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COMPOSITION OF BLOOD PLASMA (Calcium,Phosphorus, Magnesium, Proteins) DURING THE

NEONATAL PERIOD IN THE CALF. INFLUENCEOF THE STATE OF HEALTH

G. Cabello, M.C. Michel, Christiane Foucher, C. Lafarge

To cite this version:G. Cabello, M.C. Michel, Christiane Foucher, C. Lafarge. COMPOSITION OF BLOOD PLASMA(Calcium, Phosphorus, Magnesium, Proteins) DURING THE NEONATAL PERIOD IN THE CALF.INFLUENCE OF THE STATE OF HEALTH. Annales de Recherches Vétérinaires, INRA Editions,1977, 8 (3), pp.203-211. �hal-00900931�

COMPOSITION OF BLOOD PLASMA (Calcium, Phosphorus, Magnesium,Proteins) DURING THE NEONATAL PERIOD IN THE CALF.

INFLUENCE OF THE STATE OF HEALTH.

G. CABELLO M.C. MICHEL

Christiane Foucher C. Lafarge.

I.N,R.A., Laboratoire des maladies métaboliques, C.R.V.Z. de Theix, 63110 BEAUMONT, (France)

Résumé

COMPOSITION DU PLASMA SANGUIN (Calcium, Phosphore, Magnésium, Protéines) PEN-DANT LA PERIODE NEONATALE CHEZ LE VEAU. INFLUENCE DE L’ETAT DE SANTE. ―L’évolution de la concentration plasmatique de calcium, phosphore minéral, magnésium etde quelques fractions protéiques a été étudiéede la naissance à l’âge de 20 jours chez 68veaux. 32 animaux restèrent en bonne santé tandis que 36 eurent de la diarrhée mais sur-vécurent. Dès la naissance, les veaux qui seront malades ou non étaient différents du pointde vue biochimique. Tout au long de la période étudiée, la calcémie, la phosphorémie etl’albuminémie des veaux qui subissent des diarrhées et qui survivent étaient systématique-ment inférieures à celles mesurées chez les animaux qui ne présentent pas de symptô-mes pathologiques. De plus, après l’ingestion de colostrum, l’augmentation des protéinestotales et des globulines était beaucoup plus faible chez les veaux ultérieurement maladesque chez les veaux sains. Les causes possibles de ces anomalies et leur rôle éventuel surl’apparition de la pathologie sont discutés.

Introduction

Although there has been much work oncalf pathology (study of infectious etiology,modifications of blood composition causedby diarrhea, effects of the nutritional and

pathologic states of the mother during preg-nancy on calf health, etc.) further knowledgeis required of the pre-existing differences bet-ween animals which will show disease symp-toms and those that remain healthy in thesame herd.A study was undertaken of the evolution

of plasma composition in healthy and diarr-heic calves, to obtain a better understandingof the factors which cause morbidity.

Materials and methods

1. Animals .

Blood samples were taken from sixty eightFriesian or Holstein X Friesian calves of thesame herd born between November 1973 and

January 1974. No breed difference could beshown. The percentage of mortality obser-ved in this herd was low (less than 4 %) but36 of the 68 animals suffered from diarrheabetween 5 and 11 days of age; all the sickcalves survived.These animals received maternal colostrum

for 24 to 36 hours and then were kept in

open stabulation with an artificial milk diet

2. Blood samplingBlood samples were taken each day at

9 a.m. up to 11 days of age and then at 15

and 20 days. Heparinized blood sampleswere obtained by puncture of a jugular vein.Plasma was separated by centrifugationwithin 15 minutes and frozen at -20 °C until

analysis.

3. Analytical methods

Plasma calcium and magnesium were mea-sured .by atomic absorption spectrophotome-try using a Perkin Elmer 303 apparatus afterdilution of plasma to 1/50th in desionizedwater.

