EFFECT
OF
AGE,
SEX, AND
CYSTIC
FIBROSIS
ON
THE
SODIUM
AND
POTASSIUM
CONTENT
OF
HUMAN
SWEAT
Charles C. Lobeck, M.D., and Dorothy Huebner, B.S.
Department of Pediatrics, University of Wisconsin Medical School, Madison, Wisconsin
Supported by grant A-2815 from the National Institute of Arthritis and Metabolic l)isease and by
gifts from the Wisconsin Chapter, National Cystic Fibrosis Research Foundation. ADDRESS: (CCL.) 1300 University Avenue, Madison 6, Wisconsin.
P1r.I3IAUUC5, August 1962
ARTICLES
172
T
HE OBSERVATIONby
Darling et ai.1 thatthe eccrine sweat of children with
cystic fibrosis of the pancreas has greater
concentrations of sodium, potassium, and
chloride than those found in healthy
sub-jects has given new impetus to studies of
the physiology of sweating. These high
concentrations, which are found in almost
every clinical case of the disease, are not
only of unquestioned diagnostic value but
also may be of importance in considerations
of etiology.
The study of sweating in cystic fibrosis
requires an awareness of the sources of
variability in the composition of the sweat
of healthy, active individuals. The most
im-portant of these sources, which have been
previously described, are the increase in
sweat sodium and chloride concentrations
with increased rates of sweating,2’3 the
ef-fect of adrenal activity, exemplified by the
high sweat sodium and chloride
concentra-tions found in Addison’s disease,4 and the
recently described increase in sweat sodium
content with aging.5 Other factors, such as
increase in deep skin temperature,6
inter-mittent occlusion of blood supply, and
re-peated stimulation of secretion8 can cause
increases in sweat sodium and chloride
con-centrations. These are more easily
con-trolled in experimental situations.
The search for incomplete expressions of
the sweat abnormality of cystic fibrosis in
parents and siblings of children with this
disease, or in patients with similar
syn-dromes, gives further impetus to the study
of variations in the electrolyte content of
sweat from healthy, unrelated subjects. For
instance, several observers9’ have reported abnormally high sodium and chloride con-centrations in some of these parents and siblings. Other observations have revealed that some patients with bronchiectasis,2
pulmonary emphysema,1:: asthma,hi and
peptic ulcers’ have elevated sweat sodium
and chloride concentrations. The
interpre-tation of these findings depends upon the
range of variation that can be observed in
control subjects.
This paper describes the variability in
sweat sodium and potassium concentra-tions, with measurements of tile rates of
sweating, following a standard pilocarpine
iontophoresis procedure in children with
cystic fibrosis, their siblings and parents, as
compared to control children and adults of
both sexes and varying ages.
METHODS
The control subjects consisted of 197
children and adults varying from 1 month through 60 years of age. Some of tile
cliii-dren under 11 years of age were
hospital-ized for diseases not clinically related to
cystic fibrosis. Results obtained from these
children did not differ from those of
healthy children of the same age. All of
the adolescents and adults were healthy
and active without pulmonary disease or clinical evidence of ulcers. Controls were compared to 34 patients with cystic fibrosis
who had abnormally high electrolyte
con-centrations in sweat with evidence of either
or foul 1)tllky stools and a slow rate of
growth and osseous maturation. These
pa-tients were seen and studied by one of the
authors (C.L.). Fifty-three parents and 18
siblings of these patients, all healthy and
active, were also studied.
Each of the subjects was a resident of
either Wisconsin or Northern Illinois. All
sweat collections except those of the
cliii-dren with cystic fibrosis were made
he-tween the dates of September 12 and June
5. The average monthly environmental
temperature for Madison varied between
17#{176}Fand 64#{176}Fduring this period.
Sweat was collected following
pilocar-pine iontophoresis from the flexor aspects
of either forearm in an air conditioned
room with a temperature of approximately
72#{176}Fand relative humidity of 60 to 70%.
