VETERINARSKI ARHIV 68 (2), 71-77, 1998

ISSN 0372-5480
Printed in Croatia





Postnatal development of pancreatic juice lipase
activity in bovine calves

Ketan S. Christi, and Vijaykumar P. Vadodaria*

Department of Physiology & Biochemistry, College of Veterinary Science and Animal Husbandry, Gujarat Agricultural University, Anand, India





* Contact address:
Prof. Dr. Vijaykumar Premchandbhal Vadodaria,
Department of Physiology & Biochemistry, College of Veterinary Science & Animal Husbandry, Gujart Agricultural University, Anand-388 001, India,
Phone: 91 269 221 666 Ext. 318; Fax: 91 269 241 520


CHRISTI, K. S., V. P. VADODARIA: Postnatal development of pancreatic juice lipase activity in bovine calves. Vet. arhiv 68, 71-77, 1998.

ABSTRACT

The present investigation was made on 10 crossbred bovine calves (Kankrej Jersey) with reference to lipase activity in pancreatic juice from birth to the early ruminant stage. Pancreatic juice was collected in situ by cannulating the pancreatic duct. Samples were collected 30 min before feeding (BF) and 30 min after feeding (AF) both in the morning (MH) and in the evening (EH). Results were of significant effect during AF throughout the study period. Overall, lipase activity fluctuated little, except during the initial two days. Further, total activity (volume concentration; VC) was found to increase with age when expressed as volume (flow rate) of pancreatic juice secreted during a period of 30 min. Diurnal variation revealed non significant higher lipase activity during EH when compared to morning hours, except that significant higher activity was recorded at EH at  1 day, 2 day, 8 weeks and 11 weeks of age. Overall lipase activity increased due to feeding to a level of 14.9% (0.53 U/ml) as compared to its basal level. Average lipase activity (U/ml) at different feeding stages were: 2.90.36 during colostrum feeding, 3.90.13 during milk replacer powder feeding, 3.90.11 with concentrate and hay feeding, and 4.10.09 with fodder (green and dry) feeding. Findings suggest that lipase activity present at birth, increases with age in terms of volume secreted. The developmental pattern may be modified by the colostrum and milk substitute intake, as well as upon weaning due to development of fore-stomachs and increased amount of solid food intake.

Key words: lipase, pancreatic juice, bovine calves, age, diurnal variation, feeding effects



Introduction

Bovine neonates are generally given colostrum during the first two days of life, before changing to whole milk or a milk substitute diet. Pre-ruminant calves are exclusively milk fed and are then usually maintained at this stage up to the age of 3-4 months. When  dairy breed calves are reared for herd replacement they are offered solid food ad libitum at an early stage, and decreasing amounts of milk. Solid food enters the rumen, and subsequent development of the fore-stomach is observed, together with an increasing amount of microbial digestion (THIVEND et al., 1980). At the end of the weaning period calves are no longer considered to be pre-ruminants but ruminants. Studies dealing with the biochemical and physiological changes accompanying this important anatomical modification of the gut and related structures are somewhat scarce (GUILLOTEAU et al., 1992). Pancreatic exocrine secretion and composition in relation to nutritional changes have been studied in various species (CORRING et al., 1978; PIERZYNOWSKI et al., 1991; SHIRAZI-BEECHEY et al., 1991; CHRISTI et al., 1996). MCCORMICK and STEWART (1967), TERNOUTH and ROY (1973) showed the dynamic processes occurring in daily pancreatic secretion. The aim of the present study was to characterise the development of pancreatic juice lipase enzyme in cow calves during the first 15 weeks after birth. The development of the enzyme was considered in relation to age, diurnal and feeding effects.

Materials and methods

The present investigation was carried out on 10 crossbred male bovine calves (Kankrej Jersey). Surgical preparation for pancreatic duct cannulation and postoperative care as per the method described (CHRISTI et al., 1996).

Experimental design. The calves were maintained in well ventilated, clean individual pens. The developmental stages and feeding schedule per calf applied for raising the calves during the experimental period were as described in Table 1.


Table 1. The feeding schedule of bovine calves (N=10) in study of pancreatic juice lipase activity development

Develop- mental stage

Age

Colostrum
(g/2 l)

MRP
(g)

Mineral mixture (g)

Concentrate (g)

Hay (g)

Green
fodder (kg)

Dry fodder (kg)

A

0-1 day

1.5

-

-

-

-

-

-

2-6 days

-

300

5.0

-

-

-

-

B

2-4 weeks

-

350

5.0

25

100

-

-

5-8 weeks

-

400

5.0

25

200

-

-

C

9-10 weeks

-

300

5.0

50

300

1.0

0.5

11-15 weeks

-

200

5.0

100

-

2.0

1.0

MRP=Milk replacer powder; A=Preweaning stage; B=Weaning stage; C=Early neonatal stage

Feed was offered at 8.00 and 16.00 hours. Water was supplied ad libitum. The health of calves was monitored through recording the rectal temperature and body mass, in addition to examination of faecal samples for the presence of any parasitic infestation. Pancreatic juice samples were collected 30 minutes both before feeding (BF) and 30 minutes after (AF) during morning (MH) and evening hours (EH). The lipase was estimated from the samples (MC NEELY, 1980) and the data were analysed as per the standard statistical methods (SNEDECOR and COCHRAN, 1967).