Phosphatemia was determined by a colori-metric method developped by Michel (1971)with a Technicon autoanalyzer.The total protein concentration in plasma

was measured by the biuret colorimetricreaction, also using a Technicon autoanaly-zer (Michel, unpublished). A protein solu-tion to which copper and sodium sulphatesare added gives a stable violet colorationdue to peptide linkages - NH - CO-. The

intensity of this colour, read at 550 nm, is

proportional to the protein concentration.Albuminemia was measured by a colori-

metric reaction with bromocresol green usinga Technicon autoanalyzer (Michel, unpu-blished ; details of these methods are avai-lable on request). Addition of bromocresol

green at pH 3,6 to an albumin solution givesa green coloration, the intensity of whichread at 550 nm is proportional to the albuminconcentration.Plasma globulin concentration was estima-

ted by the difference between total proteinsand albumins.

Results

1. Plasma calcium variations (fig. 1 JThe calcemia of healthy animals was high

at birth (12.91 ± 0.28 mg/100 ml) then decrea-sed up to 15 days of age, when it reachedthe minimum value (P < 0.005) of 11.59 ±0.29 mg/100 ml.

There was a comparable change in diarr-heic animals : plasma calcium decreasedfrom birth (12.31 ± 0.22 mg/100 ml) up to11 days of age, when it was significantlylower (11.09 ± 0.36 mg/100 ml, P < 0.005).An analysis of variance of all calcemia

(healthy and diarrheic calves during 20 days)showed that variations in concentration bet-ween days were significant (F = 3.66 for

14 and 373 d.f., P < 0.01) and that plasmacalcium concentration was highest in healthycalves (F = 18.78 for 14 and 373 d.f., P <

0.01). This difference between diarrheiccalves and controls remained almost constant

during the period under study (Interactionnot significant, F = 0.45 for 14 and 373 d.f.).

2. Plasma phosphate variations (fig. 2)In healthy animals, the plasma concentra-

tion of mineral phosphorus decreased signi-ficantly (,P < 0.025) between days 1 (7.75± 0.20 mg/100 ml) and 5 (7.01 ± 0.73 mg/100 ml). During the period when the sickcalves showed diarrhea (days 5 to 11), the

phosphatemia of healthy animals increasedbetween days 5 (7.01 ± 0.73 mg/100 ml)and 8 (8.18 ± 0.40 mg/100 ml, P < 0.025).During the period under study, the phospha-temia increased significantly from birth (7.27± 0.27 mg/100 ml) to 20 days (8.55 ± 0.44mg/100 ml, P < 0.025).There were parallel variations of plasma

phosphate in diarrheic animals. As in heal-

thy calves, the phosphatemia increased si-

gnificantly from birth (6.29 ± 0.23 mg/100ml) to 20 days (7.38 ± 0.25 mg/100 ml, P <0.005).The concentration of inorganic phosphorus

in diarrheic calves was always lower thanthat of healthy animals, from birth to 20

days of age. The differences were signifi-cant during the first 24 hours (P < 0.01)and at 1 day, 3 days, 8 days (P < 0.05), 10days, 20 days (P < 0.025) and 15 days(P < 0.005).When groups of calves were constitued

on the basis of phosphatemia value at birth,it appeared that 72 % of the animals forwhich this concentration was lower than7 mg/100 ml showed diarrhea during thenext days.Only 26 % of the calves for which this

concentration was higher than this value

developed pathology. These figures differsignificantly (x2 = 3.91, P < 0.05).

3. Plasma magnesium variations (fig. 3)

The magnesemia of healthy animals was

high at birth (2.13 ± 0.10 mg/100 ml) andthen decreased progressively up till day 11,when it was significantly lower (1.75 ± 0.07mg/100 ml, P < 0.025). There was a similar

change in diarrheic calves from birth (1.96 ±0.04 mg/100 ml) to day 15 (1.69 ± 0.004 mg/100 ml, P < 0.005).The level of plasma magnesium in sick

calves was significantly lower during day1 (1.89 ± 0.04 mg/100 ml) than that of thehealthy animals (2.26 ± 0.11 mg/100 ml,P < 0.001 ).