The direct current source for pilocarpine
iontophoresis was constructed similarly to
that of Gibson and Cooke.3 The electrodes
employed were circular with a porous metal
base topped by a reservoir. Their diameter
was 3.1 cm and their surface area 7.54 X
10 square meters. The positive electrode
was filled with an aqueous 0.5% pilocarpine
nitrate solution and the negative with an
aqueous 1.0% NaNO:: solution. To prevent
burns and the stinging sensation that
occa-sionally occurs during iontophoresis, the
surface of the positive electrode was
cov-ered with a circle of ashless filter paper
saturated with pilocarpine nitrate and the
negative electrode wrapped with a gauze
saturated with NaNO:s solution. The
posi-tive electrode was held firmly in place at
about the midpoint of the flexor surface of
the forearm and the negative electrode
op-posite it on the extensor surface with a
rubber strap.
A current of 1.5 ma was passed through
the arm for 5 minutes. The electrodes were
then removed and another 5 minutes
al-lowed to elapse before tile area previously
occupied by tile positive electrode was
carefully washed with distilled water and
covered with a circle of tared no. 42
What-mann ashless filter paper of tile same
sur-face area as the electrode. A vapor barrier
of parafilm was taped over the filter pa-per, and sweat was collected for 25 to 35
minutes. The collection period was
care-fully timed to determine its exact length
within these iimits, for determination of the
rate of sweating. For purposes of
compari-son, the use of collection periods of
ap-proximately equal length was necessary,
since in preliminary experiments on adults
the rate of sweating and sodium
concentra-tion of the sweat decreased continuously
during the 30-minute period. Thus, varying
the length of the collection period between
subjects could be a source of variation in
observed electrolyte concentrations and
rates of sweating.
The weight of sweat collected was
de-termined by weighing the filter paper on
an analytical balance immediately after
col-lection. Since the area from which the
col-lection was obtained and the exact time the
paper was in contact with the skin were
known, the grams of sweat secreted per
square meter of skin per minute (gm/m2/
mm) was calculated to express the rate of
sweat secretion during the 30-minute period.
Electrolytes were eluted from the paper
by washing twice with 10 ml of distilled
water. The eluate was centrifuged and
ali-quots of the supernate were used for the
analysis of sodium and potassium in a
Baird Associates flame photometer with
lithium as an internal standard. In recovery
experiments, with the same technique and
aliquots of the same volume as in the
un-known sweat samples, it was found that
the maximum experimental error was
ap-proximately 10% if more than 0.001 meq of
sodium was present in the original sample
while less than this amount gave a
maxi-mum error of 25%. In the case of potassium,
a maximum error in the analysis of 6% was
obtained, but it was found that the elution
procedure increased this to 20% at all levels
of potassium concentration observed in the
sweat samples.
RESULTS
Sweat Rate Sweat Na Sweat K
Subj eel.Number (giu/in2/min)
Arerage ± SD#{176} Range
(iiieq/l) (meq/l)
.4rerage ± Sl)*
Average ± SD* Range
7.8±4.5 1.7-19.7 10.7±3.6 3.8-’20.1
8 6.1±’2.0 3.’2-9.1 11.4±3.6 5.4-16.’2
‘25 6.1±3.0 ‘2.5-14.1 17.9±8.7 7.1-38.0
17 5.6±’2.8 ‘2.l-1’2.4 16.7±8.7 6.1-37.9
6-10 yr
9.9±3.’2 (14)
11.3±3.4 (16)
7.5±1.6 (14) 10.0±2.1 (6)
11-19 yr
Male
Felnale
‘20-6(1 yr
Male
Female
Patients with cystic fibrosis
3 mo-17 yr
Male
Felnale
Parents
‘26-5’2 yr
Male
Female
Siblings
3-15 yr
MIlk
F’elnak-* Standard deviation.
7.1±0.9(11) 10.0±’2.5 (15)
10.1±1.6 (4)
9.9±3.’2 (8)
t Numbers in parentheses refer to number of subjects with potassium analyses.
period after pilocarpine iontophoresis are
shown in Table I. Adult males in both the
group of control subjects and parents of
children with cystic fibrosis had
signifi-cantly higher rates of sweating than
fe-males (p <0.001). This sex difference was
not found during childhood.
