Auditory brain stem dilatation - BMJ

Archives of Disease in Childhood, 1989, 64, 17-23

Auditory brain stem responses in infants withposthaemorrhagic ventricular dilatationS LARY, L S DE VRIES, A KAISER, L M S DUBOWITZ, AND V DUBOWITZ

Department of Paediatrics and Neonatal Medicine, Hammersmith Hospital, London

SUMMARY Nineteen infants with posthaemorrhagic ventricular dilatation had auditory brainstem responses measured during the period of maximal ventricular dilatation. These showedvarious patterns ranging from normal, through various abnormalities, to complete absence ofresponses. When serial auditory brain stem responses were studied in parallel with the evolutionof posthaemorrhagic ventricular dilatation it was seen that the abnormalities of auditory brainstem response usually resolved irrespective of the persistence or progression of ventriculardilatation. No correlation was found between cerebrospinal fluid pressure and prolongedinterpeak intervals on the auditory brain stem response. In three patients with posthaemorrhagicventricular dilatation improvement in the auditory brain stem response occurred whencerebrospinal fluid was withdrawn. Intermittent withdrawal of cerebrospinal fluid (by ventriculartap or lumbar puncture) in two of these infants was followed by improvement in the auditorybrain stem response after a period of 24 hours (but not sooner). In one infant born at full termimprovement in the auditory brain stem response was noted one week after shunting.

Disturbances in auditory brainstem responses havebeen reported in disorders associated with ventricu-lar dilatation in both infants and children,1-3 and theuse of the auditory brain stem response to assess thepossible impact of ventricular dilatation on thebrainstem has been described.14The aim of the present study was to evaluate the

auditory brain stem response abnormalities in in-fants with posthaemorrhagic ventricular dilatationand to determine whether such abnormalities couldbe altered by drainage of cerebrospinal fluid.

Patients and methods

Of the 855 infants admitted to the HammersmithHospital neonatal intensive care unit between Octo-ber 1981 and April 1984, 145 had periventricularhaemorrhage diagnosed on ultrasound scanningduring the first week of life; 18 of these (12%)developed posthaemorrhagic ventricular dilatation.Two further infants who were transferred to the unitwith established posthaemorrhagic ventriculardilatation at the ages of 2 and 8 weeks, respectivelywere included in the study. Of these 20 infants, 19were fit for testing. The remaining infant wascritically ill and considered unsuitable for assess-ment of auditory brain stem response; he subse-quently died.

17

The diagnosis of posthaemorrhagic ventriculardilatation was made when two or more measure-ments of ventricular width on ultrasonographyexceeded by at least 4 mm the 97th centile of themeasurements appropriate for the gestational agedetermined by Levene.5Of the 19 infants with posthaemorrhagic ventricu-

lar dilatation, 16 were preterm (gestational ages26-34 weeks) and three had been born at full term(38-39 weeks). Gestational ages were calculatedfrom gestational assessment6 and the dates of themother's last menstrual period, which agreed withinone week in all cases.The recordings of auditory brain stem response

were usually made while the infant was lying pronewith one ear on the mattress. An earphone was heldgently over the other ear taking care not to occludeor collapse the external auditory canal, which mayresult in appearances simulating a conductive lesion.Rarefaction clicks, 100 ,us square waves, at a rate of10/s were made into one ear through a TDH-39earphone. Each response was calculated from a totalof 1024 to 2048 stimuli. Two machines were used;the first a Medelec MS6 model using a bandpassfilter of 250-1600 Hz, the second a Medelec Sensormachine using a filter of 300-3000 Hz. Threestandard electrodes were used, the active electrodewas placed over the vertex (Ml), and the reference

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18 Lary, De Vries, Kaiser, Dubowitz, and Dubowitz

electrode over the mastoid process ipsilateral to thestimulated ear. The contralateral mastoid processwas used for the ground electrode (M2). A fourthelectrode was sometimes applied to the foreheadand used for grounding while M2 was recording thecontralateral ear in a second channel. Due tolimitation of time and availability of the babies, andto avoid excessive handling, we found it moreconvenient to use three electrodes most of the time.Contact impedances were generally of the order of1000 to 2000 ohms, but on rare occasions were ashigh as 6000 ohms.

