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/lp/oxford-university-press/salivary-igg-levels-in-neonatal-calves-and-its-association-to-serum-BXyG27Knc5
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- © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science.
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- 2573-2102
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- 10.1093/tas/txz001
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Abstract
Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txz001/5298312 by Ed 'DeepDyve' Gillespie user on 05 February 2019 Salivary IgG levels in neonatal calves and its association to serum IgG: an observational pilot study *,1, †, ‡ || || Julie Føske Johnsen, Matteo Chincarini, Åse Margrethe Sogstad, Liv Sølverød, Marie Vatne, * $ Cecilie Marie Mejdell, and Laura Hänninen * † Department of Health Surveillance, Norwegian Veterinary Institute, Oslo 0106, Norway; Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo 64100, Italy; ANIMALIA, Norwegian Meat and Poultry || $ Research Centre, OSLO 0513, Norway; TINE Mastittlaboratoriet i Molde, Molde 6416, Norway; and Faculty of Veterinary Medicine and Research Centre for Animal Welfare, University of Helsinki, Helsinki 00014, Finland ABSTRACT: The diagnosis of inadequate (r = 0.7, P < 0.001) between saliva IgG (mean transfer of colostrum immunoglobulin G (IgG) ± SD; 0.2 ± 0.11 g/L) and serum IgG (32.1 ± to calf serum, often known as failure of passive 11.94 g/L) was found. Saliva IgG ranged from transfer (<10 g/L IgG1 at 24 to 48 h), neces- the lowest detectable value, 0.1 g/L (n = 6 sitates blood sampling from the calf and in samples) to 0.6 g/L. Saliva Brix (1.2 ± 0.69%) some instances the presence of a veterinarian. was not significantly correlated to serum IgG Sampling saliva is both less invasive and easy (n = 12, r = 0.43, P = 0.155); however, it was for the producer. Previous research has shown significantly correlated to saliva IgG (n = 12, that quantification of saliva IgG is possible r = 0.7, P = 0.018) and Brix in serum (n = 12, in juvenile and adult cattle. The objectives of r = 0.7, P = 0.013). We conclude that IgG was this observational pilot study were to investi- quantifiable in most of the saliva samples. For gate whether IgG can be quantified in neonatal saliva IgG to be of any value with regards to calf saliva, if it is correlated to serum IgG con- detecting failure of passive transfer, future centrations, and if the indirect quantification studies should investigate methods that can of saliva IgG is achievable by use of a digital detect IgG <0.1 g/L. The results indicate that refractometer. Paired blood and saliva sam- saliva IgG can be used to predict serum IgG at ples were collected from 20 healthy dairy calves levels above 10 g/L, which may warrant further aged 1 to 3 d. In these samples, IgG was quanti- exploration of the use of saliva in the surveil- fied directly with single radial immunodiffusion lance of failure of passive transfer. The results and indirectly by use of a digital refractome- of the current pilot study did not support the ter indicating Brix % (a subsample of n = 12 potential usage of a Brix % refractometer to saliva samples). A strong positive correlation quantify saliva IgG. Key words: dairy, health, immunity, welfare © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com. Transl. Anim. Sci. 2019.XX:XX–XX doi: 10.1093/tas/txz001 INTRODUCTION Corresponding author: Julie.johnsen@vetinst.no A successful colostrum management pro- Received August 8, 2018. gram requires that calves receive a sufficient Accepted January 17, 2019. 1 Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txz001/5298312 by Ed 'DeepDyve' Gillespie user on 05 February 2019 2 Johnsen et al. volume of clean, high-quality colostrum within MATERIALS AND METHODS the first few hours of life (Godden, 2008). Inadequate transfer of immunoglobulines (Igs; Animals and Management isotypes IgG1 through IgG4; IgG1 being the All procedures were in accordance with the reg- most predominant) is commonly defined by ulations controlling experiments and procedures in serum IgG1 levels of <10 g/L at 24 to 48 h of live animals in Norway (Ministry of Agriculture and age, a condition called failure of passive transfer Food, 2015). We used 20 Norwegian Red dairy calves (FPT; Besser et al., 1991). Because FPT is asso- (10 bull calves and 10 heifer calves; the experimental ciated with increased mortality, and decreased units) kept at the research facility of the Norwegian weight