Greater variability in observed rates of
sweating was noted in infants under 1 year
of age than in older children. In the former
group, 8 subjects, or 27%, had sweat rates
above 10 gm/m2/minute; only 6% of the
108 remaining control subjects under 20
years of age had rates above this figure. Of
these 15 children in both groups with high
rates of sweating, 13 were male. The same
increased variability in sweat rates was
ob-served in infants with cystic fibrosis. Three
of 7 under 2 years of age as compared to 2
of 27 older children had rates higher than
TABLE I
AGE AND SEX VARIATION IN TIlE RATE OF SWEATING, SWEAT SoDIUM, AND POTASSIUM (0NCENrIIATION
Controls
1-PI 1110 Male
Feinalt-1-5 yr Male
Felnale
Male
Female
15 3.7±1.6 .1-7.7
13 3.9±.l I.-9.()
16.5±5.8 7.1-i8.3
20.6±9.7 1’4.0-46.5
10.7±1.9 (9)t
loi.8±1.6 (‘2)
10.’2±3.1 (10)
11.’2±_.’2 (9)
11.1 ±1.9 (l’2) 9.8±1.5 (8)
‘20 5.7±3.3 0.9-15.9 6.9±13.3 5.3-5’2.’2
18 4.3±3.4 0.9-17.’2 ‘26.3±13.1 7.4-61.3
33 7.±1.8 3.5-11.9 51.9±’21.1 9.9-96.4
‘26 4.6±1.6 ‘2.1-8.8 36.5±18.7 9.5-80.1
16 7.0±.9 ‘2.-14.8 111.6±16.’2 87.6-141.’2 16.1±5.1(5) 18 5.8±.7 1.0-10.9 106.3±’24.8 54.9-158.’2 14.0±’2.3(6)
‘2’2 6.’2±.5 ‘2.3-11.3 45.1±17.7 ‘2.4-84.8
31 4.0±’2.() 1.3-9.1 39.’2±’20.6 5.9-86.3
8 4.6±3.3 oL4-1’2.4 ‘21.7±10.5 7.7-39.1
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ARTICLES 175
PARENTS CONTROLS
10 0
RATE OF SWEATING (gm/m’/minute)
FIG. 1. Relationship of sweat sodium concentrations to rates of sweating in adults, in (left) 22 fathers and 31 mothers of children with cystic fibrosis, varying from 26 to 5:3 years of age, and (right) 33 male and 26 female control adults varying from 20 to 61 years of age. (Coefficients of correlation: parents,
R = 0.34, p < th05; controls, R = 0.42, p < 0.01.)
10 gm/m2/minute. Only two of the five
children with high rates were males. There
were fl() differences observed in rates of
sweating between siblings of children with
cystic fibrosis and control children of the
same age. In other words, sex differences in
tile rate of sweating were not marked until
adulthood, but there was much more
vari-ability in the rates of sweating induced in
infants with or without cystic fibrosis. A
preponderance of the children with high
rates were males.
Sweat sodium concentration increased
with age. As shown in Table I, under the
age of 1 year there was a very low average
sodium concentration, which increased
slowly during the ensuing years until the
adult value was reached after the age of
20. In adults the variability of these
concen-trations was much greater than in children.
No differences in the sodium
concentra-tions were observed between parents and
control adults or between siblings and
con-trol children. Tile variability of these
con-centrations also did not differ between
these groups. As with the rates of
sweat-ing there were no sex differences in sodium
concentration under tile age of 20 years; in
adulthood, however, males in the control
group had higher sodium concentrations
than females (p < 0.01). Concentrations in
control children and siblings did not over-lap the distinctly higher concentrations in children with cystic fibrosis. This indicates
the value of this determination for
diag-nosis during childhood. Values in adults,
however, did overlap considerably those in
children with cystic fibrosis; 29% of tile
values in control adults and parents of the
patients with cystic fibrosis were over 55
meq/l, the lowest concentration for a child
with the disease.
