Camp. Biochem. Physiol. Vol. IOZA, No. 3, pp. 585-590, 1992

03Ot-h9629/92 SS.00 + 0.00 0 1992 Pergamon Pmss Ltd

Printed in Great Britain

EFFECTS OF EXERCISE AND FOOD RESTRICTION IN PREGNANT AND NEWBORN RATS. PRE-PREGNANCY MAXIMUM OXYGEN CONSUMPTION Jest G. PERALES,*FRANCY R. S. PATRICIO,*OLGA M. S. AMANCIO,* IVAN C. PIC,umo,t LUIZ 0. C. RoDRIGmt

and ADRIANA K.

Russot$

TDepartamento de Fisiologia e *Departamento de Pediatria, Escola Paulista de Medicina, Caixa Postal 20393, 04034 Sgo Paulo-SP, Brasil. Fax: 1I-549-2127 (Received 24 October 1991) Abstract-l. In the present study, the effects of exercise and food restriction in pregnant and newborn rats were investigated. 2. The following groups were formed: adequate food supply, with and without exercise (AE and AN) and 30% food restriction, with and without exercise (RE and RN). 3. Exercise was performed throughout the pregnancy on a treadmill at a speed of 18m/min for 30 min/day, which represented 84% of maximum V,, . 4. The results show that food restriction affected body weight gain while exercise only affected the RE group (P < 0.05). 5. Body temperature was increased by exercise. The initial temperature was lower in group RE. 6. No differences were obtained in average offspring number but reabsorption, preterm and natimortality were observed in group RE. 7. Newborn body weight was lowered by food restriction rather than by exercise. 8. Newborn brain and heart weights were not affected but lung and liver weights were significantly affected by the nutritional factor (P < 0.05).

INTRODUaON The

first observations of the influence of physical activity on maternal and fetus health appeared at the end of the last century when, in 1895, Pinard suggested the benefits of resting during the last period of pregnancy (Briend, 1980). In the last two decades several papers have dealt with exercise and pregnancy in women. Some suggest good effects of exercise either for the mother or for the offspring (Zaharieva, 1972; Erkkola, 1976a; Erdelyi, 1962); others have shown reduced weight gains in mothers and lower body weights of offspring (Alegre et al., 1984; Rodrigues-Escudero et al., 1980; Clapp and Dickstein, 1984). The deleterious effects were more evident during the last 3 months of pregnancy, correlating with greater premature birth and placenta-infarction figures, which suggests a reduction in uterus-placenta blood flow during exercise (Naeye and Petters, 1982). Several species of animals subjected to different levels of exercise during pregnancy exhibited reduced body weight gains and newborn body weights and greater fetal or newborn mortality rates (Lotgering et al., 1985; Gorski, 1985). Several factors such as species, age, weight, health condition, type of exercise, relative exercise load and nutritional status of the mother may influence the exercising mother or newborn. SCorrespondence should be addressed to Dra. Adriana Kowaleslcy Russo, Departamento de Fisiologia, Escola Paulista de Medicina, Rua Botucatu, no 862-5’ andar, 04023 SBo Paulo-SP, Brasil.

Most of the studies have not taken into account the maximum oxygen consumption ( Vs max) or utilized the absolute work load which makes comparisons of results difficult. There are few papers that correlate exercise at relative work loads and calorie-protein deficiency in pregnant animals. This study was performed to evaluate some variables of the mother and offspring associated with exercise and food restriction. The methods employed investigate interactions between these factors. MATElUAU AND METHODS This study was performed at the Laboratories of Exercise Physiology and Pediatric Research of Escola Paulista de Medicina, SBo Paul0 at an altitude of 76Om, approx. 80% relative humidity and mean annual temperature of 18°C. Wistar rats were used, which came to the laboratory at 70 days of age. They were fed ad lib. a stock diet (Purina, Brasil) and kept in 12 hr : 12 hr light : dark cycle (lights on at 7:00 a.m.). The cages were kept at 24°C. Female rats were subjected to a training period in order to verify which ones adapted themselves to run in a treadmill for 5 min at a speed of 12 m/min, 0” slope. This was done 5 days a week until the animal reached 90 days of age, the age of reproductive maturation, and a body wt of 180-220 g, Rats which did not present a good performance were not studied further. Brooks and White method (Brooks and White, 1978) was used to evaluate V, max, whereby animals are stimulated to run and O2 consumption and CO, production are measured. The last two variables were measured using Beckman OM-11 and LB-2 equipment. The electrical stimulus was abolished during pregnancy. The ergometric test was 585

