Apnea after immunization of preterm

infants
Pablo J. S6nchez, MD, Abbot R. Laptook, MD, Linda Fisher, RN, MSN, CPNP,
Janet Sumner, RN, MSN, Richard C. Risser, MS, and Jeffrey M. Perlman, MB
From the Departments of Pediatrics and Academic Computing Services, University of
Texas Southwestern Medical Center at Dallas, and Women and Children Services,
Parkland Me morial Hospital, Dallas, Texas

Objective: To determine the frequency of adverse reactions, particularly the oc

currence of apnea, among preterm infants after immunization with diphtheria and
tetanus toxoids and whole cell pertussis vaccine adsorbed (DTP) and Haemophi lus
influenzaetype b conjugate (HibC) vaccine in the neonatal intensive care unit.
Study design: After the occurrence of apnea in two preterm infants following im
munization with DTP and HibC, a prospective surveillance of 97 preterm infants
younger than 37 weeks of gestation who were immunized with DTP (94 also received
HibC at the same time) in the neonatal intensive care unit was performed to assess
the frequency of adverse reactions and in particular, the occurrence of apnea. For
each infant, data were recorded for a 3-day period before and after receipt of the
immunization.
Results: The majority of preterm infants tolerated immunizations with DTP and HibC
without ill effects. However, 12 (12%) infants experienced a recurrence of apnea, and
11 (I I%) had at least a 50% increase in the number of apneic and brady cardic
episodes in the 72 hours after immunization. This occurred primarily among
smaller preterm infants who were immunized at a lower weight (p = 0.01), had ex
perienced more severe apnea of prematurity (p = 0.01), and had chronic lung
disease (p = 0.03).
Conclusion: The temporal association observed between immunization of pre term
infants and a transient increase or recurrence of apnea after vaccination merits
further study. Cardiorespiratory monitoring of these infants after immuniza tion may
be advisable. (J Pediatr 1997; 130:746-5 I)
diatrics in most cases, irrespective of the infant's gestational
two ELBW infants who had chronic lung disease of prema turity.
One infant was 25 weeks of gestation and weighed 700 gm at
Immunization of preterm infants with diphtheria and tetanus
birth. She received DTP and HibC (HibTITER, Lederle-Praxis
toxoids and whole cell pertussis vaccine (adsorbed) and
Biologics) immunizations on day 62 of life,
Haemophilus influenzae type b vaccine at 2 months chrono
logic age is recommended by the American Academy of Pe
Chronic lung disease
Presented in part at the 33rd lnterscience
age and even if the infant is of extremely lowConference on Antimi crobial Agents and Continuous positive airway pressure
birth weight) However, adverse effects of Chemotherapy (ICAAC), New Orleans, La., Diphtheria and tetanus toxoids and whole
cell pertussis vaccine adsorbed
DTP immunization adminis tered to ELBW Oct. 17-20, 1993.
Extremely low birth weight
infants have not been fully evaluated. 2-5 CLD
Haemophilus influenzae type b conjugate
We noted the occurrence of apnea after CPAP DTP
vaccine Neonatal intensive care unit
immunization of
ELBW HibC NICU
at which time she weighed 1840 gm and was receiving
Submitted for publication Nov. I6, 1995; accepted Oct. 11, 1996. theophylline therapy for apnea of prematurity. Four hours after
the vaccinations, lethargy and a marked increase in ep
Copyright 9 1997 by Mosby-Year Book, Inc.
0022-3476/97/$5.00 + 0 9/21/78494