The relationship of sweat sodium concen-tration to rate of sweating is shown in Figures 1, 2, and 3. In control adults, chil-dren with cystic fibrosis, and their parents
(Figs. 1 & 2), though great variability
between subjects was observed, the
high-est sodium concentrations were found at
tile highest rates of sweating. This was not
true in control children from 1 month to 11
years of age where the highest sodium
con-centrations were found at the lowest rates
of sweating (Fig. 3). Comparison of the
parents of the children with cystic fibrosis
and control adults (Fig. 1) revealed no
sig-nificant differences. In the parent group the
higher sodium concentrations at lower rates
of sweating and the absence of low sodium
I MONTH TO IIYEARS
oFEMALE
#{149}MALE
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176 CYSTIC FIBROSIS
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0
#{149} 0
0 #{149} 0 FEMALE
0 SMALE
50i#{176}i I I I I I I
0 0
RATE OF SWEATING (gm/m2/minute)
15
FIG. 2. Relationship of sweat sodium concentrations
to rates of sweating in children with cystic fibrosis.
The 34 subjects were between 3 months and 18
years of age. (R = 0.39, p = 0.05.)
was probably due to the fact that 58% of
this group was comprised of females, whereas only 44% of the control group were
females.
The sweat potassium concentrations are
shown in Table I. In childhood, the
aver-age sweat potassiums showed no sex
differ-ences and remained remarkably constant.
In adulthood, males had significantly lower
values than females, who remained at the
childhood level. Again parents and siblings
of children with cystic fibrosis did not
dif-fer from control subjects of the same age
and sex. However, children with cystic
fi-brosis had significantly higher potassium
concentrations than other children.
In the case of potassium, there also was a
relationship of concentration to rate of
sweating, but the highest potassium
con-centrations were found at the lowest rates
of sweating in all age groups. These
rela-tionships are shown in Figure 4; in control
adults and parents of children with cystic
fibrosis, the females with the lower rates of
sweating had higher potassium
concentra-tions while the males had low
concentra-tions at all sweat rates. As stated
previ-ously, it will be noted in Figure 4 that only
3 male control children had potassium
con-centrations below 8 meq/l at any rate of
sweating, while 20 control males had
con-centrations below this figure, but none
lower than 5.5 meq/l. Children from 11
through 19 years of age were intermediate
between these two age groups. The 11
children with cystic fibrosis whose sweat
was analyzed for potassium showed no
dis-tinct relationship of potassium
concentra-tions to rates of sweating. It was noted,
however, in this small group, that there
was a tendency to higher potassium
con-centrations at high rates of sweating rather
than at low rates; the four highest
potas-sium concentrations were at rates of
sweat-ing above 7 gm/m2/minute, and five of the
lower values were at lower rates.
COMMENT
Our results confirm the observation by
Anderson and Freeman5 that the sodium
concentration of tile sweat is lower and less
variable in prepubertal children than in
adults. These investigators using the
intra-dermal injection of methacholine chloride
and collecting sweat for 1 hour obtained
results essentially identical to ours despite
the differences in technique. Data are not
available for comparing our results with
those from sweat obtained after thermal
stimulation. Gr#{216}nbaek,17 however, observed
marked increase in tile average Na/K ratio
of the sweat with aging in collections from
the hand following thermal stimulation.
The magnitude of the change he observed,
from 1.24 in children under 9 years to 3.25
40
a.
30
z
I.-20
U.,
0
A
CONTROLS
0 5 0 5
RATE OF SWEATING (gm/m2/minute)
FIG. 3. Relationship of sweat sodium concentrations
to rates of sweating in 100 control children-38
II.
a. U, E
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5
0 II
S #{176}
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-#{149}CONTROL MALE
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23 TO 53 YEARS-a FEMALE PARENT I
-I
5 a MALE PARENT
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-A
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MONTH TOIIYEARS
II I 1 1111 11__J.___i1 I I I I I I I 1 I I
5 10 0, 5 0
RATE OF SWEATING (gm/m’/minute)
FIG. 4. Relationship of sweat potassium concentrations to rates of sweating. On
the left are shown data from 50 control children; on tile right, from 20 control
adults and 26 parents of children with cystic fibrosis. (Dashed line is at 8 meq/l.)