586

J& G. F’ERALES et al. Table I. Food

Exercise

Adequate Adequate Restricted Restricted

Name AN AE RN RE

Without With Without With

continuous, with progressive loads represented by an increase in speed of 5 m/min every 3 tnin until exhaustion. 0, consumption at each work load was expressed in STPD

terms and was calculated from O1 and CO, percentages and flow rate which was set at 5 l/mm. After the training period and V,, max measurements, the rats were housed with males and copulation was confirmed by visualization of spermatozoids in the vaginal spread. They were then randomly assigned to experimental groups. The day of copulation was considered as day 0 of pregnancy. The groups were formed as indicated in Table 1. Groups AN and AE received a stock diet (Purina, Brasil) and 23% protein ad lib. and groups RN and RE received 13 g per day of the same diet, which corresponded to approx. 2/3 of the normal feed intake of a pregnant rat. Water was given ad lib. for all groups. The exercise intensity for AE and RE groups corresponded to 18 m/min for 30 mm from day 0 to day 20 of pregnancy,‘which represented about 84% of V,,, max for all animals. Body weights of pregnant rats were recorded daily on an Ohaus (model 119s) balance. Rectal temperature was measured before and after each exercise period. On the 21st day of pregnancy, the offspring were removed by surgery (referred to as newborn groups corresponding to mothers), weighed, separated by sex and killed for tissue weight recordings. After fresh weighing, the tissues were dried in an oven at 120°C for 2&22 hr and the dry weight was obtained. The difference between both weights was considered as the water present in the tissues. For these weighings a Sauter (model 424) analytical balance was used.

The statistical procedure included multi-factorial analysis of variance and the least significant difference or LSD-for variables with normal distribution and Kruskal-Wallis for frequencies (Morrison, 1967; Sokal and Rolhf, 1969). The rejection of null hypothesis was set at P < 0.05. RESULTS

No differences in V,,max were obtained between AE and RE groups (Table 2). Table 2 also shows that exercise significantly changed body temperature of exercised groups (AE and RE). Although food restriction lowered body temperature before exercise, the temperature gain

after exercise was similar in restricted and nonrestricted groups. No differences in pregnant initial body weight were detected. Nevertheless, the final body weight was significantly lower than control body weight in group RE, which suggests a synergistic action of food restriction and exercise. Furthermore, exercise showed a tendency to reduce the final period of pregnancy in the AE group when compared to control (Table 2, Fig. 1). However, group RE initial body weight was unchanged during the anabolic phase with the increase occurring only in the final catabolic phase (Fig. 1). Exercise and level of food intake did not influence the number of offspring (Table 3). Offspring body weight was significantly lower in group RN and there was a further non-significant decrease in group RE compared to group AE. Exercise itself did not interfere with newborn body weight. The female newborn had a lower body wt (7%) than the male newborn (Table 3). Table 3 shows that neither nutrition nor exercise affected brain and heart fresh weights in the newborn. However, lung and liver weights were lower in the restricted groups (RN and RE). In group AG there was a slight but non-significant increase in lung weight. The same results were true for the dry weights of each organ (Table 4).

