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Thermo-Loggers in Cattle Administered with Lipopolysaccharide

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pISSN 1598-298X / eISSN 2384-0749 J Vet Clin 35(3) : 97-99 (2018)

http://dx.doi.org/10.17555/jvc.2018.06.35.3.97

97

Detection of Fever with Subcutaneously Implanted

Thermo-Loggers in Cattle Administered with Lipopolysaccharide

Younghye Ro*, Jin-Duck Bok**, Hun-Jun Lee**, Sang-Kee Kang**,***, Danil Kim*1 and Yoonseok Lee****1

*Department of Farm Animal Medicine, College of Veterinary Medicine, Seoul National University, Seoul 08826, Korea

**Institute of Green-Bio Science and Technology, Seoul National University, Pyeongchang-gun, Gangwon-do 25354, Korea

***Graduate School of International Agriculture Technology, Seoul National University, Pyeongchang-gun, Gangwon-do 25354, Korea

****Department of Biotechnology, College of Agriculture & Life Science, Hankyong National University, Anseong-si, Gyeonggi-do 17579, Korea

(Received: October 20, 2017 / Accepted: June 08, 2018)

Abstract : The aim of this study is to determine whether subcutaneous temperature (ST) was correlated with rectal temperature (RT) in cattle with inducing artificial fever. In order to determine the correlation between their temperatures, the experiment was performed as follow: Among nine Holstein steers, lipopolysaccharide (LPS) was intravenously administered at a dose of 0.5µg/kg of body weight to six Holstein steer, then, 6 ml of saline was administrated to three steers as a control group. After LPS injection, ST was recorded using subcutaneously implanted thermo-logger sensors at 10-min intervals, and RT was measured using a digital thermometer at 0, 1, 2, 3, 4, 8 and 12 h. In steers with LPS injection, RT was highest at 3 to 4 h and recovered to a pre-challenge temperature at 8-22 h. A similar fluctuation was shown in ST except for an unexpected decrease at 1 h, and a positive correlation between RT and ST was observed in LPS-challenged steers (r = 0.497, P = 0.04). This result suggests that ST could be utilized as an index for early detection of infectious diseases or physiological events.

Key words : Holstein steer, early disease detection, thermo-logger sensor, lipopolysaccharide challenge, subcutaneous temperature.

Introduction

In the domestic livestock industry, the number of large- scale farm has been increasing because of decline in the agri- cultural workforce as well as the increasing age of agricul- tural workers. Approximately 3.48 million cattle and pigs had been buried in South Korea during the FMD outbreak in 2010 to 2011, causing a property loss of more than 3 billion dollars (5). In a case study of a simulated outbreak of FMD in California, 565 million US dollar of additional economic damage was forecasted for every hour delay of detection after 21 days, which emphasizes the importance of early detection methods (2). In order to prevent massive economic damage, an early detection system of pandemics in domestic animals should be established.

Early detection methods for pandemics in domestic ani- mals include body temperature monitoring systems that could alert farm workers to deal properly and promptly with the sit- uation (2). In homeotherms, fever is a complex physiological reaction to maintain homeostasis and is an important defense mechanism against infection and inflammation. Thus, eleva- tion of body temperature could be one of the primary diag-

nostic symptoms for clinical viral or bacterial infections (3) and the most useful measurable indicator of many economi- cally important events in cattle, such as calving and estrus (1). Thus, body heat monitoring is central to early detection of infectious diseases as well as physiological events.

In a previous study, the authors showed that body temper- ature could be monitored in healthy cattle by using thermo- loggers subcutaneously implanted in the upper scapula region (4), and it was needed to evaluate the thermo-loggers in feverish animals. Therefore, the aim of this study is to deter- mine whether subcutaneous temperature (ST) recorded by subcutaneously implanted thermo-logger sensors is correlated with rectal temperature (RT) in hyperthermic cattle that were artificially induced with a lipopolysaccharide (LPS).

Materials and Methods

Animal protocols were approved by the Institutional Ani- mal Care and Use Committee of Seoul National University;

all applicable national laws and university policies regarding the care and use of animals were followed during the experi- ment (SNU-140217-4). Nine Holstein steers (18 month-old, 565 ± 15 kg) were used in this study. During the experiment (average cowshed temperature 4.89 ± 1.57oC), steers were housed together in a free stall barn, without any heating sys- tem, which was enclosed with solid fences and a roof. The

1Corresponding author.

