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Effects of small ruminal boluses used for electronic identification of lambs on the growth and development of the reticulorumen^1,2

D. Garín^3,*, G. Caja^4,* and F. Bocquier

^* Grup de Recerca en Remugants, Departament de Ciència Animal i dels Aliments, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain and and UMR Élevage des Ruminants en Régions Chaudes, Campus ENSAM-INRA 34 060 Montpellier Cedex 1, France

⁴ Correspondence:
fax: +34-935811494; E-mail:
gerardo.caja{at}uab.es.

	Abstract

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Fifty-four male lambs were used to study the effects of two types of small electronic boluses on the dimensions and epithelial characteristics of their reticulorumen. Newborn lambs were assigned according to bolus type and age of application to the following treatments: 1) control (C, n = 21), without bolus; 2) mini (M, n = 21), identified with a 9.3 x 37.4-mm, 5.2-g bolus during the first week after birth; and 3) small (S, n = 12), identified with a 15.0 x 39.1-mm, 20-g bolus after weaning at wk 5, when lambs weighed more than 12 kg. After weaning, lambs were given ad libitum access to concentrate and barley straw. Six lambs were euthanized at the start of the experiment to measure initial reticulorumen characteristics. Ten lambs (five from M and five from C treatments) were slaughtered at weaning and 24 (eight per treatment) were slaughtered when they reached 24 kg. After bolus recovery, the reticulorumen was emptied and filled with polyurethane foam to obtain reticulorumen casts. Weight of the emptied reticulorumen and volume of the casts were measured. Four representative lambs from each treatment were also slaughtered at 24 kg, and their reticulorumen used to evaluate papillae size, number of dead cells, and degree of keratinization of both the reticulum wall and the rumen wall epithelia. Weight at weaning (13.8 kg), age at the end of fattening (65 d), and mortality rate (4%) did not differ among treatments. Retention rate for M and S boluses was 82.4 and 100%, respectively. Fresh weight and volume of the reticulorumen did not differ among treatments at weaning (130 g and 1,679 mL) or at the end of the fattening period (640 g and 5,931 mL). Lambs in the M treatment had greater (P < 0.05) rumen papillae size and lower (P < 0.10) keratinization than C lambs; values in the S lambs were intermediate between M and C lambs. Neither the M nor S type of bolus affected dimensions of the reticulorumen, but the earlier presence of M boluses induced a greater papillae size, with no negative effects on health and fattening performances of young lambs.

Key Words: Lambs • Rumen Development • Rumen Epithelium • Transponders

	Introduction

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Electronic identification using passive radiofrequency transponders enclosed in ruminal boluses has proved to be a safe and permanent option for individual tagging of ruminants (Caja et al., 1999; Lambooij et al., 1999; Fallon, 2001). Different electronic boluses have been developed for goats, cattle, and sheep, and no negative effects on performance have been reported (Caja et al., 1999; Lambooij et al., 1999; Garín et al., 2000). Despite the large size of the bolus, no effects on intake and digestibility have been reported in sheep (Caja et al., 1999), and no effects on the appearance of the ruminal wall were reported in cattle (Hasker and Bassingthwaighte, 1996) or in sheep and goats (Caja et al., 1999). However, this conclusion is only drawn from the subjective assessment of the rumen wall. Foreign bodies (magnets, additive release boluses, etc.) are also commonly introduced into the rumen of cattle and sheep without apparent alteration of animal function. In milk-fed ruminants, growth of the forestomachs has been attributed to the presence of particles (Tamate et al., 1962; Hamada, 1975; Lyford, 1988) and to the effect of fermentative products (Tamate et al., 1962; Hamada, 1975; Dziuk, 1984). Larger particles can stimulate rumination and motility (Dziuk, 1984; Campion and Leek, 1996) and prevent a hyperkeratinization of the epithelium (McGavin and Morrill, 1976; Nocek and Kesler, 1980; Jones et al., 1997). Both growth and development of the reticulorumen were induced using food (Tamate et al., 1962; Nocek and Kesler, 1980; Beharka et al., 1998) or inert materials (Tamate et al., 1962; Hamada, 1975). It is not known if the early presence of a ceramic bolus in the forestomachs of lambs can produce injuries and affect development and growth. Therefore, the objective of this study was to examine effects of two small electronic boluses applied at early ages in growing lambs on the growth and development of the reticulorumen.