gain (Robison et al., 1988; Wells et al., University of Life Sciences. Calves were separated 1996; Weaver et al., 2000), it represents a risk for from the dam immediately after birth and housed in poor calf welfare, i.e., increased risk of injury, single pens with straw bedding. Only calves without disease, negative feelings, or failure to cope clinical signs of disease were included. Within 4 h of (EFSA, 2012). To investigate FPT, serum has birth, calves were bottle-fed 4 L of colostrum from been used; however, blood sampling is invasive. their own dam. Colostrum quality was measured The presence of a veterinarian is also required in with a digital refractometer (Digital Brix refractom- some instances (as in Norway and Italy; Ministry eter MA871; Milwaukee Instruments, Inc., Rocky of Agriculture and Food, 2001 (Norway), and Mount, NC, USA). Colostrum with Brix % >24 National Association of Veterinarians Italy, was considered high quality whereas colostrum with 2019). If absorbed maternal IgG1 transfers into Brix 18% to 24% was considered of medium qual- the calf’s saliva and its concentration predicts ity. Calves that did not drink the entire amount, or that of serum, saliva may represent a noninvasive received colostrum of medium quality were again medium from which FPT status of calves could be offered colostrum 2 h later. During the first 3 d after evaluated. In young (4 mo) and adult cattle, IgG birth, the calves were bottle-fed colostrum or tran- has been determined in saliva (e.g., Butler et al., sition milk (7 L divided on 5 meals per d) from their 1972; Duncan et al., 1972). However, due to the own dam and had free access to hay, concentrate, intestinal transmission of Igs to the blood circu- and water from the first day. lation occurring until “gut closure” (Deutsch and Smith, 1957), the saliva IgG profile of neonatal Sampling and Analyses of Saliva and Serum calves may differ from that of juvenile or adult cattle. To the authors’ knowledge no study has Between d 1 and 3, matched samples of saliva investigated salivary IgG levels in neonatal calves and blood from the calves were obtained. To mini- and its correlation to serum IgG. mize risk of contamination from previous milk meals, Recently, methods to determine the ade- milk was retained for at least 2 h prior to sampling. quacy of both colostrum quality, i.e., colostrum Saliva samples were taken with a clamped cotton IgG >50 g/L; McGuirk and Collins (2004), and swab (IVF Schauffhauser Dental Rolls No. 2; Paul calf serum IgG have been developed for use on Hartmann AG, Neuheusen, Switzerland), which dairy operations. Digital refractometers indirectly was held into the calves’ mouth for 1 min until it was assess IgG levels through relative density (Brix soaked with saliva (Geburt et al., 2015). Thereafter, %) and have proven valuable for use by producers the cotton was compressed using a 20 mL syringe, fol- (Chigerwe and Hagey, 2014; Elsohaby et al., 2015; lowing which saliva was collected in Eppendorf tubes Morrill et al., 2015) for colostrum as well as serum. (ref. 72.706.400, Sarstedt AG & Co, Nümbrecht, If IgG in saliva reliably predicts that of serum, its Germany). Subsequent to saliva collection, blood indirect quantification by use of a digital refrac- was collected via jugular vein puncture into 10 mL tometer could represent an easy way for producers vacutainer tubes (VACUETTE, Greiner Bio-One, to classify each calf ’s passive transfer status with- Kremsmünster, Austria). Then, the blood sample was out blood sampling. centrifuged immediately in order to extract serum. The purpose of this observational pilot study With a digital refractometer (same as earlier the Brix was to investigate whether it is possible to detect values of both serum and subsample of (n = 12) and quantify IgG1 in saliva of neonatal calves saliva samples were obtained within 60 min after using both single radial immunodiffusion (SRID) sampling. Serum and saliva samples were thereafter and digital refractometry and to investigate associ- stored at −18 ˚C. Once all samples were collected, ations to both serum IgG and serum Brix. they were submitted in cool, insulated boxes to TINE Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txz001/5298312 by Ed 'DeepDyve' Gillespie user on 05 February 2019 Salivary IgG levels in neonatal calves 3 Mastittlaboratoriet i Molde, Norway, for analyses. To Linear regression showed that saliva IgG signif- determine IgG in saliva and serum, SRID Ultra Low icantly explained variation in serum IgG, model Level