4. Plasma total proteins variations (fig. 4)

Influenced by intake of colostrum, theplasma level of total proteins in healthy cal-ves increased from 5.40 ± 0.29 gl100 ml atbirth to 7.04 ± 0.49 g/100 ml at day 1 and7.66 ± 0.71 g/100 ml at day 2, the differencesbeing significant (P < 0.005). Then, there

was a regular fall in the value of this para-meter up to day 5, when it reached 5.79 ±0.38 g/100 ml, significantly lower than at

day 2 (P < 0.025).The effect of colostrum intake on the pro-

teinemia of the calves which will suffer from°

diarrhea was much smaller, although the

plasma proteins level increased from 5.00 ±0.15 g/100 ml at birth to 6.10 ± 0.26 g/100ml at day 2 (P < 0.001). Thus, the protei-nemia of the calves which will suffer fromdiarrhea was lower than that of the healthycalves during days 1 (P < 0.025) and 2

(P < 0.05).During the period when the sick calves

developed diarrhea (days 5 to 11), the pro-teinemia of healthy animals increased bet-ween days 5 (5.79 ± 0.38 g/100 ml), and 9(6.87 ± 0.38 g/100 ml) and then decreasedsignificantly until day 11 (5.88 ± 0.26 g/100ml, P < 0.05). Such variation did not occurin sick calves.

5. Plasma globulins variations (fig. 5)

Colostrum intake also caused an increasein the blood globulin level in healthy calvesfrom birth (2.88 ± 0.36 g/100 ml) to days 1

(4.72 ± 5.58 g/100 ml, P < 0.01) and 2 (5.52± 0.80 g/100 ml, P < 0.005).Then, the globulinemia dropped signifi-

cantly until day 5 (3.25 ± 0.36 g/100 ml,P < 0.01). ).As for total proteins, the sick calves sho-

wed a smaller variation, from 2.73 ± 0.10

g/100 ml at birth to 3.21 ± 0.25 g/100 ml

at day 1 and 3.56 ± 0.17 g/100 ml at day 2(P < 0.01). This increase continued until

day 4 (3.86 ± 0.19 g/100 ml). Thus, the

globulinemia of the sick animals was signi-ficantly lower than that of the healthy calvesduring days 1 (P < 0.01) and 2 (P < 0.025).

During days 5 to 11, when diarrhea was

apparent in sick calves, the globulinemia ofhealthy calves increased between days 5

(3.25 ± 0.36 g/100 ml) and 9 (4.12 ± 0.35

g/100 ml) then decreased significantly until

day 11 (3.28 ± 0.19 g/100 mi, P < 0.05). In

diarrheic calves, there was no such change.

6. Plasma albumin evolution (fig. 6)The blood albumin concentration increa-

sed during the first three weeks of life, in

healthy calves, from 2.61 ± 0.09 g/100 mlat birth to 3.05 ± 0.21 g/100 ml at 20 days(P < 0.05) and in sick animals, from 2.27 ±0.09 g/100 ml to 2.56 ± 0.10 g/100 ml in thesame period (P < 0.025).

Except in day 2, the albuminemia of diarr-heic animals was always lower than that of

healthy calves, up to 20 days of age. Thedifference was significant on days 0, 8, 20

(P < 0.025), 3 (P < 0.005), 7 and 15 (P <0.05).

Of 27 animals with a plasma level ofalbumin a birth lower than 2.42 g/100 ml,24 suffered from scours (74 %). Only 6 ofthe 21 calves with a higher albuminemia atbirth became sick (28.6 %). The composi-tion of the two groups differed significantly(X2 = 4.3, P < 0.05).

Discussion

1. Validity of the results1.1. At birth

It is well known that, in cattle, the foetaland postnatal calcemia and phosphatemiaare high compared with those of adult ani-!mals. Sato (1933) found a plasma calciumconcentration of 15.9 mg/100 ml in calvesfoetus during the last 4 months of gestation.At birth, Barlet et al. (1971) observed acalcemia of 11.2 mg/100 ml and a phospha-temia of 7.2 mg/100 ml, while Robinsonet al. (1929) and Michel and Dardillat(1972) obtained values of 6.9 and 7.42 mg/100 ml respectively for the phosphatemia.Our measurements of blood calcium (12.91 .

± 0.28 mg/100 ml in healthy animals and12.31 ± 0.22 mg/100 ml in diarrheic calves)and phosphate (7.27 ± 0.27 mg/100 ml in

healthy animals and 6.29 ± 0.23 mg/100 mlin sick calves) are of the same order.