	Materials and Methods

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Animals, Treatments, and Feeding
A total of 54 male lambs from Manchega dairy breeds, born in the Experimental Farm of the Servei de Granges i Camps Experimentals of the University Autònoma of Barcelona, were used. Newborn lambs were blocked by birth type and stratified by birth weight and maternal parity, prolificacy, BW, and BCS prior to being randomly assigned to one of three treatments. Treatments were 1) control, without bolus (n = 21); 2) mini, identified with a bolus of 5.2 g at 1 wk old (n = 21); and 3) small, identified with a 20 g bolus after weaning (end of wk 5, when lambs weighed approximately 12 kg; n = 12). Ewes and lambs were penned together according to the experimental treatments. Lambs had free access to suckling for 18 h/d (between 1600 to 1000) during the first 4 wk of age. During wk 5, lambs suckled from 2000 to 0700 to force concentrate intake before weaning. Lambs had free access to barley straw, water, and a commercial concentrate (DM, 87.9%; CP, 19.3%; ether extract, 3.3%; NDF, 17.0%, DM basis, Fimsa, La Bisbal del Penedés, Tarragona, Spain) from birth to the end of fattening. Lambs were slaughtered when they reached market weight as Spanish Pascual lambs (24 kg of BW). During the suckling period, lambs had access to concentrate by creep feeding. After weaning, all the lambs were fed together as a mixed group. Ewes were kept in a semi-confinement system and were allowed to graze for 6 h daily in an annual Italian ryegrass prairie and were supplemented indoors with 0.8 kg of chopped dehydrated forage mixture (50% whole plant corn and 50% alfalfa hay; DM, 92.4%; CP, 12.0%; NDF, 50.4%, DM basis), 0.3 kg alfalfa pellets (DM, 93.0%; CP, 15.8%; NDF, 43.8%, on DM basis) and 0.6 kg of concentrate (DM, 90.1%; CP, 21.4%; ether extract, 2.5%; NDF, 33.7%, DM basis) per ewe, according to the INRA requirements (Bocquier and Thèriez, 1989).

Bolus Transponders and Transceivers
Two types of small cylindrical boluses made of alumina (Al₂O₃) according to the patents of The European Community et al. (1998), and Caja et al. (2001) were used. Boluses were designed for two different oral application ages in lambs. The mini boluses, which were applied during the first week postpartum, were 9.3 mm o.d. x 37.4 mm length, weighed 5.2 g, and had a specific gravity of 2.15. The small boluses, which were applied after weaning, were 15.0 mm o.d. x 39.1 mm length, weighed 20.0 g, and had a specific gravity of 3.08.

One 32.5 x 3.8-mm passive half-duplex, glass-encapsulated transponder was inserted in each bolus. The transponders worked at a frequency of 134.2 kHz according to ISO 11785 (ISO, 1996), and each one was encased and fixed in a bolus by epoxy resin (MP Super, Ceys S.A., Barcelona, Spain). Serial numbers of the read-only transponders (model Ri-Trp-RR2B-06; Tiris, Almelo, The Netherlands) ranged from 8,305,156 to 16,392,507.

Two types of portable transceivers were used for the reading controls: Portoreader B.V. (Insentec, Marknesse, The Netherlands) and Gesreader II (Gesimpex Comercial S.L., Barcelona, Spain). Portable transceivers allow a reading distance up to 25 cm.

