toxemia, maternal illness, maternal infection, bleeding during labor, type of presentation, vaginal or cesarean delivery, conduct of labor, placental detachment, dystocia, acute or chronic fetal distress, time of rupture of membranes, blood in the amniotic fluid, quantity of amniotic fluid, and presence of meconium-stained amniotic fluid. Meconium-stained amniotic fluid was defined as the presence of thick meconium, whether the staining was noted early or late during labor. Three cases (five temporal bones) were excluded from the study because the charts were unclear about the degree of meconium staining. Information about the neonate included gender, gestational age, weight classification by percentile, height, Apgar score at 1 and 5 minutes, tracheal
neonatal temporal bones
Patient No.
Cellular content of middle ear and mastoid cavity (mm 3)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
38/169 11/128 9/170 7/186 6/144 5.5/212 3.4/94 3.2/65 2.3/97 1.9/155 1.9/120 1.6/257 1.2/142 1.0/97 0.9/312 0.5/200 0.5/188 0.3/411 0.0/t3
911
Amniotic fluid Thickly stained
Unstained
X X
aspiration at birth, respiratory assistance, and postpartum age. There was no clinical information about the otoscopic appearance of the ear. A complete autopsy report was available for all but one patient, from whom only the temporal bones were removed for study. The autopsy protocols were reviewed to assess signs of neonatal hypoxia; facial, renal, digestive tract, or other congenital malformation; and acute or chronic intrauterine infection, as well as to determine the cause of death. Random microscopic slides of the lungs were placed in an unnumbered series and assessed for the presence of amniotic fluid cellular content by two pathologists working independently. The amount of this material in the lungs was graded according to the following classification: +, less than 10% of alveoli containing cellular material; + +, more than 10% of alveoli with cellular material but none in the bronchi or bronchioles; + + + , cellular material in bronchioles and small bronchi but not in the large bronchi; + + + + , cellular material in large bronchi. All chart information collected was compared with the volume of cellular material in the middle ear. Detailed results of the lung comparison and of the clinical and autopsy findings are available from the authors. RESULTS The 19 neonates were born in a hospital, and in 15 cases the mother had been under prenatal medical supervision.
912
Piza E. et al.
The Journal of Pediatrics December 1989
Fig. I. A, Right attic and antrum of ear of neonate born through thick, meconium-stained amniotic fluid. Case 1, four days postpartum. Amniotie fluid cellular content, visible as desquamated keratinized epithelial cells, fills 43% of middle ear and mastoid cavity at this level. M, Malleus; I, incus; MF, mesenchymal fold; arrows, amniotic fluid celluar content. B, Higher-power view of area (in box.)
Fig. 2. A, Left ear mesotympanum at level of stapes (S) of neonate born through thick, meconium-stained amniotic fluid. Case 7, one day postpartum. EAC, External auditory canal; M, malleus; L incus; arrow, amniotic fluid cellular content visible as desquamated keratinized epithelial cells. B, Higher-power view of amniotic fluid cellular content at arrow in A.