746
The Journal of Pediatrics Sdnchez et al. 7 4 7 Volume 130, Number 5

isodes of apnea and bradycardia developed; the infant sub
sequently required mechanical ventilation for severe and re
current apnea. The second infant weighed 978 gm at birth and
had a gestational age of 27 weeks. On day 92 of life, she
received DTP and HibC vaccines after having had no apnea for
7 days. Within hours of the immunization, four episodes of
apnea and bradycardia developed that required tactile
stimulation; after 48 hours, no further episodes occurred. These
cases prompted a prospective evaluation of the fre quency of
adverse reactions and, in particular, the occurrence of apnea,
among premature infants who receive DTP and HibC
immunizations in the neonatal intensive care unit.
METHODS
The study population for the prospective evaluation of the
potential adverse effects of immunization on preterm infants
consisted of 101 consecutive premature infants younger than 37
weeks of gestation who received an intramuscular injec
tion of DTP vaccine (0.5 ml, Lederle Laboratories) in the NICU
at Parkland Memorial Hospital during a 17-month period (Nov.
14, 1991, through April 21, 1993).
Four ot" the 101 infants were excluded from the study
analysis. One had CLD and oxygen requirement at 58 days of
life; 17 hours after immunization with DTP and HibC vaccines,
respiratory distress developed and the infant required nasal
continuous positive airway pressure therapy. The chest
radiograph, however, was consistent with pneu
monia. Three other infants received DTP and HibC immu
nizations but their medical records were not available for re
view. Of the remaining 97 infants, 94 also received 0.5 ml of
HibC vaccine (HibTITER [Diphtheria CRM197 protein
conjugate], Lederle-Praxis Biologics) intramuscularly on the
same day as the DTP vaccine but at a separate site and with a
separate syringe. The decision and timing for the admin istration
of the vaccinations were made by the attending neonatologist.
All immunizations were administered by the nurse caring for the
infant.
The infants' medical records and history were reviewed.
Particular attention was directed to previous medical prob lems
such as hyaline membrane disease, apnea of prematu rity, CLD,
intraventricular hemorrhage, periventricular leu komalacia,
seizure disorder, sepsis, and meningitis. Chronic lung disease
was defined as persistent oxygen requirement beyond 28 days of
life that was associated with abnormal chest radiographic
findings.
Apnea of prematurity is determined by clinical observa tion of
the infant, invariably in association with cardiorespi ratory
monitoring; it is defined as a respiratory pause of 20 seconds or
longer, usually associated with bradycardia (heart rate less than
80 beats/min) and for which no other cause can be identified. 6
Apneic and bradycardic episodes were wit nessed and recorded
7 4 8 Sdnchez et al. The Journal of Pediatrics May 1997
Table. Comparison of infants who experienced recurrence or increase of apnea after immunization (group 1) with those infants who did
by the nurses who cared for the infants
as part of clinical practice and not by the research personnel.
The nursing staff were unaware of the ongoing surveillance
study. The standard response of nursery personnel to these
episodes is as follows: initial visual assessment of the infant for
evidence of chest wall movement and color, followed by cardiac
auscultation for determination of heart rate. If spon
taneous recovery of heart rate and respiration does not oc cur,
then gentle tactile stimulation of the infant is performed,
followed by oxygen therapy, bag-mask ventilation, chest
compressions, and intubation with subsequent mechanical
ventilation depending on the clinical severity and the re sponse
to the intervention.
The "severity" of the apnea was assessed by the need for
intervention and type of respiratory support required for its
management. The nursery protocol for management of ap nea of
prematurity consists of no specific therapy if episodes are mild
and self-limited, followed by theophylline therapy for frequent
and recurrent episodes that require nursing in tervention. If apnea
and bradycardia are more severe and re calcitrant to
methylxanthine therapy, then nasal CPAP is used. Finally,
mechanical ventilation is used for the most severe episodes that
are not responsive to combination ther apy with theophylline and
nasal CPAP.
For each infant, the maximum daily temperature, the number
of apneic episodes, the use of a cardiorespiratory monitor, and
the respiratory status were recorded for a 3-day period before
immunization, the day of immunization, and 3 days after
immunization with DTP. Complications that previously have
been attributed to DTP immunization also were noted (e.g.,
erythema, induration or abscess at the in
jection site, irritability, convulsion, persistent screaming, and
hypotonic-hyporesponsive episode)]
The study infants were assigned to one of two groups de
pending on the number of apneic episodes in the 3 days be fore
and the 3 days after receipt of their immunization. Group 1
consisted of infants who either (1) had no apneic episodes in the
3 days before immunization, but subsequently expe rienced at
least one episode in the 3 days alter immunization; or (2) had
apnea in the 3 days before immunization, but ex perienced a 50%
increase in the number of apneic episodes in the 72 hours after
immunization. Group 2 consisted of all other study infants who
either ( 1 ) had no apnea before or al ter immunization, or (2) had
the same or fewer number of apneic episodes in the 72 hours
after vaccination.
Statistical analysis. Data were analyzed by Student t test,
chi-square for contingency tables, and the Fisher Exact Test,
where appropriate. An exact linear trend test was performed for
analysis of maximal support required for management of apnea
of prematurity, as well as respiratory support at the time of
immunization between those infants who experi
enced either recurrence or increase of apnea after immuni zation
(group 1) and those infants who did not (group 2).
not (group 2)