Intensities of 80 and 60 dB were routinely used.These intensities were altered as needed for particu-lar subjects and circumstances, and according to theresponses obtained. If the responses were poor, in-tensities were increased by increments of 10 dB. If theresponses were good with well identified wave com-ponents the stimulus was decreased to 40 dB. Allrecordings were repeated to check for consistency.Normal control data for each machine and setting

were derived from two previous studies carried outin this unit.7 8The cerebrospinal fluid pressure in nine of the 19

infants was also studied.9 In six infants this was donewithin two of hours of their auditory brain stemresponses having been measured. The pressureswere recorded by direct measurement during lum-bar or ventricular taps with a Gaeltic pressuretransducer attached to the needle in the ventricularof subarachnoid space. The upper limit of normalcerebrospinal fluid pressure was taken as 0*8 kPa(6 mm Hg).The four aspects studied were: the evolution of

the abnormalities in auditory brain stem responsein relation to the occurrence of periventricularhaemorrhage and intraventricular haemorrhage andto the development and resolution of the ventriculardilatation (n=12); the assessment of the auditorybrain stem responses at the time of maximumventricular dilatation (n=19); the general associa-tion between abnormalities in auditory brain stemresponse and cerebrospinal fluid pressure (n=9);and the changes in auditory brain stem response inresponse to withdrawal of cerebrospinal fluid byeither shunting, or periodic drainage by lumbarpuncture or ventricular tapping (n=7).

Results

EFFECTS OF THE EVOLUTION OF POSTHAEMORRHAGICVENTRICULAR DILATATION ON THE AUDITORY BRAINSTEM RESPONSEEleven preterm infants and one born at full termwere studied. In the preterm infants periventricularhaemorrhage or intraventricular haemorrhage of

variable severity were diagnosed during the firstweek of life. During the same time auditory brainstem responses were recorded and were abnormal inall 11 infants. The haemorrhages and sequentialauditory brain stem responses were measured andshowed improvement at a time when the ventriculardilatation was still present on the scans, or evenincreasing in size. In five of the 11 preterm infantsthe auditory brain stem responses returned tonormal although there was still pronounced dilata-tion of the ventricles. Fig 1 gives an example of thesefive infants. In three the auditory brain stemresponses remained abnormal at the ages of 10, 14,and 20 weeks, respectively. Though the ventriclesdecreased in size during this period, they stillremained moderately dilated.

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Fig 1 An infant born at32 weeks' gestation developedbilateral intraventricular and periventricular haemorrhageson day 3. Auditory brain stem responses on day 4 wereabnormal (latencies, intervals, and waveforms) at 90 dB oneach side. By the second week the auditory brain stemresponse showedpronounced improvement on waveformsbut the I-V interval remained prolonged. Ventriculardilatation and cystformation were now present on ultra-sonography. By day 19, the auditory brain stem responsehad reverted to normal, but there had been further dilatationon ultra sonography. Click stimuli used in all traces at 101s(rarefaction phase).



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Auditory brain stem responses in infants with posthaemorrhagic ventricular dilatation 19

In one infant the auditory brain stem responseremained abnormal and the child was referred tohearing specialists. Two infants died at the ages of 2and 4 weeks, respectively.A single infant born at full term with posthaemor-

rhagic ventricular dilatation was also studied andshowed an initially normal auditory brain stemresponse. Ventricular dilatation increased progres-sively over the next 10 weeks. A repeat recordingearly in this period remained normal. Subsequentauditory brain stem responses measured at the ageof 3 months showed deterioration.

EFFECTS OF POSTHAEMORRHAGIC VENTRICULARDILATATION ON THE AUDITORY BRAIN STEM RESPONSEAT TIME OF MAXIMUM VENTRICULAR DILATATIONAuditory brain stem responses were measured in 19infants during the phase of maximum dilatation ofthe ventricles. Five records were normal and 14were abnormal. The abnormal tracings showedvarious patterns. Two infants had 'severe' impair-ment: absent responses in one, and appreciablyreduced wave amplitude in the other (figs 2a and b,respectively). Two infants had 'peripheral' abnor-malities including absent wave amplitude or wave 1more than two standard deviations from the mean(fig 2c). Five infants had 'central' abnormalities.Three showed prolonged I-V interpeak intervals(more than two standard deviations from the mean),one with an absent wave V, and one with anabnormal V:I amplitude ratio (figs 2d and e). Twoinfants had short I-V interpeak intervals but normalwave configuration. Three infants had abnormal andnon-reproducible traces on repeated testing. Thesewere classified separately.