For nine neonates the amniotic fluid was noted to be thickly stained with meconium. In these~]3~tients the middle ear consistently had larger volumes of cellular content t h a n in patients whose amniotic fluid was Unstained (Table, Figs. 1 and 2). In the f o r m e r group the volume of cellular content in the middle ear ranged between 1 and 38 m m 3, with an average of 9.3 m m 3. In the ear containing the greatest vol-
ume, 23% of the middle ear space was occupied by cellular content (Fig. 1). In the 10 patients without m e c o n i u m contamination of the amniotic fluid, the volume of cellular content in the middle ear ranged from none to 3.2 m m 3, with an average of 0.9 m m 3. The cellular content in the lungs was also evaluated to compare it to with volume in the middle ear. In four of five
Volume 115 Number 6
fatal cases of meconium aspiration syndrome, there were relatively greater amounts of this material in both the middle ear and the lungs. (In the fifth case, lung autopsy data were not available.) O f the four infants in whom tracheal aspiration was attempted, two had less than 10% of cellular material in the lungs (+), one had more than 10% of cellular content in alveoli but not in bronchi ( + + ) , and one had cellular material in the large bronchi ( + + + + ) . In all nine patients who had thick, meconium-stained amniotic fluid, the middle ear contained relatively larger amounts of this material. For the remaining clinical and autopsy factors evaluated, there was no correlation with volume of cellular content in the middle ear. DISCUSSION In utero the middle ear and mastoid cavity of the fetus are in communication with the amniotic fluid via the eustachian tubes. The fetus begins to swallow by 20 weeks of gestation, 21 and the middle ear and mastoid cavities are created as the mesenchyme begins to resorb during the second trimester. 22 Thus amniotic fluid, with its cellular content, is swallowed and enters the middle ear, a normal phenomenon by the third trimester. Keratinized cells are present in the amniotic fluid from the beginning of the second trimester, and their concentration increases with maturation. 23 The presence of amniotic fluid and its cellular content in the middle ear of newborn infants has been observed in several studies. 111 Aschoff, 4 in 1896, studied random paraffin sections from 85 temporal bones of neonates and found cellular content in 36%. Notably, he found these cells in all 17 instances of meconium staining of the amniotic fluid. The amount of cellular content in amniotic fluid is assumed to be increased by meconium contamination. 16 Tracheal aspiration at the time of birth can assist with evacuation of this material from the lung, an organ in which the adverse effect of meconium is well known. 24, 25 Further harmful effect can occur from meconium spillage into the maternal peritoneal cavity during cesarean section. Such spillage has been thought to provoke granulomatous reactions and peritonitis. 26 Theoretically the ear also could be put at risk from contamination by meconium. Histologic examination of the amniotic fluid's cellular content measures the volume of material that has been inoculated into the ear and provides an indirect marker of possible biochemical irritation that can occur from meconium. Our study shows that there is more cellular content in the middle ear of newborn infants when the amniotic fluid is contaminated with meconium than when the amniotic fluid is clear. This pattern is maintained whether or not the trachea has been aspirated. Teele et al. 14 stressed the high frequency of otitis media in infants during the first year of life. Marchant et al. 15 also
Meconium contamination o f neonatal middle ear
91 3
showed that when the onset of middle ear effusion occurs at or before 2 months of age, the probability that a chronic effusion will develop is 33% versus 7% in patients with a first episode after that age. Furthermore, infants with bilateral middle ear effusions at 2 months accounted for 80% of the patients who had chronic otitis media with effusion in the first year. The presence of a foreign body inflammatory reaction in the middle ear might explain some of the cases of otitis in the neonatal period, as well as the development of chronic effusion. Technically, as an inflammation in the ear, this middle ear process represents "otitis media." The correlation between the amount of amniotic fluid cellular content in the middle ear and clinical and autopsy findings has not been described previously to our knowledge. From this study, which was limited to patients surviving 16 days or fewer from birth, there is no way of knowing what volume of inoculum might lead to middle ear disease. However, it is reasonable to speculate that the more cellular content in the middle ear and mastoid cavities, the greater will be the foreign body inflammatory reaction. Because patients born lhrough thick, meconium-stained amniotic fluid have a greater volume of cellular content in the middle ear, they may be at increased risk for subsequent otitis media. A quantitative study of this nature could not have been carried out without properly removed temporal bones in which the middle ear and antrum cavities were not opened at autopsy. We are grateful to Antonio Bonilla L. and Guido Rodriquez G. for removing temporal bones so carefully. We are also grateful to Prof. Benjamin Landing for his encouragement in this study and review of the manuscript. REFERENCES
1. deSa DJ. Polypoidol organization of aspirated amniotic squamous debris (amnion nodosum) in the middle ear cavity of newborn infants. Arch Dis Child 1977;52:148-51. 2. deSa DJ. Mucosal metaplasia and chronic inflammation in the middle ear of infants receiving intensive care in the neonatal period. Arch Dis Child 1983;58:24-8. 3. Northrop C, Piza J, Eavey RD. Histological observations of amniotic fluid cellular content in the ear of neonates and infants, lnt J Pediatr Otorhinolaryngol 1986;11:I 13-27. 4. Aschoff L. Die Otitis media neonatornm: Ein beitrag zur Entwicklungsgeschichte der Paukenhole. Z Ohrenh (Wiesbaden) 1897;31:295-346. 5. Benner MC. Congenital infection of the lungs, middle ears and nasal accessory sinuses. Arch Pathol 1940;29:455-72. 6. Bnch NH, Jorgenscn MB. Leukocytic infiltration in the middle ear of newborn infants. Arch Otolaryngol 1964:80:141-8. 7. deSa DJ. Infection and amniotic aspiration of middle ear in stillbirths and neonatal deaths. Arch Dis Child 1973;48:87280. 8. Hemsath FA. Intrauterine and neonatal otitis. Arch Otolaryngol 1936;23:78-92. 9. Johnson WW. A survey of middle ears: 101 autopsies of infants. Ann Otol Rhinol Laryngol 1961 ;70:377-402. 10. McLellan MS, Strong JP, Johnson QR, Dent JH, Otitis me-
9 14
11.