Group I Group 2
No. (%) No. (%) p Value

23 74 --
Mean birth weight (gin) 873 _+ 218 1023 _+ 308 0.01 Mean gestational age (wk) 27 _+ 2 28 _+ 2 0.32 Median
Apgar scores 5/7 4/7 NS HMD 21 (91) 41 (55) 0.01 CLD 15 (65) 26 (35) 0.03 Apnea of prematurity:
Past history 23 (100) 70 (95) 0.60 Maximal support* 0.01 t None 0 (0) 4 (6)
Theophylline 2 (9) 19 (27)
Nasal CPAP 5 (22) 18 (26)
IMV 16 (69) 29 (41)
Time of immunization
Mean age (days) 67 _+ 9 71 _+ 22 0.25 Mean weight (gin) 1191 + 521 2279 _+ 597 0.01 Theophylline 8 (35) 24
(32) 0.90 Respiratory support 0.36t
None 16 (70) 59 (80)
Oxygen 5 (22) I I (15)
Nasal CPAP 1 (4) 3 (4)
IMV 1 (4)$ 1 (I)w
CLD, Chronic lung disease; CPAP, continuous positive airway pressure; HMD, hyaline membrane disease; IMV, intermittent
minute ventilation. *Maximal support refers to the maximum intervention required for management of apnea of prematurity (see
text).
tExact linear trend test.
~IMV, rate 14 breaths/min.
w rate 20 breaths/min.
were grades III or IV. One infant had a
ventriculoperitoneal shunt placed for posthemorrhagic hy
Differences were considered statistically significant for val ues of drocephalus. Nine (9%) infants had cystic periventricular
p <0.05. leukomalacia. Four (4%) infants had seizures in the imme diate
newborn period; seizures were attributed to hypoxia/ ischemia and
RESULTS no further ones were noted during the remain der of the nursery
Patient characteristics. The study population consisted of 97 stay.
infants; there were 50 girls and 47 boys. The mean birth weight A total of 33 episodes of sepsis and 3 of meningitis occurred
was 991 -+ 296 gm (range 460 to 2620 gm) and mean gestational among 26 infants; none occurred during the 7-day study period.
age was 28 -+ 2 weeks (range 24 to 34 weeks). Median Apgar Ninety (93%) of the 97 infants had cardiores piratory monitoring
scores were 4 and 7 at 1 and 5 minutes, re on the day of immunization, whereas 87 (90%) had monitoring on
spectively. The majority of the subjects were black (47%) and the day after immunization. Six (6%) infants were discharged to
Latin-American infants (33%). home 2 days after their im munization and 4 (4%) infants went
The majority (62/97, 64%) of infants had hyaline mem brane home on the third day after immunization.
disease; in 41 (42%) CLD developed. Ninety-three (96%) infants Immunization status. Of the 97 infants, 94 received DTP and
had experienced apnea of prematurity; the maximum intervention HibC vaccines on the same day. Three infants received HibC
for apnea was theophylline therapy in 21 infants, nasal CPAP in vaccine 7, 10, and 60 days after receipt of the DTP vaccine; no
23 infants, and mechanical ventilation in 45 infants. At the time of adverse events were noted and, specifically, no apnea occurred.
immunization, 32 infants were receiving theophylline and 16 The infants were immunized with DTP at a mean age of 70 _+ 19
required oxygen therapy, 4 were being treated with nasal CPAP, days (range 54 to 207 days) and at a mean weight of 2202 _+ 594
and two were receiving mechanical ventilation (Table). gm (range 987 to 4405 gm). Specifically, at the time of
Forty-seven (48%) infants had an intraventricular hemor rhage; 29 immunization with DTP, one in fant weighed less than 1000 gm,
of the hemorrhages (62%) were either grades I or II, and 18 (38%) 10 weighed between 1000