EFFECTS OF CEREBROSPINAL FLUID PRESSURE ON THEAUDITORY BRAIN STEM RESPONSENine infants had serial cerebrospinal fluid pressuresand auditory brain stem responses recorded, six ofwhom had the auditory brain stem responses re-corded on the same day and within a few hours ofrecording the cerebrospinal fluid pressures. In thesesix infants therefore (five preterm and one born atfull term) a total of 21 direct cerebrospinal fluidpressure measurements were coffelated with theauditory brain stem response measurements thatwere recorded simultaneously. There was no cor-relation between the cerebrospinal fluid pressureand the presence of auditory brain stem responseabnormalities as assessed by the I-V interpeakinterval (fig 3).

EFFECTS OF CEREBROSPINAL FLUID DRAINAGE ON THEAUDITORY BRAIN STEM RESPONSEIn seven infants the auditory brain stem responses

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Fig 2 Auditory brain stem response recordings showingvarious types ofabnormalities. (a) Absent responses at80 dB. (b) Severely reduced response at intensity: 80 dB.(c) Absent wave 1. (d) Prolonged interpeak intervalsbetween waves I-V in an infant, postmenstrual age 34 weeks;interpeak interval is 6-2 ms-that is, more than two SDfrommean. (e) Poor wave V with abnormal V:1 ratio. Clickstimuli used in all traces at a rate 101s and the intensities usedin traces c-e were 60 dB.

were studied before and after drainage of cerebro-spinal fluid. In all seven the auditory brain stemresponses were abnormal before the drainage wascarried out. Repeat measurement of auditory brainstem responses after two to six hours showed littlechange, but auditory brain stem responses measured24 hours after drainage showed an increase inamplitude in two of the four cases where this wastested (fig 4).Four infants had shunts inserted. Auditory brain

stem responses measured before the shunts wereinserted were normal in one, unequivocally abnor-mal in another, and showed a pattern of uncertainimportance in the remaining two, with normal wave

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Fig 3 Simultaneous cerebrospinal fluidpressures andinterpeak intervals I-V recorded on 12 occasionsfromfivepreterm infants (black circles), and on nine occasionsfromone infant born atfull term (white circles). The upper limitofnormal cerebrospinal fluid pressure is shown by thehorizontal line.

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morphology and hearing thresholds, but interpeakintervals shorter than were appropriate for theirages. The shunting procedure had no effect on theauditory brain stem response in one patient in whomthe auditory brain stem response was normal beforeshunting or in two patients who had abnormalities inthe auditory brain stem response of uncertainimportance. In the one infant born at full term,however, the abnormal auditory brain stem re-sponse recorded before the shunt reverted to normalwithin a week of the shunt being inserted (fig 5).Discussion

Previously reported abnormalities in auditory brainstem responses in children with hydrocephalus werefound in much older subjects3 lo or in children ofunspecified age.' In some instances the cause of thehydrocephalus was not documented. Previousinvestigators1 2 have showed that in the presence ofventricular dilatation there were increased I-Vinterpeak intervals that they attributed to increasedintracranial pressure. We know of no previouspublications on the association between the changesin auditory brain stem response and the develop-ment of posthaemorrhagic ventricular dilatation, the

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Fig 4 Effect ofventricular tap on the auditory brain stem response ofa baby girl born at 29 weeks' gestation with rightsided periventricular and intraventricular haemorrhages on ultrasonography. Before drainage the auditory brain stemresponses (both left and right) showed abnormal waveforms and latencies. One hour after cerebrospinalfluid tap there waslittle change in the auditory brain stem response (a unilateral increase in the amplitude of wave I on the left). The responsesremained abnormal. When auditory brain stem responses were measured again 24 hours later, there was considerableimprovement, particularly on the left, where both latencies and I-V interval had returned to normal limits. The right sideremained abnormal (prolonged I-V interval and abnormal waveforms). All stimuli at 80 dB and 10 clicksls.