CONTROLS
< 5 gm/m2/min.
50
--->7
gm/m2/min.
gm/m2/min.
a-E
z
I-1<
w
1’
10
I II MO-5
6-10
11-19
20-61AGE (YEARS)
FIG. 5. Increase in sweat sodium concentration
with increasing age. Independence of age
varia-tion from rate of sweating demonstrated by lines
drawn through average sweat sodium
concentra-tions of subjects grouped as to rates of sweating. in adults over 30 years, indicates that it
must have been due largely to increase in
sweat sodium concentration. From our data
it is clear that the increase in sodium
con-centration with aging is independent of
variations in the rate of sweating (Fig. 5).
Increase in sodium or chloride
concentra-tion with increasing rates of sweating has
been previously described by several
in-vestigators.2- Our data suggest that this
relationship holds true only in adults and
in one group of children, those with cystic
fibrosis. Its presence in the latter group
in-dicates that this relationship of sodium
con-centration to rate of sweating depends
upon tile presence of high concentrations of
sodium in the secreted sweat and not on
age alone.
In control children, the relationship of
sodium and potassium concentrations to the
rate of sweating were similar, i.e., the
high-est concentrations of both cations were
found at the lower rates of sweating.
How-ever, no correlation between sodium and
potassium concentrations were observed
(R = 0.10), indicating that the higher
so-dium and potassium concentrations in this
group were not simply the effect of water
reabsorption in the gland.
It has been postulated by Schwartz and
Thaysen2 that the reason for the depend-ency of sodium concentration on the rate
of sweating in adults is the ability of tile
tubule of the gland to reabsorb a relatively
fixed quantity of sodium from the initial
secretion. In the light of this hypothesis,
our data suggest that children with cystic
fibrosis, their parents, and healthy adults
178 CYSTIC FIBROSIS
This would indicate that, in cystic fibrosis,
the primary secretion has an abnormal
com-position and that the defect is not simply
one of failure of reabsorption.
Marked sex differences were noted in
adults whether or not they were parents
of children \Vitil cystic fibrosis. The
obser-vation that women had lower sweat rates
than men confirms the findings of several
Otiler investigators18 19 that women sweat
less than men in response to a standard
stimulus. Tile lower sodium concentrations
observed in women are probably due to the
low rates of sweating produced. However,
in women, potassium concentrations were
variable and tended to be at the same level
found in children, while men had lower
potassium concentrations than children at
all rates of sweating. Thus, we have
ob-served two attributes of the adult male:
(
1) increase in tile responsiveness of thesweat gland to stimulation and (2) secretion
of a sweat potassium concentration
ap-proaching tllat of extracellular fluid.
If the widely ileld contention that cystic
fibrosis is transmitted as an autosomal
re-cessive characteristic is correct,2#{176} then each
one of the parents silould carry tile trait.
From our data it is obvious that a partial
expression of the sweat abnormality
can-not be detected on the basis of a single
sweat electrolyte determination after
pilo-carpine iontophoresis. Since survival of
chil-dren with the disease to adulthood is a
rarity, the many differences described
above between children and adults make
it important to compare children with
cys-tic fibrosis only witil other cilildren of tile
same age. Assuming the autosomal
reces-sive inheritance, 66% of tile healthy children
born to families having a child with cystic
fibrosis should also be heterozygous. Tile
small number of siblings of children with
cystic fibrosis in tilis study reveal no
dif-ferences from unrelated children. Age
dif-ferences must also be kept in mind when study is made of patients with related
ill-nesses. The values reported as indicating
excessive sweat salinity in asthma,”
bron-clliectasis,12 peptic ulcer,” and pulmonary
emphysemaH are all within tile range we
have observed for adults without these
conditions.