12. 13. 14. 15.
16. 17.
18.
19.
Piza E. et al.
dia in premature infants: a histopathologic study. J PEDIATR 1962;61:53-7. Wittmaach K. Uber die normale and die pathologische Pneumatisation des Schlafenbeines. Jeua, Germany: Gustav Fischer Verlag, 1918:24. Cioce C, Canubi A. L'otite del neonato. Ann Luring 1978; 76:571-6. Pestalozza G. Otitis media in newborn infants. Int J Pediatr Otorhinolaryngol 1984;8:109-24. Teele DW, Klein JO, Rosner B. Epidemiology of otitis media in children. Ann Otol Rhinol Laryngol t980;89(suppl 68):5-6. Marchant C, Shurlin PA, Tuczyk VA, Wasikowski DE, Tutihashi MA, Kenney SE. Course and outcome of otitis media in early infancy: a prospective study. J PED1ATR1984;104:826-31. Bacsik RD. Meconium aspiration syndrome. Pediatr Clin North Am 1977;24:463-79. Matthews TG, Warshaw JB. Relevance of the gestational age distribution of meconiurn passage in utero. Pediatrics 1979; 64:30-1. Gregory GA, Gooding CA, Phibbs RH, Tooley WH. Meconium aspiration in infants--a prospective study. J PEDIATR 1974;85:848-52. Ostrea ER, Naqvi M. The influence of gestational age on the
The Journal o f Pediatrics December 1989
20. 21.
22. 23.
24.
25. 26.
ability of the fetus to pass meconium in utero. Acta Obstet Gynecol Scand 1982;61:275-7. Schuknecht HF. Pathology of the ear. Cambridge, Mass: Harvard University Press, 197:3-10. Abramovich DR. The volume of amniotic fluid and its regulating factors. In: Fairweather DV1, Eskes TKAB, eds: Amniotic fluid--research and clinical applications, 2nd revised ed. Amsterdam: Excerpta Medica, 1978:36. Eggston AA, Wolff D. Histopathology of the ear, nose, and throat. Baltimore: Williams & Wilkins, 1947:115. Huisjes HJ. Cytology of the amniotic fluid and its clinical ap~ plications. In: Fairweather DVI, Eskes TKAB, eds. Amniotic fluid--research and clinical applications, 2nd revised ed. Amsterdam: Excerpta Medica, 1978:93. Carson BS, Losey RW, Bowes WA, Simmons MA. Combined obstetric and pediatric approach to prevent meconium aspiration syndrome. Am J Obstet Gyncol 1976;126:712. Ting P, Brady JP. Tracheal suction in meconium aspiration. Am J Obstet Gynecol 1975;122:767-71. Freedman SI, Ang EP, Herz MG, Stanley WD, Foot PJ. Meconium granulomas in post-caesarian section patients. Obstet Gynecot 1982;59:383-5.