Barlet et al. (1971) observed a level of

plasma magnesium at birth (2.09 mg/100 ml)similar to those we obtained in healthy (2.13± 0.10 mg/100 ml) and sick calves (1.96± 0.04 mg/100 ml).The plasma concentrations at birth-of the

different protein fractions in calves reportedby Michel (1970) and Michel and Dar-dillat (1972) (total proteins : 5.03 g/100ml ; albumin : 2.50 g/100 ml ; globulins : 2.53g/100 ml) were similar to our values fordiarrheic and healthy calves respectively(total proteins : 5.00 ± 0.15 and 5.40 ± 0.29g/100 ml ; albumin : 2,27 ± 0.09 and 2.61 ±0.09 g/100 ml ; globulins : 2.73 ± 0.10 and2.88 ± 0.36 g/100 ml).1.2. Neonatal variationThe neonatal variation of calcemia was

similar to that described by Barlet et al.

(1971) for 7 days. However our results were

slightly higher than the values obtained bythese workers. This may suggest that calfcalcemia can vary from one herd to another.The regular decrease of calcemia is reflected

by its significant correlation with calf age :

y represents the daily calcemia mean (mg/100 ml) and x the calf age (days).The plasma magnesium level falls gra-

dually during the first two weeks of calves

life; this is comparable with the changesobserved in newborn humans (Kobayashi,1968; Teh, 1968). Anast (1964) and Har-

vey, Cooper and Stevens (1970) considerthat this fall is caused by weaning, becauseit does not occur in breast-fed babies. It

may be possible that, in the calves, the

change of feeding between 24 and 36 hours(colostrum for a milk substitute) would

explain equally the decrease of magnesemia.As with calcemia, we obtained significantcorrelations between plasma level of magne-

. sium and calf age, reflecting the regular fallof this parameter :

y represents the daily magnesemia mean

(mg/100 ml) and x the calf age (days).The plasma phosphate concentrations

obtained by Barlet et al. (1971) (7.54 mg/100 ml) and by Michel and Dardillat

(1972) (7.40 mg/100 ml) for the 7 days oldcalves are intermediate between our valuesfor healthy and sick calves (7.70 ± 0.36 and6.82 ± 0.30 mg/100 mi).The variations related to age of plasma

total proteins, albumin and globulins mea-

sured by Michel (1973) do not differ fromours, with healthy and sick calves taken

together.

2. Influence of the period of pathology onplasma parameters.

In our calves, diarrhea appeared between5 and 11 days of age. During this periodthere was a marked increase in phospha-temia, proteinemia and globulinemia.The increase in plasma concentration of

total proteins and globulins which occuredin healthy calves, at the time where diarrheawas maximal in the sick animals, cannot beexplained by a subclinical hemoconcentrationbecause hematocrit did not increase duringthis period (Cabello . 1976). The variationmust be due to an increase in protein syn-thesis (especially of globulins) in responseto microbial attacks. The absence of anysuch increase in sick calves appears para-doxical ; they seem able to synthetize pro-teins, since their plasma total proteins andglobulins concentrations continue to increaseduring days 2 to 4, thus independantly of

colostrum. Moreover, Rothschild, Oratz andSchreiber (1976) report that, in man, there isan increased loss of plasmatic proteins duringgastroenteropathy. A similar phenomenon,in diarrheic calves, together with undernutri-tion linked with the disease, explain satis-

factorily their biochemical behaviour.The phosphatemia of healthy calves in-

creased considerably from days 5 to 8.There was a similar, but less marked ten-

dency in sick animals during diarrhea.

The level of sodium in the plasma of

healthy calves dropped during days 7 and 8,while that of diarrheic animals falls more

abruptly and for a longer period between

days 3 and 9 (Cabello, 1976). This suggeststhat both groups have been infected, but thatthe first resisted without appearance of cli-nical symptoms. We found a significant ne-gative correlation between individual sodiumand phosphate concentrations for all theanimals considered together (r = 0.6810 for36 d.l., P < 0.01). It is possible that themechanisms limiting loss of sodium andwater contribute to increase phosphatemia(and specially renal retention of water).