Identification and Recording Procedures
Experimental and animal care procedures were approved by the Ethical Committee on Human and Animal Experimentation of the University Autònoma of Barcelona (Reference CEEAH 343/01). The total number of lambs used and slaughtered at different ages according to the experimental treatments is summarized in Table 1.

In order to determine BW change from bolus application to slaughter, lambs were weighed at birth and weekly during suckling (wk 1 to 5) and fattening (wk 6 to slaughter) periods with an electronic scale (FX-31, Allflex N.Z. Ltd., Palmerston North, New Zealand) connected to a Gesreader II handheld transceiver.

Six newborn lambs (three controls and three receiving a mini bolus) were euthanized with sodium pentothal (1 mL i.v., Laboratorios Abbott, Madrid, Spain) at the start of the experiment to measure initial reticulorumen characteristics. Ten additional lambs (five controls and five receiving a mini bolus) were slaughtered at weaning, and the remaining 36 (12/treatment) were slaughtered when they reached 24 kg (Table 1). Using a Gesreader II handheld transceiver, all lambs carrying a bolus were checked before leaving the farm for the abattoir and at the start of the slaughtering line. The boluses were recovered in the abattoir. The lambs were fasted for 8 h and given only water before slaughtering. Bolus location in the forestomachs was recorded when retrieved.

Reticulorumen Measures
The forestomachs of eight lambs from each experimental treatment were collected after slaughter and immediately processed according to the following procedure. Reticulorumen was isolated as a single segment by cutting the esophagus at approximately 2 cm from the cardiac sphincter and at 2 cm caudally to the reticulo-omasal orifice. Reticulorumen content was emptied through the reticulo-omasal orifice and the tissues were flushed with tap water. After dripping, fresh reticulorumen tissue was weighed to an accuracy of 2 g. Emptied reticulorumen were filled by blowing polyurethane foam from a commercial spray (Fischer Ibérica S.A., Cerdanyola del Vallès, Spain) introduced into the cardia orifice. Special care was taken to avoid air bag formations in the rumen blind sacs. Excess foam expansion was allowed to overflow through the cardia and reticulo-omasal orifices and through two 1-cm cuts in the rumen blind sacs. Full solidification was obtained placing the tissue on a soft surface for 24 h. Excess foam was subsequently removed. The reticulorumen tissue was then removed and the cast volume was measured by water displacement.

To study the effects of bolus presence on the reticulorumen epithelium, a representative sample of four fattened lambs from each treatment were slaughtered. Reticulorumen were collected at slaughtering and processed separately after emptying and washing. Samples of the reticulum wall and the ruminal atrium wall (approximately 1 x 4 cm) were cut ventrally at approximately 5 cm from the cardia and fixed in a 10% formaline solution. Samples were embedded in paraffin according to routine histological procedures, and sections were stained with hematoxylin-eosin (Kiernan, 1990). Two sections per sample, with 10 or more papillae, were used. The degree of keratinization, the length of papillae, and the frequency of dead cells in the reticulum and ruminal atrium mucosa were evaluated by observation of five papillae randomly selected per section according to a subjective scale from 0 to 3 (0, negative; 1, light; 2, moderate; and 3, heavy) similar to that described by Nocek and Kesler (1980).

Statistical Analyses
Lamb weights, reticulorumen volume and fresh tissue weight, degree of parakeratosis, length of papillae, and frequency of dead cells in the wall mucosa were analyzed as a randomized complete block design by ANOVA using the GLM procedure of SAS (version 6.12, SAS Inst., Inc., Cary, NC). Age and weight of the ewes at lambing were the blocking factors and birth weight was included as a covariate in the model used to analyze the BW of lambs at weaning. Lamb’s type of birth was the blocking factor for the analysis of BW and reticulorumen effects in each growing period. Lamb weight at slaughter was also used as a covariate for the models used to analyze the reticulorumen volume and fresh tissue weight. For the data on retention rate on the farm, slaughterhouse retrieval, and location of the boluses in the forestomachs, the LOGIT model with the estimation method of maximum likelihood (Cox, 1970) using the CATMOD procedure of SAS, was utilized. Non-significant (P > 0.20) variables and interactions were removed from the model. Statistical significance was declared at P < 0.05 and, following a significant F-test, adjusted least squares means were separated by using the Tukey test of SAS.