cells a n d hair of the amniotic fluid. This a m n i o t i c fluid cellular content provokes a foreign b o d y inflammatory reaction that c a n persist for months. To e v a l u a t e w h e t h e r clinical and postmortem findings might correlate with the amount of a m n i o t i c fluid cellular content in the middle ear, we c o m p a r e d t e m p o r a l bones of nine patients born through m e c o n i u m - c o n t a m i n a t e d amniotic fluid with those of 40 patients born through clear amniotic fluid. All patients were e x a m i n e d at l e s s than 47 days postpartum and p r o v i d e d 37 temporal bones for histologic analysis. The volume of c o n t a m i n a n t was quantified for e a c h patient. The c a s e s w e r e arranged a c c o r d i n g to volume of c o n t a m i n a n t in the middle ear and c o m p a r e d with clinical information and autopsy findings. Patients with larger volumes of contaminant in the middle e a r w e r e born through thick, meconiumstained amniotic fluid (1.9-38 mm3; a v e r a g e 9.3 mm3). Conversely, patients with l e s s e r volumes of c o n t a m i n a n t in the middle e a r w e r e born through unstained amniotic fluid (none to 3.2 mma; a v e r a g e 0.9 mma). We speculate that patients b o r n t h r o u g h thick, meconium-stained amniotic fluid may be at g r e a t e r risk of s e q u e l a e such as otitis media from this foreign b o d y inflammatory reaction in t h e m i d d l e e a r and mastoid cavity. (J PEDIATR1989,145:910-4)
Previous histologic studies of neonatal temporal bones have demonstrated that most middle ear and mastoid cavities contain varying amounts Of amniotic fluid cellular content. 1-1l Depending on tile amount of such material, a foreign body inflammatory reaction Or even inflammatory polyps may be f0rmed,! 3 possibly predisposing the middle ear and mastoid to clinical otitis media. This theoretical predisposition has been suggested since early in this Century, 1! but proof is lacking. In clinical studies an association between neonatal otitis
Presented in part as a" poster at a meeting of the" Society for Pedi9 ..~2,,~ atrlc Pathology, Feb. 27, 1988, Washington, D.C. Submitted for publication April 7, 1989; accepted June 5, 1989. Reprint requests: Mario Gonzalez, MD, PO Box 1654-1000, Hospital Nacional de Nifios, San Jos~, Costa Rica.
9/20/14488
910
media and amniotic fluid has been suggested by Cioce and Canubi 12 and by Pestalozza. 13 Perinatal meconium aspiration and prolonged membrane rupture were correlated with a higher incidence of otitis media. Epidemiologic studies have stressed ttge high frequency of otitis media that starts during the first year of life. 1 4 ; 1 5 The earlier the first episode, the more likely that the infant is to be "otitis prone." 15 Contamination of the amniotic fluid with meconium presumably increases the concentration of desquamated epithelial cells. 16 Therefore more of these cells migh t be expected in the middle ear and mastoid cavities of neonates born .through meconium-stained amniotic fluid) In this study we wanted to determine whether clinical or autopsy findings, especially meconium-stainedananiotic fluid, might correlate with a more voluminous middle ear inocuium. A quantitative study of temporal bones of neonates born at 34 weeks of gestatio n or more was undertaken, and the amount of amniotic fluid cellular contents in the middle ear was compared with 35 clinical factors.
Volume 115 Number 6
M e c o n i u m contamination o f neonatal m i d d l e ear
METHODS
T a b l e . Volume of amniotic fluid cellular content in
Temporal bones have been collected for the past 10 years in the pathology department at the Hospital Nacional de Nifios, San Jos6, Costa Rica. Between 1984 and 1987 an effort was made to review neonatal cases of infants born at a minimum of 34 weeks of gestation with meconium staining of the amniotic fluid. (Meconium staining is unusual in fetuses at less than 34 weeks of gestation. 16-~9) Forty-two temporal bones without removal artifact, taken from 22 patients at birth to 16 days postpartum, who were at least 34 weeks of gestational age at birth, were available for study. All the temporal bones were fixed in 10% formaldehyde and processed with the routine celloidin method described by Schuknecht. 2~The blocks were cut at 20 ~zm in the horizontal plane, from the superior canal ampulla to the posterior canal ampulla; every tenth section was stained with hematoxylin and eosin, making approximately 40 slides per ear, 200 ~m apart. In each ear the volume of amniotic fluid cellular content and the volume of space of the middle ear and mastoid cavity were measured. Amniotic fluid cellular content was defined as desquamated keratinized and nonkeratinized epithelial cells and hair. Every third slide (600 #m apart) was projected at x 27.5 and drawn onto graph paper by use of a camera lucida type of image made with a Tri-Simplex projector (Bausch & Lomb Inc., Rochester, N.Y. ). We calculated the volume of the cellular content and of the middle ear and mastoid by computing the area for each of the 11 projected sections, averaging the areas, and then computing the distance between each section. Some infants had a larger volume of inoculum in one ear than in the other. Therefore, for standardization, the ear with the larger volume of cellular content in the middle ear was used for analysis in each case. In all cases, information about pregnancy, labor; and delivery was gathered from the mothers' charts. The clinical histories of the neonates were reviewed. The circumstances evaluated included maternal age, number of prior pregnancies, bleeding during pregnancy, hypertension or toxemia, maternal illness, maternal infection, bleeding during labor, type of presentation, vaginal or cesarean delivery, conduct of labor, placental detachment, dystocia, acute or chronic fetal distress, time of rupture of membranes, blood in the amniotic fluid, quantity of amniotic fluid, and presence of meconium-stained amniotic fluid. Meconium-stained amniotic fluid was defined as the presence of thick meconium, whether the staining was noted early or late during labor. Three cases (five temporal bones) were excluded from the study because the charts were unclear about the degree of meconium staining. Information about the neonate included gender, gestational age, weight classification by percentile, height, Apgar score at 1 and 5 minutes, tracheal
neonatal temporal bones
Patient No.