DISCUSSION

Comparison of the present results with those in the literature, once the absolute work loads have been used, is difficult if the aerobic capacity of animals is not considered. Exercise significantly affected pregnant body weight gain in group RE; this was probably due to an inadequate nutrient flow for energy utilization during exercise. This was in evidence from the first phase of pregnancy. In group AE, which had a greater metabolic reserve, exercise only tended to al&t body weight in the last phase of pregnancy. It has been shown that light exercise does not atfect body weight gain during pregnancy (Parizkova, 1975; Shima, 1990) while moderate and hard exercise cause a decrease (Mottola ef al., 1983, 1986) which is evident from the beginning of pregnancy; however, another study reported a sign&ant decrease in body weight gain only from the 12th day (Treadway et al., 1986). According to Mottola et al. (1986), exercise mobilizes

Table 2. Mean values and standard deviation of Oa consumption (V,), rectal temperature (RT), pregnant body weight (WV) Groups AN

AE

RN

m

-

-

Kbf

*

15.21 f 14.5 64.9 f 14.0

b

-

a

-

37.5 f 0.1 38.6 f 0.2’

-

37.3 f 0.2t 38.5 f 0.3.

Variables

“02 RT

RE 12.3 63.8 f 8.7

i 198.8 f 8.9 198.6 f 9.5 198.5 f 10.6 200.1 f 8.6 261.4 f 12.87 245.3 f l9.O.t 303.7 f 16.1 290.4 f 18.8 f AE and AN-adequate food supply with and without exercise; RE aad RN-food ratricted with and without exercise; m -maximum v, (mljkg/min); r--V, of exercise performed (ml/kJmin); b and a-tetnpemtttres before and after exercise CC); f and/-initial and final

PW

pregnaat body weight (8).

P -z0.05:*exercise, tfood restriction.

Exercise and food restriction 2

310&

E .F

290

--

270

--

230

--

s

3

6

9

12

15

16

t 21

Days of Pregnancy

Fig. 1. Mean body weight (g) of rats during pregnancy AE and AN-adequate food intake with and without exercise; RE and RN-food restricted with and without exercise. P < 0.05; *exercise and +food restriction.

lipids as an energy source, as shown by decreased lipids in the carcass of eutrophic pregnant rats. Malnourished and exercised rats during the last f of pregnancy did not show a reduction in body weight gain but there was a reduction in carcass lipids and an increase in protein (Shima, 1990). Undernourished women subjected to heavy exercise showed a lower body weight gain than those subjected to light exercise during pregnancy (Tafari et al., 1980). Although no differences in the number of offspring produced between groups were seen, during this study two cases of fetal reabsorption, one dead newborn and birth anticipation in five animals were observed, all in group RE, suggesting that hard exercise and food restriction can cause sufficient stress to induce preparturition and natimortality. Light and moderate exercise were reported not to interfere with offspring number (Parizkova, 1975; Parizkova and Petrasek, 1978; Mottola et al., 1983), while hard exercise causes a decrease (Garris et al., 1985). Also, birth and perinatal deaths was reported to increase after hard exercise (Wilson and Gisolfi, 1980). Shima (1990) did not observe a difference in offspring number for pregnant rats which were subjected to light exercise and 55% food restriction during the last j of pregnancy. The pioneer paper of Pinard in 1895 noted a reduction of newborn weight, preparturition and greater neonatal mortality in mothers who did not rest in the final stage of pregnancy (Briend, 1980). Several papers have shown that in pregnant rats subjected to light or moderate exercise, no body weight reduction occurred in the newborn (Blake and