	Results and Discussion

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Animal and Bolus Performance
Growth performance of the lambs was not affected (P > 0.05) by treatments, as shown in Table 2. Average daily gains were 267 ± 27 and 276 ± 37 g for the suckling and the fattening periods, respectively, and were similar to those previously reported in intensively reared Manchega lambs (Peris et al., 1992; Casals et al., 1999). Neither weight at weaning (13.8 ± 0.9 kg) nor age at the end of fattening (64.9 ± 2.2 d) was affected by treatments (P > 0.05). No differences were observed (P > 0.05) in lamb mortality among treatments, and mortality rate from birth to slaughter was low and averaged 3.7% (Table 1). One control lamb and one receiving a mini bolus treatment died during the suckling period as a result of pneumonia and diarrhea, respectively. Because these deaths were not related to the bolus application, data from these lambs were excluded from subsequent analysis.

No losses of conventional ear tags or small boluses were observed before slaughtering at 24 kg of BW, whereas losses of mini boluses were observed from wk 4 to 7. Moreover, one lamb lost its bolus three times, but the reapplications were not included in the calculations of bolus retention rates. As a consequence, retention rates were greater for small vs. mini boluses (Table 2). Results were greater than the 59% reported by Garín (2002) when using the same mini bolus. These results confirm that mini boluses with a specific gravity of 2.15 are inadequate for midterm retention in the forestomachs of fattening lambs.

All of the small and mini boluses present at slaughter were recovered from the reticulorumen of the lambs. Recovered mini boluses had different locations in the forestomachs according to the age of lambs (P = 0.013). Only one mini bolus (20%) was located in the reticulum of a lamb slaughtered at weaning, whereas 11 (91.7%) were located in the reticulum in lambs slaughtered at the end of the fattening period. Conversely all small boluses were located in the reticulum. The overall mean (95.8%) of boluses located in the reticulum of fattened lambs (Table 2) is within the range of previous values (80 to 96.5%) reported in sheep (Caja et al., 1999; Garín, 2002). This pattern of distribution agrees with the sequence of reticulorumen motility described by Dziuk (1984) for heavier food boli or high-density bodies. It is possible that the mini boluses were located in the rumen’s cranial sac (Atrium ruminis) just after application, and were later transferred to the reticulum by ruminal motility. Ruminal motility normally develops between wk 3 and 8 of age in lambs (Poe et al., 1969; Oh et al., 1972). This was probably the reason why the mini boluses were found in the reticulum of the lambs slaughtered at weaning. Because recovery in the reticulum was less than 100%, mini boluses do not seem to reach their permanent location in the reticulum after 5 wk of age.

Growth and Development of the Reticulorumen
The weight and volume of the reticulorumen at different ages (Table 3) agreed with previously described reticulorumen development in young ruminants (Church et al., 1962; Large, 1964). Average values for fresh tissue weight and volume of reticulorumen casts were: 30 g and 160 mL in newborn lambs, 130 g and 1,679 mL in weaned lambs, and 640 g and 5,931 mL in fattened lambs, respectively. No significant differences were found between animals carrying or not carrying a bolus independent of the type of bolus (P > 0.05). The relative volume of the reticulum within the reticulorumen decreased (P = 0.009) with age from 18.2 and 10.6% in newborn and fattened lambs, respectively. This agrees with previous reports (Church et al., 1962; Lyford, 1988). There were no differences among treatments (P = 0.268) in the relative reticulum volume, but it tended (P = 0.101) to be greater in animals carrying any type of bolus.