Results and discussion

The results obtained in the present study were studied with reference to age, diurnal and feeding effects, from birth to the early ruminant period. Some selected data, from 0 day to 15 weeks, for feeding and diurnal effects are presented in Table 2. Age related daily (for first 10 days) and weekly (for first 15 weeks) developmental behaviour on lipase are depicted in Figs. 1. and 2.


Table 2. Comparative average (meanSE) and sample size (N) of diurnal and feeding effects on pancreatic juice lipase levels (U/ml) in bovine calves

Age

Diurnal effects

"t"
test

Feeding effects

"t"
test

MH

EH

BF

AF

0 day

1.800.42 (4)

2.000.73 (4)

ns

1.840.69 (7)

2.060.40 (7)

ns

1 day

3.340.33 (16)

3.830.37 (16)

**

3.210.31 (16)

3.960.38 (16)

**

2 days

3.960.39 (16)

4.460.44 (16)

**

3.600.35 (16)

4.810.45 (16)

**

3 days

4.050.30 (16)

3.870.30 (16)

ns

3.540.18 (16)

4.380.35 (16)

**

4 days

4.210.27 (16)

4.060.36 (16)

ns

3.720.27 (16)

4.550.37 (16)

**

5 days

3.630.23 (16)

3.890.27 (16)

ns

3.200.18 (16)

4.330.24 (16)

**

6 days

3.550.24 (16)

3.760.25 (16)

ns

3.270.17 (16)

4.030.27 (16)

*

8 weeks

3.390.31 (8)

3.460.42 (8)

*

3.380.28 (8)

3.470.44 (8)

*

15 weeks

4.000.31 (8)

3.860.40 (8)

ns

3.910.22 (8)

3.950.46 (8)

ns

Overall

3.710.06 (276)

3.960.08 (276)

 

3.550.07 (279)

4.080.08 (279)

 

*=Significant at 5%; **=Significant at 1%; ns=Nonsignificant;
MH=Morning hours; EH=Evening hours; BF=Before feeding; AF=After feeding

Fig 1.

Fig. 1. Lipase level and activity (VC) in pancreatic juice of bovine calves during early neonatal life


Fig 2.

Fig. 2. Lipase level and activity (VC) in pancreatic juice of bovine calves during first 15 weeks of life


Age effects. The average lipase level (U/ml) was 2.880.36 at birth, 3.650.23 at 1 week and 3.930.08 at 15 weeks of age. The early neonatal period revealed a non-significant age effect, and weekly comparison revealed age effect AF. The finding of an increase in lipase level on 2 day supported the view that secretion appears to be faster (than synthesis) during the first two days of life due to considerable storage of most of the pancreatic enzymes, including lipase, taking place in new born ruminants (SISSONS, 1981). GOODEN (1973) found that lipase activity per unit volume of pancreatic juice in 2-day-old calves was similar to that in an animal aged 2 weeks.

Data on flow rate and lipase level were used to calculate total activity (VC). Graphic presentation of total activity revealed an increase with age (Figs. 1 and 2). GOODEN and LASCELLES (1973) also attributed a three-fold increase in output of pancreatic lipase per kg body mass to a substantial increase in the flow rate of pancreatic juice. A similar increase with higher activity was recorded in buffalo calves in a concurrent study (CHRISTI et al., 1996). The first and second spurts in lipase levels were recorded on day 1 and week 1 AF, irrespective of the period of the day. The level between birth to 10 weeks, and between 8 weeks to 15 weeks, were a 1.05-fold and 0.97-fold increase. LE HUEROU et al. (1992) reported a slightly higher (1.6-fold and 2 to 3-fold) level between birth to 70 days and between 56 days to 119 days in pancreatic tissues of pre-ruminant dairy calves.

Diurnal effects. Diurnal variations revealed a non-significant higher level during EH (6.74%; 0.25 U/ml) as compared to MH, except for significantly higher levels recorded at 1 day, 2 day and 11 weeks EH.