Cellular content of middle ear and mastoid cavity (mm 3)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
38/169 11/128 9/170 7/186 6/144 5.5/212 3.4/94 3.2/65 2.3/97 1.9/155 1.9/120 1.6/257 1.2/142 1.0/97 0.9/312 0.5/200 0.5/188 0.3/411 0.0/t3
911
Amniotic fluid Thickly stained
Unstained
X X
aspiration at birth, respiratory assistance, and postpartum age. There was no clinical information about the otoscopic appearance of the ear. A complete autopsy report was available for all but one patient, from whom only the temporal bones were removed for study. The autopsy protocols were reviewed to assess signs of neonatal hypoxia; facial, renal, digestive tract, or other congenital malformation; and acute or chronic intrauterine infection, as well as to determine the cause of death. Random microscopic slides of the lungs were placed in an unnumbered series and assessed for the presence of amniotic fluid cellular content by two pathologists working independently. The amount of this material in the lungs was graded according to the following classification: +, less than 10% of alveoli containing cellular material; + +, more than 10% of alveoli with cellular material but none in the bronchi or bronchioles; + + + , cellular material in bronchioles and small bronchi but not in the large bronchi; + + + + , cellular material in large bronchi. All chart information collected was compared with the volume of cellular material in the middle ear. Detailed results of the lung comparison and of the clinical and autopsy findings are available from the authors. RESULTS The 19 neonates were born in a hospital, and in 15 cases the mother had been under prenatal medical supervision.
912
Piza E. et al.
The Journal of Pediatrics December 1989
Fig. I. A, Right attic and antrum of ear of neonate born through thick, meconium-stained amniotic fluid. Case 1, four days postpartum. Amniotie fluid cellular content, visible as desquamated keratinized epithelial cells, fills 43% of middle ear and mastoid cavity at this level. M, Malleus; I, incus; MF, mesenchymal fold; arrows, amniotic fluid celluar content. B, Higher-power view of area (in box.)
Fig. 2. A, Left ear mesotympanum at level of stapes (S) of neonate born through thick, meconium-stained amniotic fluid. Case 7, one day postpartum. EAC, External auditory canal; M, malleus; L incus; arrow, amniotic fluid cellular content visible as desquamated keratinized epithelial cells. B, Higher-power view of amniotic fluid cellular content at arrow in A.