Hyperkeratinization, a process in which the cytoplasm of the outermost cells of the epidermis is abnormally replaced by keratin, was observed in the epithelial papillae of the reticulorumen of all fattened lambs. This is due to the intensive feeding system used for the Spanish Pascual fattening lambs and agrees with the previous results of Garín et al. (2001). The presence of boluses produced a reduction (P < 0.05) in the keratinization of the reticulum wall and a tendency (P = 0.064) to reduce the keratinization of the rumen wall (Table 4). This clearly occurred in lambs with mini boluses that have a lower degree of keratinization of the reticulum wall (P < 0.05) and tended to have a lower keratinization of the rumen wall (P < 0.10) than control. Walls of the rumen and the reticulum in lambs receiving the small bolus were intermediate and did not differ from control lambs or those receiving the mini bolus. This reduction of keratinization of the reticulorumen wall due to bolus presence agrees with observations on the effect of the physical form of roughage (McGavin and Morrill, 1976; Nocek and Kesler, 1980). Textured roughages prevent accumulation of excess keratin on the surface of the ruminal mucosa and thus avoid the growth of abnormal papillae (McGavin and Morrill, 1976). In our case, the friction of mini boluses on the ruminal mucosa may explain the reduction in the degree of keratinization of the reticulum wall. This effect was not significant with the small bolus, probably because of the short carrying period. Other possibilities can also be suggested to explain the differences observed in rumen wall keratinization. Most likely, the early presence of mini boluses, in spite of their low weight, stimulated rumen motility patterns. In young calves, Nocek and Kesler (1980) reported an increase in the muscle thickness of the dorsal sac wall when the length of the diet particle was increased. They suggested that this was a consequence of the more frequent rumen contractions. Similar results on motility pattern were described when intraruminally adding polyethylene particles in adult sheep fed only with concentrate (Campion and Leek, 1996). Rumination was stimulated by the inert mass added (lineally from 5 to 50 g) and by particle length (quadratic effect from 3 to 70 mm), which had its greatest effect between 7 and 30 mm. These results suggest that mini and small boluses probably stimulated rumination earlier and more intensively than in controls. Moreover, the cranial sac is considered to be the last part of the forestomachs to respond to changes in feeding conditions and rumen environment (McGavin and Morrill, 1976). This may explain the limited effects of small boluses.

	Implications

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Application of small size ruminal boluses early in the life of lambs intensively fattened with high-concentrate diets does not alter growth performance and may even induce positive changes in the anatomical characteristics of the reticulorumen. Bolus presence limited hyperkeratinization of the reticulorumen walls, most likely as a consequence of a friction effect and a greater stimulation in ruminal motility induced by the inert fiber-like effect of the ruminal boluses. No adverse effects on the reticulorumen were observed from the mini and small-size ceramic ruminal boluses used for electronic identification and traceability of lambs. Performance and behavior of these lambs was normal.

	Footnotes

 
¹ Research included in the European Commission Research Project QLk1-2001-02229 (EID+DNA Tracing) and also supported by a grant to D. Garín from the Agencia Española de Cooperación Internacional (AECI).

² The authors wish to thank R. Costa and the crew of the Servei de Granges i Camps Experimentals (S1GCE) de la UAB for their careful assistance to animal management, F. Mestre of the Pathology Service of the UAB, Bárbara Baraibar for the histological study, J. Francesc Vilaseca of Gesimpex for providing the ceramic bolus prototypes and N. Aldam for the English revision of the manuscript.

³ Current address: Facultad de Veterinaria, Universidad de la República, Av. Lasplaces 1550, 12500 Montevideo, Uruguay.

Received for publication May 15, 2002. Accepted for publication December 27, 2002.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Garín, D. Articles by Bocquier, F. Search for Related Content PubMed PubMed Citation Articles by Garín, D. Articles by Bocquier, F.