The Journal of Pediatrics Sdnchez et al. 7 4 9 Volume 13(1, Number 5

and 1499 gin, 26 between 1500 and 1995 gin, 29 between 2000
and 2495 gin, and 31 weighed 2500 gm or more. Post natal age
at the time of immunization was 54 to 59 days (n = 9), 60 to 69
days (n = 59), 70 to 79 days (n = 18), 80 to 89 days (n = 3), 90
to 99 days (n = 4), and 100 days or older (n = 4).
Adverse events after immunization. Apneic episodes
occurred in 34 infants after immunization, In l 1 (33%) of the 34
infants, the number of apneic episodes was unchanged (n = 9) or
decreased (n = 2) compared with the number of episodes in the 3
days before immunization. In 23 (66%, group 1) of the 34
infants, there was either recurrence of ap
nea (n = 12, none in the 3 days before immunization but at least
one episode in the 3 days after immunization) or a 50% increase
in the number of apneic episodes (n = 11 ) in the 3 days before
immunization compared with the 3 days after immunization.
Among the 12 infants who had recurrence of apnea after
immunization, 6 experienced apneicforadycardic episodes that
resolved spontaneously, whereas 6 infants required some degree
of medical intervention. This consisted of bag
mask ventilation (n = 1), nasal CPAP therapy with transient
oxygen administration (n = l), transient administration of
oxygen (n = 1), increase in oxygen requirement (n = 1), and
tactile stimulation (n = 2). Among the [ 1 infants who expe
rienced apnea in the 3 days before immunization but had a 50%
increase in the number of episodes in the 3 days after
immunization, 3 experienced apnea that resolved spontane ously,
whereas the others required new medical intervention for the
increased apneic/bradycardic episodes (i.e., oxygen
administration [n=41, increase in oxygen requirement [n = 2],
and tactile stimulation ]n = 2]).
Compared with the rest of the study population (group 2,
Table), the 23 infants who experienced either recurrence or
increase of apnea and bradycardia after vaccination (group
1) had a significantly lower mean birth weight and weight at the
time of immunization, and they were more likely to have CLD.
Severity of apnea of prematurity was assessed by the maximum
intervention that had previously been required tbr its
management. Exact linear trend analysis showed a significant
trend toward a greater degree of respiratory sup
port for management of apnea of prematurity in these 23 in fants
(group 1, Table) compared with the respiratory support for
apnea of prematurity that was required for those infants in group
2. Moreover, the two groups did not differ signif icantly in the
occurrence of seizures (groups 1 and 2, 4% each),
intraventricular hemorrhage (group I, 48%; group I1, 49%),
grades III/IV intraventricular hemorrhage (group I, 22%; group
II, 18%), or periventricular leukomalacia (group I, 4%; group
11, 1 I%).
A mild elevation in body temperature was the only other side
effect noted. In the 3 days alter immunization, 4 infants
had a maximum temperature of 37.8 ~ C and 2 other infants had
a maximum temperature of 37.9 ~ C; one of the latter had an
increase in apnea after immunization.
Subsequent immunization. Seven infants received their second
set of immunizations in the NICU, and one also re ceived a third
dose of DTP vaccine. Twelve hours after re ceipt of DTP and
HibC vaccines on day 121 day of life, one infant who had a birth
weight of 460 gm, a gestational age of 26 weeks and CLD, and
who had previously had apnea after the first immunization,
experienced 31 episodes of ap nea that required oxygen by nasal
cannula for a 24-hour pe riod. All of the other infants received
7 5 0 Srnchez et al. The Journal of Pediatrics May 1997
within 24 hours of immunization in l 9 infants. These infants
had a lower gestationa[ age, had longer duration of mechan ical
ventilation, and were more likely to have CLD than those who
did not experience apnea and bradycardia. Unlike the infants in
our study, these infants were not of a lower weight at birth or at
the time of immunization than those who did not experience
apnea after immunization. Two of these in fants, however, had
upper respiratory tract infections after immunization that could
have accounted for their apnea. In a recent report on the
immunologic responses of 16 ex tremely premature infants to
tetanus toxoid, H. influenzae type b polysaccharide, and polio
vaccines, D'Angio et al. t3 noted significant episodes of apnea in
the 24 hours after the first dose of DTP (Lederle-Praxis
Biologicals) and HibC (diphtheria CRMI97 protein conjugate,
their second immuni zations between 114 and 132 days of age
without sequelae. One infant who had persistent apnea of
prematurity had no increase in apnea after a third dose of DTP
on day 186 of life.
DISCUSSION
In this prospective evaluation, we found that there was a
transient recurrence (12%) or increase in apneic episodes (I 1%)
observed in immunized preterm infants that coincided with the
administration of DTP immunization. Because sys
temic and local reactions are significantly more frequent af ter
immunization with DTP than after diphtheria and tetanus toxoids
vaccine (adsorbed) alone, 8, 9 it could be postulated that the
apnea is related to the pertussis component of the vaccine, but
this is an unproved presumption and requires further study. Most
of the infants in our study also received HibC vaccine. In 1993
Washburn et al) ~ reported no side effects from administration of
HibC vaccine (PedvaxHIB, Merck Sharp & Dohme) to 22
chronically ill preterm infants with bronchopulmonary dysplasia.
Using the same HibC vaccine, Munoz et a[] 1 in 1995 also
reported no significant side effects among 36 preterm infants
with a mean birth weight of 1060 gm and a mean gestational age
of 28 weeks.
Bernbaum et al. 2 in 1985 and Koblin et al. 3 in 1988 ad
ministered DTP vaccine to 25 and 110 preterm infants, re
spectively, at 2 months chronologic age and both found sig
nificantly fewer febrile or local reactions than observed in
term infants. However, neither reported on the occurrence of