For nine neonates the amniotic fluid was noted to be thickly stained with meconium. In these~]3~tients the middle ear consistently had larger volumes of cellular content t h a n in patients whose amniotic fluid was Unstained (Table, Figs. 1 and 2). In the f o r m e r group the volume of cellular content in the middle ear ranged between 1 and 38 m m 3, with an average of 9.3 m m 3. In the ear containing the greatest vol-
ume, 23% of the middle ear space was occupied by cellular content (Fig. 1). In the 10 patients without m e c o n i u m contamination of the amniotic fluid, the volume of cellular content in the middle ear ranged from none to 3.2 m m 3, with an average of 0.9 m m 3. The cellular content in the lungs was also evaluated to compare it to with volume in the middle ear. In four of five
Volume 115 Number 6
fatal cases of meconium aspiration syndrome, there were relatively greater amounts of this material in both the middle ear and the lungs. (In the fifth case, lung autopsy data were not available.) O f the four infants in whom tracheal aspiration was attempted, two had less than 10% of cellular material in the lungs (+), one had more than 10% of cellular content in alveoli but not in bronchi ( + + ) , and one had cellular material in the large bronchi ( + + + + ) . In all nine patients who had thick, meconium-stained amniotic fluid, the middle ear contained relatively larger amounts of this material. For the remaining clinical and autopsy factors evaluated, there was no correlation with volume of cellular content in the middle ear. DISCUSSION In utero the middle ear and mastoid cavity of the fetus are in communication with the amniotic fluid via the eustachian tubes. The fetus begins to swallow by 20 weeks of gestation, 21 and the middle ear and mastoid cavities are created as the mesenchyme begins to resorb during the second trimester. 22 Thus amniotic fluid, with its cellular content, is swallowed and enters the middle ear, a normal phenomenon by the third trimester. Keratinized cells are present in the amniotic fluid from the beginning of the second trimester, and their concentration increases with maturation. 23 The presence of amniotic fluid and its cellular content in the middle ear of newborn infants has been observed in several studies. 111 Aschoff, 4 in 1896, studied random paraffin sections from 85 temporal bones of neonates and found cellular content in 36%. Notably, he found these cells in all 17 instances of meconium staining of the amniotic fluid. The amount of cellular content in amniotic fluid is assumed to be increased by meconium contamination. 16 Tracheal aspiration at the time of birth can assist with evacuation of this material from the lung, an organ in which the adverse effect of meconium is well known. 24, 25 Further harmful effect can occur from meconium spillage into the maternal peritoneal cavity during cesarean section. Such spillage has been thought to provoke granulomatous reactions and peritonitis. 26 Theoretically the ear also could be put at risk from contamination by meconium. Histologic examination of the amniotic fluid's cellular content measures the volume of material that has been inoculated into the ear and provides an indirect marker of possible biochemical irritation that can occur from meconium. Our study shows that there is more cellular content in the middle ear of newborn infants when the amniotic fluid is contaminated with meconium than when the amniotic fluid is clear. This pattern is maintained whether or not the trachea has been aspirated. Teele et al. 14 stressed the high frequency of otitis media in infants during the first year of life. Marchant et al. 15 also
Meconium contamination o f neonatal middle ear
91 3
showed that when the onset of middle ear effusion occurs at or before 2 months of age, the probability that a chronic effusion will develop is 33% versus 7% in patients with a first episode after that age. Furthermore, infants with bilateral middle ear effusions at 2 months accounted for 80% of the patients who had chronic otitis media with effusion in the first year. The presence of a foreign body inflammatory reaction in the middle ear might explain some of the cases of otitis in the neonatal period, as well as the development of chronic effusion. Technically, as an inflammation in the ear, this middle ear process represents "otitis media." The correlation between the amount of amniotic fluid cellular content in the middle ear and clinical and autopsy findings has not been