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ORIGINALES
CATH-UP GROWTH IN THE PERINATAL PERIODAFTER INTRAUTERINE GROWTH RETARDATION
UNDER FAVOURABLE NUTRITIONAL CONDITIONSRESULTS FROM A LONGITUDINAL STUDY
Ingeborg Brandt *Universitäts-Kinderklinik Bonn, F.R. Germany
Since the classic publication of Prader, Tanner and von Harnack in1963 on catch-up growth this idea has become current in pediatrics, andhas attained increasing relevance. The subject of this first publication hasbeen catch-up growth in bone age, weight and height in the second to the13th year of life. Also subsequent publications about this phenomenon havebeen concerned with bone age, and growth in length and/or weight beyondthe first six months of life.
There is still little literature on catch-up growth of head circumferenceafter intrauterine growth retardation and no information about the timingof the catch-up (Falkner, 1966; Babson et al., 1974).
To begin with some definitions: by «perinatal period» is understoodthe time from 28 postmenstrual weeks to the seventh day after term oraf ter expected date of delivery. In he preterm infant the perinatal periodcovers the third trimester of pregnancy in the full term infant. Postmens-trual or gestational age is the time from the first day of the mother's lastmenstrual period until birth or until date of examination. Catch-up growthin head circumference is defined as follows: birth measurements signifi-cantly below the man of the AGA preterm controls and below the 10thpercentile of Lubchenco, head growth reaching the normal range untilshortly after term, i.e. no significant difference to AGA preterm and fullterm infants, and proven by a period of significantly higher growth velocitythan in the AGA preterm infants.
Although the causes of intrauterine growth retardation are heteroge-nious, two major groups can be differentiated:
a) Fetal factors as genetic defects, chromosomal abnormalities, mal-formations, infections, radiations of hypoxemia. The further fate of these
Trabajo presentado en la Sociedad Catalana de Pediatría en mayo de 1976.
181
infants is depend besides on the quality of postnatal care on the primarycausative factors.
b) Maternal and placental factors such as «vascular insufficiency»mechanisms, toxemia, smoking, undernutrition, which after birth have nofurther influence upon development. The fate of these SGA is dependentbesides on duration, timing and severity of intrauterine restriction onpostnatal care and nutrition. Not only immediate hypoglycemia but alsolack of energy during the brain growth spurt in the perinatal period arerisk factors for those infants who, because of lacking adipose lissue(Burmeister et al., 1974), and deficient reserves of glycogen have no reserves.
Methods For the judgement of an infant —if appropriate (AGA) " or smallfor gestational age (SGA) "— the first prerequisite is the diagnosis
of gestational age as exact as possible by the external clinical characteristics(Farr et al., 1966) and by newborn neurology. Precision of diagnosis is increasedby repeated ultrasound measurements of the fetus in the early weeks of preg-nancy (Hansmann, 1974) and by an exact obstetric history. In some cases thedate of conception is known by measurements of the basal temperature. Thesecond prerequesite are intrauterine growth curves for comparison. As SGAare classified preterm infants with a birth weight below the 10th percentile ofLubchenco. No. 1 in figure 1, corresponding well to the 10th percentile of theGerman data from Hoseman (1949), No. 2 in Figure 1. The synopsis of intrauterine«growth curves» from different authors in Figure 1 shows that between 33 and37 postmenstrual wceks the curves of Lubchenco, Hoseman, Gruenwald and Ho-henauer agree quite well, whereas the curves of Thomson and of Babson run ahigher level, similar to the Sterky curves, not plotted here.
In a longitudinal study of postnatal growth and development of pretermand full term infants, started in 1967 at the Bonn Universitäts-Kinderklinik, tillnow also 43 SGA preterm infants have been examined regularly. 21 of whombelong to a new special group, hitherto with a more favourable developmentthan the other SGA of the study. Figure 2 shows their birthweight —in all butthree below 1500 g—, as well as head circumference and supine length afterbirth according to fetal age, compared with the percentiles from Lubchencoet al. (1963 and 1966).
Figure 3 demostrates the biparietal and thorax diameters of those infantswith follow-up prenatal ultrasound examinations. In comparison with the Bonnstandards (Hansmann, 1973, 1974 and 1976) the growth retardation is clearly tobe seen in both parameters, the biparietal diameter being less affected however.The same has been proven in a group of about 100 growth retarded infants. Thisis in accordance with the results of Gruenwald (1963), Naeye et al. (1966), andMyers et al. (1971) that brain weight —and therewith the head— may be leastaffected by intrauterine malnutrition.