and SRID (Triple J Farms, Bellingham, WA, fit was R = 0.20, P = 0.047 (Figure 2). Two of USA) respectively were used according to the man- the outlying saliva IgG values (0.2 and 0.6 g/L ufacture instructions. Lower detection limits of the IgG, respectively) had a strong influence on the two tests are 0.1 and 1.9 g/L, and the detection range regression equation, and removal of the outliers of the digital refractometer was 0% to 85% according resulted in an increase in R = 0.63, P < 0.001 to manufacturers (Triple J Farms). (Figure 3). Mean Brix in saliva were 1.2 (±0.69)% with ranges from 0.0% (one sample) to 2.5%. Saliva IgG Statistical Analysis also correlated significantly with saliva Brix values A normal distribution of serum IgG was con- (n = 12, r = 0.7, P = 0.018). Although a significant firmed by visual inspection (Stata, version 14, correlation between the Brix values of saliva and StataCorp LLC, College Station, TX, USA). Saliva serum IgG measured by SRID was not confirmed IgG was right skewed and Spearman rank correla- (n = 12, r = 0.43, P = 0.155), Brix values of saliva tion coefficients were calculated to investigate asso- did correlate with Brix in serum (n = 12, r = 0.7, ciations between saliva IgG and serum IgG as well P = 0.013). As expected, serum IgG correlated with as saliva Brix, and also serum IgG and serum Brix. serum Brix (n = 20, r = 0.8, P < 0.001). A linear regression was used to determine how well saliva IgG explains variation in serum IgG. Inspection of the residuals in the residuals-vs.-fit- ted values plot (rvfplot command) revealed two outlying cases that were far removed in value from the others. The model was rerun without these outliers to investigate their effect of on the model output. Results from both models are presented. Significance was declared at P < 0.05. RESULTS AND DISCUSSION Mean (±SD) serum IgG was 32.1 (±11.94) g/L ranging from 14 to 54 g/L and mean serum Brix % was 9.9 ± 0.82 ranging from 8.2% to 11.2%. Mean Figure 2. Relationship between serum IgG and saliva IgG meas- saliva IgG was 0.2 (±0.11) g/L ranging from the ured with single radial immunodiffusion in 20 one- to three-d-old dairy calves. The solid horizontal reference line indicates serum IgG levels lowest detectable value, 0.1 g/L (n = 6 samples) to below which calves are diagnosed with failure of passive transfer. The 0.6 g/L. A strong significant positive correlation dotted line indicates the line of best fit. (r = 0.7, P < 0.001) between saliva IgG and serum IgG was found. Except for one sample (0.6 g/L), all samples had values around 0.1 to 0.2 g/L (Figure 1). Figure 3. Relationship between serum IgG and saliva IgG meas- ured with single radial immunodiffusion after removal of two outlying saliva IgG values (n = 18 dairy calves). The solid horizontal reference Figure 1. The frequency distribution of calf saliva IgG in 20 sam- line indicates serum IgG levels below which calves are diagnosed with ples taken from 1- to 3-d-old dairy calves. failure of passive transfer. The dotted line indicates the line of best fit. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txz001/5298312 by Ed 'DeepDyve' Gillespie user on 05 February 2019 4 Johnsen et al. IgG was quantifiable in 14 of 20 of the saliva systemic immunity by passive diffusion from serum samples and the results indicate that saliva IgG (Brandtzaeg, 2013). The design of our study can- can predict that of serum IgG. Saliva IgG of neo- not explain the origin of the IgG1 found in the calf natal calves were higher than that of adult cat- saliva. However, it is likely to be derived from local tle: 0.034 g/L, range 0.017 to 0.050 (Butler, 1983). synthesis, selective transport from the blood, or There was variability in the saliva IgG values, which both (Pedersen, 1973). The study of Husband and should be evaluated using larger study samples. It is Lascelles (1975) indicates that the calves’ self-syn- unknown why IgG in one of the saliva samples was thesized IgG appears first at 32 d postpartum, which threefold that of average IgG. An inadvertent lacer- suggests that the IgG measured in the calves’ saliva ation of the mucous membranes by the metal clamp originated from colostrum. On the other hand, used to hold the cottons swab could potentially cause self-synthesis of IgG1 has been proven already dur- a contamination of the sample, although no appar- ing the first week of life by others (Sasaki et al., ent signs of blood were seen on any of the cotton 1977; Devery et al., 1979). The selective transport swabs. This calf