3. Influence of colostrum intake on plasmaprotein level.

Colostrum contains very little albumin, butis very rich in globulins, particularly in gam-maglobulins. Thus, colostrum intake haslittle effect on albuminemia but alters con-

siderably globulinemia and proteinemia.In healthy calves, during day 1, globulinemia

increased by 1.82 g/100 ml and proteinemiaby 1.64 g/100 mi. Between days 2 and 5,their globulinemia and proteinemia fall res-

pectively by 2.27 and 1.87 g/100 ml. These

rapid reductions may be explained partly bythe catabolism of colostral proteins, but

mainly by proteinuria (Howe, 1924; Smithand Little, 1924). According to El Nageh(1970), the main proteins excreted in urineafter colostrum intake are (i lactoglobulins,a lactalbumin and gammaglobulins.The influence of colostrum intake on the

plasma level of proteins and globulins wassmaller in the calves which will suffer fromdiarrhea than in the healthy animals. The

increase of their proteinemia (0.57 g/100 ml)and globulinemia (0.48 g/100 ml) during day1 are small. The later increase in these two

parameters, up to day 4, seems to indicate

that there is a particularly active synthesis ofglobulins in sick calves.

The weak aquisition of colostral globulinsof the diarrheic calves may be explained intwo ways (which may be complementary) :- Colostrum absorbed by these calves

may be low in immunoglobulins. Evidencefor this is provided by Dardillat (1973)who showed a positive correlation betweenthe gammaglobulinemia of 48 hours old cal-ves and immunoglobulin content of theabsorbed colostrum.

- The intestinal absorption of immuno-globulins may be deficient. According to

Klaus, Bennet and Jones (1969) and Fey(1971), it seems that variations in gamma-globulinemia of young calves can also berelated to their ability to absorb colostral

proteins. This hypothesis appears of greatinterest : measurements of plasma hormonaliodine, triiodothyronine and free thyroxineindex show that the calves which will be sickwere in a state of hyperthyroidism from birthto day 2, and probably during gestation(Cabello, 1976). Malinowska et al. (1974)showed that neonatal administration of thy-roxine to young rats markedly reduces theirperiod of intestinal absorption of macro-

molecules.

The hyperthyroidism demonstrated in sickcalves may cause a reduction of the intes-tinal immunoglobulin absorption period, thusexplaining the small quantity of globulinsabsorbed by the animals. Since the globu-linemia of diarrheic calves is low at 48 hoursof age, their y globulinemia is probably alsolow, which could explain the apparition ofdiarrhea.

Many workers (Gay et al., 1965; Stapleset a[., 1969; Tennant et al., 1969; Dar-dillat and Michel, 1972 ; Dardillat, 1973,1976) have shown that mortality and or

morbidity were more frequently observedin hypogammaglobulinemic calves, as their

immunitary protection was insufficient.

Mac Cance and Widdowson (1959) foundthat in piglets, colostrum intake causeda considerable increase in plasma vo-

lume, while Birke (1966) reported that an

increased level of immunoglobulins in plasmaresulted in an increase of the blood volume.The effect of colostrum intake on plasma vo-lume thus seems to be due to its provision ofgammaglobulins. The increase in blood vo-lume following colostrum intake in calvesshould be greater in healthy than in sickanimals. Then, the latter would be more

susceptible to the extracellular dehydrationwhich occurs during diarrhea.

4. Plasma composition in healthy anddiarrheic calves during the first 20 days oflife.

4.1. Minerals.The calcemia and phosphatemia of sick

animals are systematically lower, during thewhole period, than those of healthy calves ;impaired placental transfer of these mineralsduring gestation or abnormal fetal and neo-natal regulation may explain this phenome-non. However, the persistence of these dif-ferences for at least 20 days appears to

exclude the placental transfer as causal fac-tor. A deficiency in regulation likely tocause hypocalcemia and hypophosphatemiacould be at many levels, among them we cancite :- The thyroid C cells may secrete exces-

sive quantities of calcitonin, a calcemiaand phosphatemia reducing hormone.- A deficiency of 1-25 dihydroxycholecal-

ciferol synthesis, the active metabolite ofvitamin D, which involves hepatic and renalsteps (De Luca, 1974), may cause hypocal-cemia and hypophosphatemia.As calcemia and phosphatemia observed

at birth are representative of the valuestowards the end of gestation, it is likelythat these differences existed before birth.