Theoretically the proof of «real catch-up» of an infant is possible only if thegenetic potential of the individual in known of —in the case of an older child-the deviation from the growth channel and/or the returning to it has been ob-served. For differential diagnosis between a merely «genetical small infant» andintrauterine growth retardation in a small SGA newborn, the previous knowledgeof the intrauterine course of growth and of the Urning of retardation is of greathelp. The causative maternal factors for intrauterine restriction as placentalinsufficiency, multiple birth or maternal undernutrition affect the fetus in thethird trimester only. This retardation does not fall into the period of neuronal
' Abreviations: AGA = appropriate for gestational ageSGA = small for gestational age
182
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I90%
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32
36
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postmenstrual weeks
FIGURE 1: Intrauterine standards for weight, based on birthweightmeasure-Trients of infants born at different postmentrual ages.
multiplication which is —according to Dobbing (1974) and Herschkowitz (1973)—already completed in the third trimester. The period of rapid brain growth—and therewith of head circumference— in the perinatal period is due to glialmultiplication, myelination and dendritic growth (Dobbing, 1974). Because ofthis a catch-up growth seems possible as long as the brains continues to growat this rapid rate. Before the third trimester the fetus is relatively safe fromdeficiency by these cited causative maternal factor (Naeye et al., 1973). If thereare no other growth affecting factors —as cited under a)—, then a normal growthof the fetus can be expected in the first and second trimester of pregnancy.
A further prerequisite to the proof of a catch-up is the knowledge of normalgrowth dynamics of head circumference in the perinatal period as parameterof comparison. Conclusions from weight determinations of the brain of fetuses,infants and children —died at different ages— to growth dynamics cannot bedrawn with any accuracy since the data are —obligatory— cross-sectional.Because of this Dobbing and Sands (1973) have calculated no velocity curvesfrom their data on quantitative brain growth.
183
30 32 34 36 38 40
30 32 34 36 38 40
30 32 34 36 38 4Qimstmerlereal weeks term postrnenstrual weekS term postmenstrual weeks lern%
Head cm Supinecircumferençe 52 Length2800
2400
2000
1600
1200
10 20
biparietat diameter ±2 sdBonn Standards
thorax diameter (transversei -±2sd11
10
10 20
percentiles from Lubchenco
FIGURE 2: Weigth, head circumference and supine length after birth accordingto fetal age, small-for-gestationel age (SGA) preterm infants, special group;compared with the percentiles from Lubchenco (1963 and 1966).
cm13 -
12 -
pestmenefrued weAs pos'moosenold weil.*
FIGURE 3: Biparietal and thorax diameters of those SGA infants of the specialgroup with prenatal ultrasound examinations.
184
50: Hm! circumference
18• 1 • •
6 9 12 15months ofter term
•n•••
45-
40:
Preterm infants mean 2S 0c3AGA ogoinst C:3 SGA,speciolgroup
from 35 postmsnstrvol wesss (p.0.0005) unti11month ottor WM ( p . 0.025) +fitterence soandieelafrom 2 months ofter term f90.051until18 months (p.0.25) chttoronct not sichdiesof
35-
30 -
25-
1 ' I T -v uv-
28 32 36 40 1Postmenstruol
weeks
3
Results and discussion Contrary to reports in the literature that thereexists no catch-up growth for the brain —and
herewith the head circumference— after intrauterine growth retardation(Dobbing, 1972; Davies, 1975), such a «catch-up» of • head circumferencehas been established in our special group of at present 21 SGA preterm in-fants. Comparison is made with distance and velocity standards of headcircumference growth of normal AGA preterm and full term infants of theBonn study (Brandt, 1976).
From 35 postmentrual weeks (p < 0.0005) until one month afterterm (p < 0.025) the growth curve of head circumference of the SGA pre-term infants runs at a significantly lower level than that of the AGA; fromtwo months (p < 0.05) after term on there is no significant differente fromthe AGA preterm infants that means the SGA infants have caught Up (Fig. 4).
FIGURE 4: Head circumference growth (distance) mean and two standard de..viations. SGA preterm infants, special group, shadowed area with hatched unes,compared with AGA preterm infant, continuous une (Brandt, 1976).
Accordingly the grcrwth velocity of the special group —calculated inCM per month— from the 36th postmentrual week (p < 0.01) to the secondmonth after term (p < 0.05) is significantly higher than that of the AGApreterm and full term infantsw ith a higher and later mean peak velocityof 5.0 cm in the 36th postmentrual week; subsequently, the velocity curves
185
cm/month6 term
Head circumferencevelo city
Preterm infords,mean±1 SDE3 A G A\ \\
\ SGA , tpeciol group• \\
•N •
o129628 32 36 40 1 3
postmenstruolweeks
15 18
months ofter term
agree in their course, and from the third month on there is no significantdifferente (p < 0.05). Although this group of SGA infants is small and bete-rogeneous, the timing of the «catch-up» hat occured in all of them duringa period of very rapid growth —the spurt— of head circumference and hasbeen accomplished until the third month after term. This spurt of normalhead circumference growth extends —in accordancc with a period of rapidbrain development— from 10 weeks before until about six months afterterm (Fig. 5).