was very lively at sampling, which of IgG1 from plasma to tears has been proven in 4- possibly could influence the measurement of IgG. to 10-mo-old cattle (Pedersen, 1973). A decreased Residual colostrum in the calves’ mouth may also permeability of the calves’ intestinal mucosa to have caused a false inflation in the saliva IgG lev- large molecules, “gut closure,” occurs already sub- els. Measures were taken to prevent this, since milk sequent to the first colostrum-feeding (Michanek was retained for at least 2 h prior to saliva sampling. et al., 1989) and a similar mechanism may occur However, optimal sampling routines with respect to in the oral mucosa (Brandtzaeg, 2013). However, time of the day, time since feeding etc. can be inves- colostral IgG may similarly pass into calf saliva as tigated in future research. Further studies are also Smith et al. (1976) showed that colostral IgG passes needed to investigate saliva IgG with more sensi- into nasal mucus of lambs. Unfortunately, this tive methods. For comparison, Duncan et al. (1972) study did not investigate IgG1 levels in pre-colos- found small amounts of IgG1 have been found in tral saliva that could yield more knowledge on the (juvenile and adult) ruminant tears (0.15 ± 0.09 g/L) origin of the saliva IgG. We encourage future stud- and nasal secretions (0.16 ± 0.12 g/L). IgA and not ies to include this measure to improve the under- IgG is the most abundant Ig in saliva, which affects standing of the saliva IgG kinetics. the total protein content (Butler et al., 1972). The Although only 12 of the calves’ saliva were latter may also affect the indirect quantification of investigated using the digital refractometer, saliva IgG by use of Brix. Owing to low IgG concentra- Brix was associated with saliva IgG. However, tions in saliva relative to IgA, other fluids may be this study could not confirm that saliva Brix % is more suitable for the assessment of passive immu- a valid indirect measure of serum IgG. Possible nity. The studies of Duncan et al. (1972) and Butler reasons for the lack of correlation between serum et al. (1972) revealed higher IgG levels in e.g., nasal IgG and saliva Brix can be related to different frac- secretions, tears, and vaginal secretions. tions and concentrations of Igs in saliva vs. that of Limitations to the dataset exist which should serum (Butler, 1983). A recent review revealed that be taken into consideration while evaluating the the diagnostic accuracy of Brix refractometry to results. Of the saliva samples, 30% had IgG lev- diagnose FPT in calves is varying (Buczinski et al., els below the detection limit of the SRID test 2018). The results of this study could not support (<0.1 g/L). More sensitive methods to quantify that saliva Brix can predict serum IgG. IgG (e.g., enzyme-linked immunosorbent assay or Our study was based on a low number of calves turbidimetric immunoassay) should be explored in and as such results can only provide the basis for future studies (McVicker et al., 2002; Dunn et al., future studies on the relationship between calf serum 2018). The correlation of saliva IgG to other indi- and saliva IgG. However, the usefulness of saliva as rect measures of IgG, as serum total protein, is of a medium to assess calf passive transfer of immunity interest in future research. None of the sampled from colostrum may deserve further attention. calves had serum IgG levels <10 g/L. Therefore, it Conflict of interest statement . None declared. is unknown how the lower serum IgG levels (and thus calves with FPT) can be predicted by saliva ACKNOWLEDGMENTS IgG given that IgG values <0.1 g/L can be quanti- The study was funded by the Norwegian fied using other methods. research funding for agriculture and the food indus- Most of the IgG in human saliva originates try (MATFONDAVTALE; Norwegian Research from the blood circulation, and thus represents Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/advance-article-abstract/doi/10.1093/tas/txz001/5298312 by Ed 'DeepDyve' Gillespie user on 05 February 2019 Salivary IgG levels in neonatal calves 5 biomarkers for maternal behavior in cows—a compari- Council project number 268023). We thank the staff son of beef and dairy cattle. Physiol. Behav. 139:361–368. at the research facility of Norwegian University of doi:10.1016/j.physbeh.2014.10.030 Life Sciences and especially M.M. Taralrud for Godden, S. 2008. 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Journal
Translational Animal Science – Oxford University Press
Published: Jan 21, 2019