Hazelwood, 1971; Parizkova, 1975, 1978; Parizkova and Petrisek, 1978; Jenkins and Cicconne, 1980; Mottola et al., 1983). However, the same work load was shown to provoke body weight reduction, greater mortality and a delay in ossification (Terada, 1974). Hard exercise (SO-88% Vo, max) evoked greater mortality at birth and neonatal period which suggests lower body weight of the newborn (Wilson and Gisolfi, 1980) while others did not detect any changes (Mottola et al., 1986; Treadway et al., 1986). On the other hand, exercise performed during the second half and the whole pregnancy period caused greater fetal mortality and heavier survivors (Garris et al., 1985). Thus, the deleterious effects of exercise are greater in late pregnancy, as also occurs in women (Naeye and Petters, 1982; Clapp and Dickstein, 1984). In other species of animals, moderate and hard exercise during pregnancy induced either a reduction in fetal weight (Dhindsa et al., 1978; Longo et al., 1978) or no alteration (Gilbert et al., 1979; Hohimer et al., 1984). Malnutrition is correlated with a decrease in newborn body weight. Protein-calorie deprivation (50%) during pregnancy induces a lO-30% decrease in fetal weight (Ahokas et al., 1984; Fernandes et al., 1985; Rosso and Kava, 1980; Villescas et al., 1981). Chronic (Araya et al., 1978, 1986; Araya and Ruz, 1981) and severe protein deprivation when pregnant (Tonete et al., 1983a,b) induced stronger effects on newborn body weight. Shima (1990), in malnourished pregnant rats subjected to light exercise, showed heavier fetuses than controls, suggesting a favorable effect of exercise,

Table 3. Mean values and standard deviation of newborn body weight (NW) and number of offspring (N) Groups Variable MW

n

ma f@ N

AN

AE

RN

RE

4.72 + 0.3 4.85 * 0.2 4.60 * 0.4*

4.53 * 0.5 4.68 f 0.4 4.38 f 0.5.

4.31 * 0.37 4.45 f 0.2 4.17 f 0.2.

4.28 f 0.5t 4.41 f 0.4 4.15 f 0.58

10.9

11.2

11.3

10.0

AE and AN-adequate alimentation with and without exercise; RE and RN-food restricted with and without exercise; n-total body weight of offspring; ma and&-male and female body weight of offspring. P c 0.05; *sex, tfood restriction.

Jc& G. PEIULES et al.

588 Tabk

4. Mean values of fresh and dry tissue weights from newborn

(mg)

Groups AN

AE

RN

RE

Brain

fresh dry

191.0 f 10.5 24.4 f 5.2

191.0 f 16.7 21.8 * 2.4

185.8 f 21.7 21.1 f 2.3

181.0 k 37.7 22.0 f I .9

Lung

fresh dry

142.5 + 35.0 20.0 f 3.5

159.0 + 23.8 21.9 f 10.6

140.8 f 19.1’ 17.4 f 2.29

136.7 f 26.5. 16.4 k 4.0.

Heart

fresh dry

26.5 f 3.9 4.3 + 1.2

26.9 f 3.4 4.1 f0.6

26.6 ? 6.9 4.0 f 0.8

25.6 5 3.8 4.2 + 1.2

Liver

fresh dry

338.2 f 41.2 79.8 f 11.2

311.1 k44.4 71.0 * 10.1

292.6 * 39.9. 63.3 f 10.2.

291.2 k 38.5. 65.9 * 8.5’

Variable

AE and AN-adequate food intake with and without exercise; RE and RN-food and without exercise. P i 0.05; ‘food restriction.

probably due to maternal lipid mobilization. However, hard work in malnourished pregnant women in Ethiopia reduced newborn weight (Tafari et al., 1980). Lotgering et al. (1984) suggested that maternal exercise does not represent stress or hypoxia for the fetuses and the slight weight reductions observed are the consequence of maternal physiological adaptations still unknown. Our results have shown that newborn body weight was affected by the level of the food intake and not by exercise, suggesting the possibility that some maternal unknown adaptive mechanism occurs in order to protect the fetus from damage to the pregnant mother. Jenkins and Ciconne (1980) did not find modifications either in weight or in biochemistry of newborn brains from pregnant rats subjected to light moderate exercise. An increase in brain weight was reported by Shima (1990). In guinea pigs, moderate and hard exercise did not lead to a decrease in brain weight, although placental and fetal weights decreased, suggesting a protection of brain tissue (Gilbert et al., 1979; Nelson et al., 1983). In humans, undernutrition leads to impairment of the fetal brain (Zamenhof et al., 1968; Winick and Rosso, 1969; Naeye et al., 1973) leading to mental retardation and lower intellectual performance (Cravioto et al., 1966; Nobrega, 1974; Parizkov$ 1975). Shima (1990) observed a tendency to an increased brain weight in undernourished and exercised group, increased DNA and protein content and decreased RNA, which suggests the utilization of fatty acids for fetal brain growth (Battaglia and Meschia, 1978). It is also possible that exercise could improve ketone body utilization as an energy source (Tafari et al., 1980). Our results show that brain weight was not affected by the variables studied. A better blood distribution in detriment of other organs could be one possible explanation, although morphological and physiological modifications cannot be discarded. As far as the lung is concerned several papers show the effects of prenatal undernutrition on its biochemistry and weight in the newborn (Naeye et al., 1973; Diaz de1 Castillo, 1975; Winick, 1970). Our results co&m a lower lung weight in the newborn. Neither exercise nor food restriction led to alterations in newborn heart weight. The same was shown by Parizkova (1975) with a light exercise, although this author has detected an increase in capillaries and muscle fibers per unit of area and also in the ratio