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O Initial auditory brain stemresponse on 10th day

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Fig 5 Effect ofshunting on the auditory brain stem response in an infant born atfull term with posthaemorrhagicventricular dilatation. (a) Initial auditory brain stem responses show normal latency and wave configuration at 60 and40 dB. Ultrasonography shows some ventricular dilatation. (b) Effects ofprogressive ventricular dilatation lasting over threemonths (pronounced deterioration ofwave configuration, and disappearance ofresponses at 40 dB). Both lateral ventriclesshowpronounced dilatation on ultrasonography carried out on the same date as the auditory brain stem response. (c)Auditory brain stem response measured one week after shunting showing reversion to normal. The ultrasound scan showedthat the ventricles, while still dilated, had diminished in size. All stimuli at 10 clicksls.

effects of intermittent drainage of cerebrospinalfluid, or the rise in intracranial pressure. In thepresent study, we found no correlation, eitherpositive or negative, between the I-V interpeakinterval and the intracranial pressure in preterminfants, and this is probably due to better adaptationof the immature brain to increased intracranialpressure.The mechanisms whereby the brains of preterm

infants can adapt to increased intracranial pressureare open to speculation. One may be the balancebetween increased ventricular volume and the re-sorption of extracerebral cerebrospinal fluid. Whenthe limits of compensation are reached a sustainedrise in the intracranial pressure will ensue giving riseto the classic signs of increased intracranial pressurewith increasing head circumference, tense anteriorfontanelle, and suture diastasis."1

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Necropsy studies have also shown that in preterminfants with posthaemorrhagic ventricular dilatationconsiderable degrees of dilatation can occur beforethere is any rise in intracranial pressure.12 13Periventricular oedema, produced by cerebrospinalfluid extravasating through ruptures in the epen-dyma, may compress periventricular capillaries andcause ischaemic injury.14 Hill and Volpe have alsostressed that the immature state of the periventricu-lar tissue and the fact that it has been compromisedby a variety of hypoxic and ischaemic insults mayinfluence its adaptation to increased intracranialpressure.15Another factor influencing this adaptation is the

comparatively large subarachnoid space within thecranium of the premature infant.12 16 Among pre-term infants there is a wide variation in the size ofthe brain and of the extracerebral space dependingon the pressure to which the head has beensubjected in the uterus and on variations in fetalmaturity and nutrition.13 These facts are probablyrelevant to our findings concerning the associationbetween intracranial pressure and I-V interpeakintervals.The data should probably not be extrapolated to

infants born at full term or to older children. Ourdata for our single infant born at full term weresimilar to those previously reported. Nagao et alreported associated reductions in the amplitudes ofwaves IV and V, and prolonged latencies of wavesIII, IV, and V after experimentally induced intracra-nial hypertension in cats (the intracranial pressurebeing raised by expansion of a supratentorialballoon). 17 Although increased intracranial pressureand abnormalities in auditory brain stem responsehave been described in animals and in humans, 17-19Kraus et aP3 found ABR abnormalities in auditorybrain stem response in patients after shunts hadbeen inserted in the absence of increased intracra-nial pressure.Much less is known about the specific associations

between intracranial pressure and brain stem func-tion. Goodman and Becker studied the vascularabnormalities in the brain stem induced by intracra-nial hypertension in cats.20 They found that asintracranial pressure rose there was a parallelprogression of vascular disturbances, first in themicrocirculation and finally in the macrocirculation.Such reversible ischaemic changes in the brain stemcaused by alterations in blood flow may account forthe changes in auditory brain stem response onintermittent withdrawal of cerebrospinal fluid seenin some of our patients. In an experiment on cats,Nagao et al found progressive reduction in theamplitude of waves IV and V as the intracranialpressure was gradually increased by balloon infla-

tion, followed by progressive recovery during athree hour period after the balloon had beendeflated.21 They suggested that these changes weredue to direct mechanical pressure. The changeswere clearly not irreversible. Recently Little et alshowed that intraoperative auditory brain stemresponse recording during surgical treatment of abasilar artery aneurysm resulted in contralateralamplitude reduction of waves III-V only duringpontine retraction.22 The effect was transient andthe patient completely recovered. Another explana-tion for our data could be the recovery of brain cellsfrom interstitial oedema (or effused cerebrospinalfluid), a recovery reflected in an increase in waveamplitude.

This study has shown that in premature infantsabnormalities in auditory brain stem responses mayresolve irrespective of the persistence or progressionof ventricular dilatation. No correlation was foundbetween cerebrospinal fluid pressure and certainabnormalities of auditory brain stem responses(such as prolonged interpeak interval) but animprovement of the auditory brain stem response-especially of the amplitude-could occur afterdrainage of cerebrospinal fluid.A larger number of infants born at full term needs

to be studied to observe whether their response toventricular dilatation and raised intracranial press-ure is indeed different from that in preterm infants.

References

l Starr A, Amlie RN. The evaluation of the newborn brainstemand cochlear functions by auditory brainstem potentials. In:Krobkin R, Guilieminault C, eds. Progress in perinatal neurol-ogy. Baltimore: Williams and Wilkins, 1981:65-83.