Feeding effects. Feeding effects for a particular age group were compared for pre-weaning, 0-1 day colostrum feeding, 2-6 day milk replacer powder  (MRP) feeding, weaning (2-8 weeks) and early ruminant stage (9-15 weeks). Feeding colostrum increased the lipase level insignificantly at birth but significantly on 1 day during MRP feeding. It increased significantly and for remaining ages there was an insignificant increase, except for an insignificant decrease recorded at 9 day (weaning stage) and at week 10 (early ruminant stage). Findings of increased lipase activity during the first week after weaning (week 9) and a decrease thereafter compared very well with similar observations made by LE HUEROU et al. (1992). Additionally, they reported an increased lipase level after weaning which, despite the fact that lipid intake was much lower than in pre-weaning, could be due to a greater increase in dry matter intake rather than to variations in the amounts of substrates.

HENNING (1986) reported an ontogenic pattern in enzyme activity, modified at birth by  colostrum and milk intake and upon weaning, due to the development of the fore-stomachs and, to a certain extent, to an increase in the amount of solid food intake. Secretin, ketones and fatty acid metabolites are proposed mediators of pancreatic adaptation to dietary fat (HENNING, 1986; BRANNON, 1990). Secretin acts via a translation control mechanism (BRANNON, 1990).

Overall lipase level in pancreatic juice increased to a level of 14.9% (0.53 U/ml), as compared to their respective basal values. GUILLOTEAU et al. (1985) reported more lipase activity in diets containing a higher amount of fat. A concurrent study undertaken on buffalo calves revealed a 42.7% (3.41 U/ml) increase, which was 2.88 times greater than in bovine calves (CHRISTI et al., 1996), indicating a greater potency in buffalo calves in adapting the exocrine pancreatic function.

Average lipase activity (U/ml) increased from colostrum feeding (2.890.36) to MRP feeding (3.920.13), and at inclusion of concentrate and hay to the feeding schedule (3.920.11), and at feeding dry and green fodder (4.110.09). ULBRICH et al. (1981) demonstrated that lambs reared on milk replacer displayed higher activities of pancreatic lipase than those reared on ewe milk. There is evidence that lipase activity in pancreatic juice is affected by the nature of the dietary protein. TERNOUTH et al. (1975) compared the effect of diets containing either milk, soya bean or fish protein on pancreatic enzyme secretion in calves fitted with duodenal re-enterant cannulas and pancreatic sac cannulas. They found that pancreatic lipase activity during a 12-hour period after giving liquid feeds containing non-milk protein was significantly less than for diets containing skimmed milk.


Acknowledgements
The authors are grateful to the C.S.I.R., New Delhi, for providing financial assistance in the form of a Senior Research Fellowship. Thanks are also extended to the Department of Surgery and Animal Genetics & Breeding for their help in this work.


Reference

BRANNON, P. M. (1990): Adaptation of the exocrine pancreas to diet. Annu. Rev. Nutr. 10, 85-105.

CHRISTI, K. S., V. P. VADODARIA, V. M. MEHTA (1996): Pancreatic juice lipase in buffalo calves from birth to early ruminant stage. Proceed. 2nd Asian Buffalo Association Congress. Manila, Philippines. pp. 451-462.

CORRING, T., A. AMAITRE, G. DURAND (1978): Development of digestive enzymes in the piglet from birth to 8 week. I: Pancreas and pancreatic enzymes. Nutr. Metab. 22, 231-243.

GOODEN, J. M. (1973): The importance of lipolytic enzymes in milk fed and ruminating calves. Aust. J. Biol. Sci. 26, 1189-1199.

GOODEN, J. M., A. K. LASCELLES (1973): Relative importance of pancreatic lipase and pregastric esterase on lipid absorption in calves 1-2 weeks of age. Aust. J. Biol. Sci. 26, 625-633.

GUILLOTEAU, P., T. CORRING, R. TOULLEC, R. GUILHERMET (1985): Enzyme potentialities of the abomasum and pancreas of the calf. II: Effects of weaning and feeding a liquid supplement to ruminant animal. Reprod. Nutr. Develop. 25, 481-493.

GUILLOTEAU, P., I. L. LE HUEROU, J. A. CHAYVIALLE, A. MOUATS, C. BERNARD, J. C. CUBER, J. BURTON, A. PUIGSERVER, R. TOULLEC (1992): Plasma and tissues levels of digestive regulatory peptides during postnatal development and weaning in the calf. Reprod. Nutr. Dev. 32, 285-296.

HENNING, S. J. (1986): Development of gastrointestinal tract. Proc. Nutr. Sci. 45, 39-44.

LE HUEROU, I. L., P. GUILLOTEAU, C. WICKER, J. A. CHAYVIALLE, J. BURTON, A. MOUATS, R. TOULLEC, A. PUIGSERVER (1992): Gastric and pancreatic enzyme activities and their relationship with pancreatic enzyme activities and their relationship with some gut regulatory peptides during postnatal development and weaning in cow calves. J. Nutr. 122, 1434-1445.