restricted with

capillary : fiber. Nevertheless, hard exercise did not evoke any heart alterations (Wilson and Gisolfi, 1980). In guinea pigs, moderate and hard exercise decreased the fetal heart weight (Gilbert et al., 1979; Nelson et al., 1983). Intra-uterus undernutrition was reported to modify weight, morphology and biochemistry of the fetal heart (Naeye, 1965; Naeye et al., 1973; Winick, 1970). No reports on the effect of exercise and food restriction were found. The liver weight was affected by food restriction and not by exercise. The organ most affected by undernutrition is the liver, together with the adrenal glands, both in humans and animals (Naeye et al., 1973; Diaz de1 Castillo, 1975; Roeder and Chow, 1972; Winick, 1970; Tonete, 1990). Parizkovi and Petrasek (1978) reported significant metabolic alterations in the liver of newborns from eutrophic exercised rats. In this paper it was observed that the exercise did not impair the weight of these organs. The dry weight of the organs showed that neither exercise nor food restriction interfered with water content of the tissues studied. V,, max was obtained by increasing work load until exhaustion. It depends on cardiovascular, respiratory and metabolic conditions, as shown in humans (Mitchell and Blomqvist, 1971; Astrand and Rodahl, 1977), rats (Brooks and White, 1978; Shepherd and Gollnick, 1976) and pigs (C&one et al., 1982). The results obtained in this paper are similar to other reported values (Pasquis et al., 1970; Wilson and Gisolfi, 1980; Conley et al., 1985; Bedford et al., 1979). Higher values have also been reported (Shepherd and Gollnick, 1976; Brooks and White, 1978). The differences may be the consequence of differences in species, sex, training status, test duration and equipment sensibility. Food restriction induced a lower rectal temperature before exercise, probably due to the reduced adipose tissue in group RE. There is a lack of data to analyse exercise, undernutrition and pregnant temperature (Metcalfe e? al., 1984). There is concern that exercise in pregnant women could lead to hyperthermia with consequences on the fetuses (Schaefer, 1979; Gorski, 1985; Lotgering et al., 1985), mainly during the first 3 months of pregnancy (Maeder, 1985; Dale, 1987). In pregnant guinea pigs and rats subjected to high temperatures, microcephaly and skeletal muscle defects were reported (Edwards, 1967, 1968, 1974; Hensleigh and Johnson, 1971). On the other hand, exercise in pregnant women and sheep

Exercise and fc)od restriction

does not affect fetuses even with the thermal load imposed (Jones et al., 1985; Lotgering et al., 1983b). Our results agree with this hypothesis since, although the exercise increased rectal temperature, no apparent malformations were seen. The results presented in this paper that exercise affects the pregnant rat under food restriction, a synergistic action of exercise and food restriction on mother-newborn was achieved. Reductions in pregnant body weight gain, fetal reabsorption, newborn mortality and premature births were observed. Biochemical studies on carcass and plasma from mother and newborn are required in order to examine further observed effects and also to study the offspring development. Acknowledgements-The

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