2 De Vlieger M, Sadikoglu S, Van Eijndhoven JHM, Atac M.Visual evoked potentials, auditory evoked potentials and EEGin shunted hydrocephalic children. Neuropediatrics 1981;12:55-61.

3 Kraus N, Ozdamar 0, Stein L, Reed N. Absent auditorybrainstem response: peripheral hearing loss or brainstemdysfunction. Laryngoscope 1984;94:400-6.

4 Stockard JE, Stockard JJ. Brainstem auditory evoked potentialsin normal and otoneurologically impaired newborns and infants.In: Henry CE, ed. Current clinical neurophysiology-update onEEG and evoked potentials. Amsterdam: Elsevier, 1981:9-71.

5 Levene MI. Measurement of the growth of the lateral ventriclesin preterm infants with real-time ultrasound. Arch Dis Child1981;56:416-24.

6 Dubowitz LMS, Dubowitz V, Goldberg C. Clinical assessmentof gestational age in the newborn infant. J Pediatr 1970;77:1-10.Fawer C, Dubowitz LMS. Auditory brainstem responses inneurologically abnormal infants. Neuropediatrics 1982;14:88-92.

8 Lary S. Auditory brainstem responses in normal and abnormalpreterm and full-term infants. London: University of London1986. 310 pp. (Thesis.)

9 Kaiser AM, Whitelaw AGL. Cerebrospinal fluid pressureduring post-haemorrhagic ventricular dilatation in newborninfants. Arch Dis Child 1985;60:920-4.

10 Stein L, Ozdamar 0, Kraus N, et al. Foliow-up infants screenedby auditory brainstem response in the neonatal intensive careunit. J Pediatr 1983;103:447-53.



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Volpe JJ. Neonatal intracranial haemorrhage: pathophysiology,neurophysiology and clinical features. Clin Perinatol 1977;4:77-101.

12 Larroche JC. Developmental pathology of the neonate.Amsterdam: Excerpta Medica, 1977:368-98.

3 Wigglesworth J. Perinatal pathology. Major problems in pathol-ogy 15. Philadelphia: WB Saunders, 1984.Wozniak M, McLone DG, Riamondi AJ. Micro and macro-vascular changes as the direct cause of parenchymal destructionin congenital murine hydrocephalus. J Neurosurgl975;43:535-45.

15 Hill A, Volpe JJ. Seizures, hypoxic-ischaemic brain injury andintraventricular haemorrhage in the newborn. Ann Neurol1981;10:109-21.

16 Pape KE, Wigglesworth J. Haemorrhage, ischaemia and theperinatal brain. Clinics in developmental medicine 69170. Lon-don: William Heinemann, 1979.

17 Nagao S, Roccaforte P, Moody RA. Acute intracranial hyper-tension and auditory brainstem responses. Part 1: changes in theauditory brainstem and somatosensory evoked responses inintracranial hypertension. J Neurosurg 1979;51:669-76.

18 Nagao S, Sunami N, Tsutsui T, et al. Serial observations ofbrainstem function in acute intracranial hypertension by audi-tory brainstem responses-a clinical study. In: Ishii S, Nagai H,

Brook M, eds. Intracranial pressure V. Berlin: Springer Verlag,1983:474-9.

19 Benna P, Gill M, Ferrero P, Bergamasco B. Brainstem auditoryevoked potentials in supratentorial tumours. ElectroencephalogrClin Neurophysiol 1982;54:8-9

20 Goodman SJ, Becker DP. Vascular pathology of the brain stemdue to experimentally increased intracranial pressure: changesnoted in the micro and macrocirculation. J Neurosurg1973;39:601-9.

21 Nagao S, Roccaforte P, Moody RA. Acute intracranialhypertension and auditory brainstem responses. Part 2: Theeffects of brain-stem movement on the auditory brain-stemresponses due to transtentorilal herniation. J Neurosurg1980;51:846-51.

22 Little JR, Larkins MV, Luders H, Hahn JF, Erenberg G.Fusiform basilar artery aneurysm in a 33 month old child.Neurosurgery 1986;19:631-4.

Correspondence to Professor V Dubowitz, Department of Paedia-trics and Neonatal Medicine, Hammersmith Hospital, Du CaneRoad, London W12 OHS.

Accepted 20 July 1988



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Auditory brain stem dilatation - BMJ