MCCORMICK, R. J., W. E. STEWART (1967): Pancreatic secretion in the bovine calf. J. Dairy Sci. 50, 568-571.

MC NEELY (1980): Gastrointestinal function. In: Gradwohl's clinical laboratory methods and diagnosis (Sonnenwirth A. C., L. Jarett, Eds.). 8th ed. C. V. Mosby Company. London. pp. 517-563.

PIERZYNOWSKI, S. G., R. ZABIELSKI, B. R. WESTROM, M. MIKOLAJCZYSK, W. BAREJ (1991): Development of the exocrine pancreatic function in chronically cannulated calves from the preweaning period up to early rumination. J. Anim. Physiol. Anim. Nutr. 65, 165-172.

SHIRAZI-BEECHEY, S. P., M. W. SMITH, Y. WANG, P. S. JAMES (1991): Postnatal development of lamb intestinal digestive enzymes is not regulated by diet. J. Physiol. 437, 691-698.

SISSONS, J. (1981): Digestive enzymes of cattle. J. Sci. Food. Agric. 32, 105-144.

SNEDECOR, G. W., W. G. COCHRAN (1967): Statistical methods. 6th ed. IBH Publishing Co. Calcutta.

TERNOUTH, J. H., J. H. B. ROY (1973): The effect of diet and feeding technique on digestive function in the calf. Ann. Rech. Vet. 4, 19-30.

TERNOUTH, J. H., J. H. B. ROY, S. Y. THOMPSON, J. TOOTHHILL, C. M. GILLIES, J. D. EDWARDS-WEBB (1975): Concurrent studies of the flow of digesta in the duodenum and of exocrine pancreatic secretions of calves. 3. Further studies on the addition of fat to skim milk and the use of non-milk proteins in milk substitute diets. Br. J. Nutr. 33, 181-196.

THIVEND, P., R. TOULLEC, P. GUILLOTEAU (1980): Digestive adaptation in the preruminant. In: Digestive Physiology and Metabolism in Ruminants (Ruckebusch, Y., P. Thivend, Eds.). MTP Press. Lancaster. pp. 561-586.

ULBRICH, M., M. HOFFMAN, N. F. A. HAKIM (1981): Investigation of the activity of pancreas lipase in growing sheep. Arch. Tierernaehr. 31, 171.

Received: 7 January 1998
Accepted: 11 March 1998



CHRISTI, K. S., V. P. VADODARIA: Razvoj postnatalne aktivnosti lipaze u gusteracnom soku teladi. Vet. arhiv 68, 71-77, 1998.

SAZETAK

Istrazivanje je provedeno na desetero teladi krizane pasmine (Kankrej Jersey), a odnosi se na aktivnost lipaze u gusteracnom soku od rodenja do rane faze prezivanja. Sok je skupljan in situ preko kanile iz izvodnog kanala gusterace, i to 30 minuta prije te 30 minuta poslije jutarnjeg i vecernjeg hranjenja. Znacajna aktivnost lipaze ustanovljena je nakon hranjenja u tijeku citavog razdoblja istrazivanja. Opcenito je njezina aktivnost neznatno kolebala, osim u prva dva pocetna dana. Nadalje je ustanovljeno da se ukupna aktivnost lipaze (volumen i koncentracija) povecavala s dobi, ukoliko se izrazava po volumenu izlucenog soka u tijeku 30 minuta. Sto se tice dnevnih razlika ustanovljeno je da nije bilo znatno vece aktivnosti lipaze u vecernjim u odnosu na jutarnje sate, osim prvog i drugog dana te osmog i jedanaestog tjedna starosti. Sveukupna aktivnost lipaze se povecala nakon hranjenja za 14,9% (0,53 U/ml) u odnosu na bazalnu razinu. Prosjecna aktivnost lipaze (U/ml) pri razlicitim fazama hranjenja bila je: 2,90,36 u tijeku hranjenja kolostrumom, 3,90,13 u tijeku davanja mlijecnih nadomjestaka, 3,90,11 za hranjenja koncentratom i sijenom i 4,10,09 pri davanju zelene i suhe hrane. Rezultati pokazuju da se aktivnost lipaze prisutna pri rodenju povecava sa staroscu i u skladu s izlucenim volumenom. Aktivnost moze biti izmijenjena uzimanjem kolostruma i mlijecnog nadomjestka, te nakon odbica zbog razvoja predzeludaca i nakon povecanog uzimanja cvrste hrane.

Kljucne rijeci: lipaza, gusteracni sok, telad, dob, dnevna kolebanja, ucinak hranidbe


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