FIGURE 5: Growth velocity of head circumference, mean and one standard de-viation, calculated in cm per month. SGA preterm infants, special group, sha-dowed area with hatched unes, against AGA preterm infants, continuous une(Brandt, 1976).
The catch-up growth in this special group of SGA preterm infants hasbeen favored by the absence of other impairing factors which after birthmay continue to restrict growth such as genetic defects, malformations, ra-diations, infections or hypoxemia. Within the eight year period of the Bonnstudy there has been a quantitative change in feeding practises. Most ofthe infants with catch-up growth have got early and high caloric feecling(Weber et al., 1974). Below in figure 6 is demonstrated the mean caloricintake per kg body weight and day, the energy quotient (EQ), from thesecond to the 1 lth day of life of the SGA preterm infants with catch-up
186
Gewichts-entwicklung girog(Mittetwort) +30-
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Energie-quotient EO(Nittelerr1) 130
110 ..••••••"'"'
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30
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FIGURE 6: Aboye: Mean weight velocity in g per day; below: mean calorie intakePer kg body weight and day, the energy quotient (EQ) from the second to thellth day of life. Dotted une = SGA preterm infants with catch-up growth (groupA), n = 21; solid line --= SGA preterm infants without catch-up growth (group B),n =--- 22.
(group A), dotted une, compared with the SGA infants without catch-upgrowth (group B), solid Ene, and aboye the weight velocity in g per day.The mean of the SGA infants with catch-up growth has started to put onweight at the second postnatal day contrary to the other SGA of the study(group B) without catch-up, who started to put on weight on an averageat the 9th day. Catch-up growth requires energy (Forbes, 1974), and sincegrowth velocity must exceed normal throughout the entire recovery periodfood must be provided in excess of normal requirements until recoveryIS complete.
There is still some controversy about optimal caloric intake of verySmall SGA preterm infants. The high-caloric feeding was tolerated verygood by the infants in the Bonn study.
Better than in mean curves the timing and extent of intrauterine re-tardation and of postnatal catch-up growth in head circumference aredemonstrated in a combined chart of the individual development of a SGApreterm girl, born in the 37th postmenstrual week with a birthweight of1280 g (figure 7). Aboye are plotted the intrauterine ultrasound measure-ments of the biparietal arid thorax diameter against the Bonn standardsfrom Hansmann (1974). The curve of the biparietal diameter runs in therange of two standard deviations below the mean, whereas the curve ofthe thorax —more affected by intrauterine restriction— is markedly below
1. 2.4.
•5. 6.
•7. 8. • 9. • 10.
187
Thorax diameter± 2S0
13
12
11
10
9
8
6
5
4
3
2
Biparietat diameter±2 SO
cm
13
12
11
10
9
e7
6
5
4
3
2
cm
2Q 30postmenstruol weeks
20 30postmenstruol weeks
Hm! círcumference± 2S0
45
35
25
CM
28 32 36 40 1 3 6postmenstruot months ofter termweekt
28 32 36 40 ; ' 3 6postmenstruol
months after termweekt
cm/month6E
Head círcumferencevelocity tim
two standard deviations. Underneath in the graph are plotted the postnatalmeasurements of head circumference against the Bonn standards (Brandt,1976). At birth the growth curve starts markedly below two standard
FIGURE 7: Combined chart of the development of a SGA infant, born in the37th postmentrual week with a birth weight of 1280 g. Aboye ultrasound measu-rements of intrauterine growth of biparietal and thorax diameter, plotted againstthe Bonn standard (Hansmann, 1974). Below postnatal measurements of headcircumference (distance and velocity), plotted against the Bonn standards forAGA preterm and fullterm infants (Brandt, 1976).
188
postmenstruol weeks20 25 30 35 40 20 25 30 35 40
postmenstrual weeks
Thorax diameter± 2 SD
2 -1
•altli11.1•11111a1.14
electivecesa nonsec tion
211•111 I .11••./....1,
cm/moMh6
cm
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Biparietal diameter 12i SD 11
•10
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8
6
cm
11lo
9
765
Heod circumference± 2 SO
45
40
35
30 1
25
Head circumferencevelocity ± 1 SO
deviations and —after a period of very rapid growth— reaches the normalrange in the third month after term. The catch-up is evident by the highvelocity with a right-shifted peak of 4.8 cm in the 40th postmenstrual week,compared to a mean velocity of 3.0 cm. On the photo in figure 5 the littleginl is to be seen at the chronological age eight days and of 13 months.