apnea. In the study by Bernbaum et al., only 13 of the 25
preterm infants received DTP vaccine before discharge from the
NICU and only a small number of the infants had med
ical problems such as broncbopulmonary dysplasia or per sistent
apnea and bradycardia that necessitated a prolonged hospital
stay. In the study by Koblin et al., only 12 (4.9%) of the preterm
infants received their first dose while still in the NICU,
indicative of a more medically stable population at lesser risk of
potential side effects than the one in our study.
In a retrospective study of 97 preterm infants immunized with
DTP before discharge from the NICU, Botham and Isaacs 12
reported the development of apnea or bradycardia
Lederle-Praxis Bio logics) in an infant with bronchopulmonary
dysplasia and ongoing oxygen requirement. Our prospective
observation supports this temporal association and the need for
contin ued study of potential side effects of vaccination of
ELBW infants.
Although the American Academy of Pediatrics recom mends
that preterm infants be immunized at 2 months chro nologic age,
t various investigators have documented that few infants in the
NICU are immunized on schedule. 14-I6 Moreover, after
discharge, many physicians caring for low birth weight infants
postpone immunization untit the infants reach a certain weight
or age. t4, 15 Others administer a half dose (0.25 ml) of DTP
vaccine even though such a dosage provides an inadequate
immunologic response without a re duction in adverse events, z
In our NICU, immunization with a full dose (0.5 ml) of DTP is
urged at 2 months chronologic age, although each neonatologist
is responsible for deciding the specific time to immunize each
high-risk infant. Ninety percent of our infants were immunized
by 3 months of age, with a median age of 63 days. At the time of
immunization, however, 12% of infants still weighed less than
1500 gm and 39% weighed less than 2000 gin. Moreover, 15%
still required oxygen, CPAP, or mechanical ventilation when
they were immunized and 34% were receiving theophylline for
apnea of prematurity.
The majority of preterm infants in this study experienced no
side effects from their vaccinations. However, a subset of infants
had a transient recurrence or increase in the frequency of apneic
episodes after vaccination; this was not limited to the first set of
immunizations. This occurred mostly among smaller preterm
infants who were immunized at a lower weight, had experienced
more severe apnea of prematurity as evidenced by past
requirement of either nasal CPAP or mechanical ventilation, and
had CLD. Given the transient nature of the apnea, these infants
may only require cardiac monitoring for 24 to 48 hours after
immunization rather than postponement of immunization until
their medical condition
is more stable or they have reached a certain weight. It is
possible that some infants who experienced apnea after their
immunization would have had similar episodes even if not
immunized. The lack of a control group in this study makes this
distinction impossible to assess. Other potential con
founders include the fact that the documentation of apnea and
bradycardia was performed in unblinded fashion by the nurses
caring for the infants; moreover, reliance was placed on bedside
nursing observation and cardiorespiratory mon
itoring rather than detailed recording of respiratory patterns.
Because of the increased survival of smaller and more immature
infants, further studies are needed on the optimal
time for their immunization and the use of acellular pertus sis
vaccines to minimize potential side effects. 17 Current
recommendations are based on very limited data concerning
both adverse events and immunologic response in these
high-risk infants. 1 In pursuit of some of these issues, a ran
domized trial of DTP vaccine versus placebo administered at 2
The Journal of Pediatrics Sfnchez et al. 7 5 1 Volume 130, Number 5
10. Washburn LK, O'Shea M, Gillis DC, Block SM, Abramson
JS. Response to Haemophilus influenzae type b conjugate
vaccine in chronically ill premature infants. J Pediatr
1993;123: 791-4.
11. Munoz A, Salvador A, Brodsky NL, Arbeter AM, Porat R.
Antibody response of low birth weight infants to
Haemophilus influenzae type b polyribosylribitol
phosphate-outer membrane protein conjugate vaccine.
Pediatrics 1995;96:216-9.
12. Botham S J, Isaacs D. Incidence of apnoea and bradycardia in
preterm infants following triple antigen immunization. J Pae
diatr Child Health 1994;30:533-5.
13. D'Angio CT, Maniscalco WM, Pichichero ME. Immunologic
months chronologic age is currently in progress to de termine
causality of apnea after immunization and to assess risk factors
for its occurrence.
We thank Maria Paris, MD, for assistance in performing the
sta tistical analyses; Fiker Zeray, RN, and N. Kristine Leos, BS,
for as sistance in data collection and entry; and John D. Nelson,
MD, for review of the manuscript.
REFERENCES
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1994 Red Book: report of the committee on infectious
diseases. 23rd ed. Elk Grove Village [IL]: The Academy,
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2. Bembaum JC, Daft A, Anolik R, Samuelson J, Barkin R,
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3. Koblin BA, Townsend TR, Munoz A, Onorato I, Wilson M,
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RD, McMillan JA, Warshaw JB, editors. Principles and
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8. Cody CL, Baraff LJ, Cherry JD, Marcy SM, Manclark CR.
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9. Howson CP, Fineberg HV. Adverse events following
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14. Vohr BR, Oh W. Age of diphtheria, tetanus, and pertussis im
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15. Langkamp DL, LanghoughR. Primary care physicians' knowl
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16. Langkamp DL, Langhough R. What do parents of preterm in
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 _50 Years Ago in The Journal of Pediatrics