described previously to our knowledge. From this study, which was limited to patients surviving 16 days or fewer from birth, there is no way of knowing what volume of inoculum might lead to middle ear disease. However, it is reasonable to speculate that the more cellular content in the middle ear and mastoid cavities, the greater will be the foreign body inflammatory reaction. Because patients born lhrough thick, meconium-stained amniotic fluid have a greater volume of cellular content in the middle ear, they may be at increased risk for subsequent otitis media. A quantitative study of this nature could not have been carried out without properly removed temporal bones in which the middle ear and antrum cavities were not opened at autopsy. We are grateful to Antonio Bonilla L. and Guido Rodriquez G. for removing temporal bones so carefully. We are also grateful to Prof. Benjamin Landing for his encouragement in this study and review of the manuscript. REFERENCES
1. deSa DJ. Polypoidol organization of aspirated amniotic squamous debris (amnion nodosum) in the middle ear cavity of newborn infants. Arch Dis Child 1977;52:148-51. 2. deSa DJ. Mucosal metaplasia and chronic inflammation in the middle ear of infants receiving intensive care in the neonatal period. Arch Dis Child 1983;58:24-8. 3. Northrop C, Piza J, Eavey RD. Histological observations of amniotic fluid cellular content in the ear of neonates and infants, lnt J Pediatr Otorhinolaryngol 1986;11:I 13-27. 4. Aschoff L. Die Otitis media neonatornm: Ein beitrag zur Entwicklungsgeschichte der Paukenhole. Z Ohrenh (Wiesbaden) 1897;31:295-346. 5. Benner MC. Congenital infection of the lungs, middle ears and nasal accessory sinuses. Arch Pathol 1940;29:455-72. 6. Bnch NH, Jorgenscn MB. Leukocytic infiltration in the middle ear of newborn infants. Arch Otolaryngol 1964:80:141-8. 7. deSa DJ. Infection and amniotic aspiration of middle ear in stillbirths and neonatal deaths. Arch Dis Child 1973;48:87280. 8. Hemsath FA. Intrauterine and neonatal otitis. Arch Otolaryngol 1936;23:78-92. 9. Johnson WW. A survey of middle ears: 101 autopsies of infants. Ann Otol Rhinol Laryngol 1961 ;70:377-402. 10. McLellan MS, Strong JP, Johnson QR, Dent JH, Otitis me-
9 14
11.
12. 13. 14. 15.
16. 17.
18.
19.
Piza E. et al.
dia in premature infants: a histopathologic study. J PEDIATR 1962;61:53-7. Wittmaach K. Uber die normale and die pathologische Pneumatisation des Schlafenbeines. Jeua, Germany: Gustav Fischer Verlag, 1918:24. Cioce C, Canubi A. L'otite del neonato. Ann Luring 1978; 76:571-6. Pestalozza G. Otitis media in newborn infants. Int J Pediatr Otorhinolaryngol 1984;8:109-24. Teele DW, Klein JO, Rosner B. Epidemiology of otitis media in children. Ann Otol Rhinol Laryngol t980;89(suppl 68):5-6. Marchant C, Shurlin PA, Tuczyk VA, Wasikowski DE, Tutihashi MA, Kenney SE. Course and outcome of otitis media in early infancy: a prospective study. J PED1ATR1984;104:826-31. Bacsik RD. Meconium aspiration syndrome. Pediatr Clin North Am 1977;24:463-79. Matthews TG, Warshaw JB. Relevance of the gestational age distribution of meconiurn passage in utero. Pediatrics 1979; 64:30-1. Gregory GA, Gooding CA, Phibbs RH, Tooley WH. Meconium aspiration in infants--a prospective study. J PEDIATR 1974;85:848-52. Ostrea ER, Naqvi M. The influence of gestational age on the
The Journal o f Pediatrics December 1989
20. 21.
22. 23.
24.
25. 26.
ability of the fetus to pass meconium in utero. Acta Obstet Gynecol Scand 1982;61:275-7. Schuknecht HF. Pathology of the ear. Cambridge, Mass: Harvard University Press, 197:3-10. Abramovich DR. The volume of amniotic fluid and its regulating factors. In: Fairweather DV1, Eskes TKAB, eds: Amniotic fluid--research and clinical applications, 2nd revised ed. Amsterdam: Excerpta Medica, 1978:36. Eggston AA, Wolff D. Histopathology of the ear, nose, and throat. Baltimore: Williams & Wilkins, 1947:115. Huisjes HJ. Cytology of the amniotic fluid and its clinical ap~ plications. In: Fairweather DVI, Eskes TKAB, eds. Amniotic fluid--research and clinical applications, 2nd revised ed. Amsterdam: Excerpta Medica, 1978:93. Carson BS, Losey RW, Bowes WA, Simmons MA. Combined obstetric and pediatric approach to prevent meconium aspiration syndrome. Am J Obstet Gyncol 1976;126:712. Ting P, Brady JP. Tracheal suction in meconium aspiration. Am J Obstet Gynecol 1975;122:767-71. Freedman SI, Ang EP, Herz MG, Stanley WD, Foot PJ. Meconium granulomas in post-caesarian section patients. Obstet Gynecot 1982;59:383-5.