The next combined chart (figure 8) shows the catch-up growth of
28 32 36 40 1 3 6 9 28 32 36 40 1 3 6"Itmenstr" months ofter term postme r.: 1 0 uol montht ofter termweeks weeks
FIGURE 8: Combined chart of the development of a SGA infant, born in the341h postmentrual week with a birth weight of 1130 g. Aboye ultrasound measu-rements of intrauterine growth of biparietal and thorax diameter, plotted againsttue Bonn standards (Hansmann, 1974). Below postnatal measurements of headcircumference (distance and velocity), plotted against the Bonn standards forAGA preterm and fullterm infants (Brandt, 1976).
5
elective 4cesorion
3 section 3
189
NOMMUMNIM»MUMMOMMOINMONONIMMMUMM,
1. 2. 4. 5. 6. Z 8.doy s ofter birth
another SGA preterm gin, born in the 34th postmenstrual week by electiveCesarean section with a birthweight of 1130 g. Aboye are plotted the intra-uterine ultrasound measurements of the biparietal and thorax diameteragainst the Bonn standards from Hansmann (1974). The growth retarda-
Eierneaen(Ec)
weigtevelocit y gmay
+60
.+50+40
+30
+20
+10
cal/ kg/doy160
—20—30-ao-50
-60
20
o
AM%
1MIMMIMMMMMIMMMMIMM MMMMMMM MMMMMIMMMMMMMMMMMMMMMMMMWIMMMMMMIMMMMMMMMIMIMIMMIMMMMIMIMMUMMMMMMMMMMMMMMM MMM MMMMMMMMMMMMMMMMMMMIMMMMMMMMMMIMIMMMMMM MMMMMMMMM MMMMMMMMMMMM MMM
140
120
100
80
60
40
o—10
4. 5. 6. 7. 8 9. 10. 11.dayt ofter birth
FIGURE 9: Weight velocity in g per day and the calories per kg and day, theenergy quotient (EO) in the first eleven days after birth of the gin in fig. 8.
190
CATCH-UP GROWTH OF HEAD C I RCUMFERENCE IN MONOZYGOTIC TWENS
Gestation(weeks)
Birthweightdifference
Difference of
at birthhead circumference
at 6 monttisSGA to AGA twin
at 12 meiths
34 14% -5 cm +0,1 cm 0 cm
37 25% cm +0,1 cm +0,1 cm
35 31% -2,5 cm +0,2 cm +0,5 cm
Pair I twin I SGA
twin 11 AGA
Pair 2 twin 11 SGA
Pair 3 twin 11 SGA
twin I AGA
twin I AGA
tion —starting beyond 28 weeks— is clearly to be seen in both parameters.At birth the growth curve starts more than two standard deviations belowthe mean and reaches the normal range at one month after term. Thiseatch-up is evident by the high velocity with a peak of 5.8 cm in the 37thpostmenstrual week, compared to a mean velocity of 3.7 cm. Figure 9Shows the weight velocity in g per day and the calories per kg and day,the energy quotient in the first 11 days after birth of the little ginl infigure 8.
Further evidence for catch-up comes from the head circumferencegrowth of monozygotic twins (Table I): in three pairs who differed in birth-weight 14 per cent, 25 per cent and 31 per cent, the smaller SGA membermakes up a difference in head circumference at birth of 1.5 cm, 2.0 cm and2.5 cm respectively before the sixth month. In height and weight there arestill growth differences between these twins.
VIELE N.° 1: Evidence for catch-up from the head circumference growthof monozygotic twins.
The SGA infants with catch-up growth show also in their mental deve-loprnent till now better results than the other SGA of the Bonn study (fi-gure 10), their developmental quotients (Griffiths, 1964; Stanford-Binet ofTerman et al., 1965) agree with those of the AGA preterm and full terminfants (Brandt, et al., 1976).
191
********** *********
* ********* .......... ..... .. •••••••••••"..
nn••• Mongelgeboreee, Gruppe A 1 von 3 bis 21 MonoteUnterschied signifikont
••••••• Mangelgeborene, Gruppe 8 J p«0,0025
Frühgeboren.
Durchschnitt!. Entwicklungskurven nach GriffithsEO
korrigiertes Alter
12 15 18 21Monote
FIGURE 10: Monthly mean developmental quotients (DO Griffiths) from 3 to 21months, corrected age. • •e••tee SGA preterm infants with catch-up growth„n 21, AGA preterm infants, n — 64, SGA preterm in-fants without catch-up growth, n -= 22.
Resumen La autora presenta el «catch-up growth» del perímetro craneal—parámetro reconocido para valorar el desarrollo cerebral—
en el período perinatal tras un retraso del crecimiento intrauterino. Tam-bién se analizan las causas que motivaron el citado «catch-up».
Summary The author report on «catch-up» growth of head circumferen-ce —a recognized parameter, for brain development— in the
perinatal period after intrauterine growth retardation, and she will try toanalyse the causes of this «catch-up».
150
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100
so
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