Compulsory prepaid medical care

Boas EP. J Pediatr 1947;30:478-81.

Fifty years ago in The Journal, the debate over health care and how to provide it raged between the foi favoring
private and those favoring public support. That now-long-past debate still sounds several thet that simply do not
appear to die. Dr. Boas writes, "Unless we regard medical care as a luxury which p ple may or may not obtain,
depending on their ability to pay for it, we are faced with the compell problem of how to make it available to all,
irrespective of income." He goes on to say, "It is at this pc that many persons leave the cold path of logic and,
rationalizing their fear or dislike for an extensior governmental responsibility, seek to find a solution in halfway
measures, such as the establishmenl voluntary health insurance schemes, and the construction by government of
hospitals and diagnostic c ters."
The past several years in the United States have seen similar tumultuous debates concerning such sues, but with
little definitive action to solve the problems of equal access to health care and the me to deliver cost-effective,
high-quality health care that evolves from new knowledge in the clinical basic sciences. In large part through
inaction or reaction, the government and the medical profession h~ abdicated their responsibility for a solution
to groups of insurers and managed care corporations. Dr. B, concludes his article with the statement that "it is
high time that physicians become aware of the cha~ ing order in science, in medicine, and in society, and that
they give their best brains and efforts, no1 delaying tactics or sabotage, but to the end that in the foreseeable
future excellent medical care will available to all of the people of the United States." It is immensely ironic that
this debate continues years later. Unfortunately, irony does not save lives or improve health care coverage.
Robert J. Arceci, MD, P
Division of Pediatric" Hematology/Oncoh
Children's Hospital Medical Cer
Cincinnati, OH 45229-3(