4.2. Albumin.With the exception of day 2, albuminemia

in sick calves was systematically lower, frombirth to day 20, than in healthy animals. A

poor maternal, and thus fetal nitrogen nutri-

tion could explain this. However, both sickand healthy calves came from mothers of

the same herd (same diet) and, in addition,the uremia at birth was similar in the two

groups of calves (Cabello, 1976). Thus,this hypothesis appears unlikely, especiallysince the difference persists for at least 20

days. An imbalance in the synthesis or cata-bolism of albumin in the sick calves maybe the origin of the difference.

It is possible that albumin catabolism is

increased in sick animals, particularly duringdiarrhea (Rothschild, Oratz and Schrei-

ber, 1966), but this would not explain the

difference at birth or during days 11 to 20.Plasma albumin synthesis occurs in the

liver. Precedently, it was suggested that

hypophosphatemia could be due to a defi-ciency of 1-25 dihydroxycholecalciferol syn-

thesis, occuring for one step in the liver

(transformation of vitamin D to 25 hydroxi-cholecalciferol) (DE LUCA, 1974). In addi-tion we have shown that, within groups ofanimals of the same age, there was a posi-tive correlation between albuminemia and

phosphatemia (day 0 : r = 0.4296, P < 0.05 ;day 20 : r = 0.6728, P < 0.01). This sug-gests that plasma phosphate and albuminlevels are influenced by a common factor,which might be hepatic activity. Overall,these results suggest than the liver may notbe sufficiently active in newborn sick ani-mals (in these respects).According to Hamashima’s histological

results (1966), it seems that hepatic synthe-sis of albumin in the fetus increases regu-larly during gestation. If albuminemia at

birth is directly related to that near the endof gestation, hypoalbuminemia of the sickcalves must precede birth.Bennhold (1956, cited by Freeman, 1967)

has shown, in man, a predisposition to

oedema in hypoalbuminemic or analbuminemicpatients due to a reduced oncotic pressureof plasma. It is possible that such a pheno-menon exists in calves, so that from birthonwards the sicks animals may have a greaterpredisposition to reduction of blood volume,due to their low albuminemia, than the

healthy animal.

Conclusions

Considerable biochemical differences ap-

pear from birth onwards between the healthyanimals and those that will suffer from diarr-hea but survive. On the day of birth, thelatter show hypophosphatemia and hypoal-buminemia. These results suggest that cal-ves of which the health state will be diffe-rent are biochemically different at birth and

probably during foetal life.

This study of the postnatal changes of theconcentrations of various plasma componentshas shown the following facts :- The increase in globulinemia and pro-

teinemia following colostrum intake are muchsmaller in the animals that will presentdiarrhea than in those which remain healthy.This may be explained partly by a deficiencyin intestinal absorption of colostral globu-lins, so that the sick calves do not acquiresufficient immunitary protection.- Calcemia, phosphatemia and albumine-

mia in the diarrheic calves are constantlylower, form birth to 20 days, than in healthyanimals.

Several hypothesis can explain these ano-malies, inducing insufficient hepatic activityin the sick calves.

This work has enabled us to observe a

number of biochemical anomalies which

occur before appearance of clinical symp-

toms, in the diarrheic calves. It’ would be

interesting to verify their existence duringthe foetal life.

Accepted for publication march 1977. ’

SummaryThe changes in plasma concentrations of calcium, phosphorus, magnesium and several pro-tein fractions, were studied from birth to the age of twenty days in 68 calves. 32 animalsremained healthy while 36 animals suffered from diarrhea but survived. The day of birththe two groups differed biochemically. During the whole period studied, calcemia, phos-phatemia and albuminemia of diarrheic calves were systematically lower than those of ani-

mals showing no pathologic symptoms. In addition, after intake of colostrum, the increasein total proteins and globulins was much smaller in sick calves than in those which remai-ned healthy. The possible causes of these anomalies and their roles in the appearanceof pathology are discussed.

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