Tile data reported in this paper also
demonstrate tile wide variability in tile response to a standard stimulus between
healtily people of tile same age. It is
pos-sible that much of this variation is due to
slight differences in the number of sweat
glands present in the area subjected to iontophoresis. Kuno2’ has reported
obser-vations by Kawahata that though tile total
number of sweat glands in various areas of
the skin remains constant after 2 years of
age, before that time tile glands, though
fewer in total number, may be more
con-centrated per unit surface area. This could
explain the greater sweat rates obtained in
some cilildren under 1 year of age but
would not explain the sex differences in tile
rates of sweating observed in adults.
SUMMARY
The following observations were made
on collections of sweat from 197 subjects
witilout evidence of disease related to
cys-tic fibrosis of the Paicreas after production
of localized sweating on the forearm by a
standard pilocarpine iontophoresis
proce-dure : 1. Sodium concentrations averaged
less than 20 meq/l in children under 11
years of age, while in adults the average
concentration rose to 45 meq/l. Sodium
concentrations were less variable in
chil-dren than in adults. Age variation in
so-dium concentration did not depend upon
variation in tile rate of sweating. 2. Tile
average potassium concentration in all
children and adult females was 11 meq/l.
It was lower, 7 meq/l, in adult males. 3.
Other sex differences, observed only in
adults, were tile higiler rates of sweating
and sligiltly iligher sodium concentrations
found in males. 4. Rates of sweating
meas-ured in children under 1 year of age were
considerably more variable than tilose
in-duced in older children or adults.
Comparison of tilese data with
observa-tions from 34 children with cystic fibrosis
ARTiCLES 179
with this disease always had higher sodium
concentrations than pre-pubertal control
subjects. Twenty-nine per cent of adult
control subjects had concentrations within
tile cystic fibrosis range. 2. Children with
cystic fibrosis had a higher average
potas-sium concentration, 15.0 meq/l, than
con-trol children. 3. No sex differences were
oh-served within this group, and tile same
in-creased variability in rates of sweating
in-duced in control infants was noted in
in-fants with the disease.
Observations on 53 parents and 18
sib-lings of the children with cystic fibrosis did
not reveal any differences from control
sub-jects of the same age. It was concluded that
age, sex, and the presence of cystic fibrosis
have a profound effect on the composition
of sweat obtained after pilocarpine
ionto-phoresis.
REFERENCES
1. Darling, R. C., et a!.: Electrolyte
abnormali-ties of the sweat in fibrocystic disease of the
pancreas. Amer.
J.Med.
Sci., 225:67, 1953. 2. Schwartz, I. L., and Thaysen, J. H.:Excre-tion of sodium and potassium in human sweat. J. Clin. Invest., 35:114, 1956.
3. Locke, W., et a!.: Studies on combined use
of measurements of sweat electrolyte
com-position and rate of sweating as an index
of adrenal cortical activity.J. Clin. Invest.,
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4. Conn, J. W.: Electrolyte composition of sweat.
Arch. Intern. Med. 83:416, 1949.
5. Anderson, C. M., and Freeman, M.: “Sweat test” results in normal persons of different ages compared with families with fibrocystic disease of tile pancreas. Arch. Dis. Child.,
35:581, 1960.
6. Robinson, S., et a!.: Effect of skin
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J.
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7. van Heyningen, R., and Weiner,
J.
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14. Hsia, D. Y. Y., et a!.: Abnormal sweat
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15. Koch, E. : Hereditary adult mucoviscidosis and
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17. Cr#{216}nbaek, P. : Tile sodium/potassium ratio in
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18. Gibson, T. E., and Shelley, \V. B.: Sexual and
racial differences in tile response of sweat
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19. Kahn, D., and Rothman, S.: Sweat response
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20. Hsia, D. Y. Y.: Inborn Errors of Metabolism.
Chicago, Yr. Bk. Pub., 1939, p. 198. 21. Kuno, Y.: Human Perspiration. Springfield,
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Acknowledgment
We are particularly grateful for the enthusiastic
cooperation of the parents, patients, and control
subjects who participated in this study. We are also indebted to Dr. Gerald Kerrigan and the staff of the Milwaukee Children’s Hospital, to the staff
of the Wisconsin High School, and to Dr. Arthur