E-mail: yoonseok95@hknu.ac.kr, danilkim@snu.ac.kr

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98 Younghye Ro et al.

steers were given concentrated feed according to guidelines outlined in the manufacturer’s beef cattle rearing program (Cargill Agri Purina, Inc., Sungnam, Korea). Rice straw, min- eral blocks, and water were provided ad libitum.

Button-shaped digital thermo-loggers (iButton DS1922L, Maxim Integrated, San Jose, CA, USA) were used to mea- sure ST and were preset to measure body temperature at 10- min intervals. The iButton thermo-loggers were surgically implanted around the upper scapula one month prior to the experiment by a veterinarian (Fig 1) using a previously re- ported method (4). For six steers, LPS (produced from E. coli 055:B5, and reconstituted with 0.9% sterile saline solution to 10µg/mL; Sigma-Aldrich) was administered into the jugular vein at a dose of 0.5µg/kg of body weight. For three steers (control group), a physiological saline solution was adminis- tered using the same protocols as for the LPS challenge group. A digital thermometer MT-16C2 (Microlife AG, Wid- nau, Switzerland) was used to measure RT which was mea- sured seven times at 0, 1, 2, 3, 4, 8, and 12 h. Data on ST were collected every 10 min from 2 h before administration to 22 h after administration. Data were computationally ana- lyzed using the OneWireViewer program (Maxim Integrated Products). In order to determine the correlation between ST and RT, the collected data were analyzed using ‘cor’ func- tion in R program. Correlation results are expressed as Pear- son’s correlation coefficients.

Results and Discussion

The change in the pattern of RT and ST during LPS chal- lenge test from 2 h before to 22 h after LPS administration in

Holstein steers is shown in Fig 2. After LPS administration, the highest RT was 40.75oC at 3 to 4 h. Thereafter, RT grad- ually decreased and returned to the level before administra- tion. In contrast, ST showed a biphasic increase in LPS- challenged steers, with a peak at 38.52oC at 3 h and 39.45oC at 4 h. A mildly elevated ST (38.67 to 38.23oC) was ob- served from 6 to 8 h, which returned to pre-dose levels 12 h after LPS administration. No significant change in ST was measured in the control group. After LPS injection, how- ever, ST rapidly dropped from 36.77oC to 35.21oC until 1 h, which was consistent with the results reported by Reid et al.

(6). This drop in body temperature indicated that the increased ST was a hypothermic response to bacterial lipopolysaccharide administration (6,7). As shown in Table 1, the correlation between RT and ST was positive during the LPS challenge test (r = 0.497, P < 0.05).

As an index of body temperature, RT has been used in bovine practice, and is maintained in a narrow range (38.00- 39.00oC) in healthy adult cattle. However, ST near the upper scapula obtained with thermo-logger sensors was more vari- able (36.56~37.98oC) in healthy steers (4) and was suspected to be affected by environmental factors as well as the state of peripheral circulation. Nevertheless, subcutaneously implanted thermo-logger sensors could detect an artificially induced fever and provided data positively correlated with tempera- ture measured from the rectum of steers in this study. This result suggested that an ST monitoring system can immedi- ately inform farm workers of the occurrence of pathological or physiological events increasing body temperature. A prompt alarm system is a very useful tool for the livestock industry, enabling detection of the outbreak of pandemics in the earliest stage, thus providing a chance to prevent the Fig 2. The pattern of RT and ST during LPS challenge from - 2 h (before administration) to 22 h (post-administration) in Hol- stein steers: a) the rectal temperature, b) the subcutaneous tem- perature as a control group, c) the subcutaneous temperature in Holstein steer injected with LPS.

Fig 1. The iButton thermo-loggers were surgically implanted around the upper scapula.

Table 1. Correlation between rectal temperature (RT) and subcutaneous temperature (ST) recorded from implantable thermo-loggers in Holstein steers during a lipopolysaccharide challenge test

Site temperature Time (h)

Mean ± SD r P-value

0 1 2 3 4 8 12

ST 36.77 35.21 36.52 38.52 39.45 38.24 36.02 37.24 ± 1.54

0.497 0.04

RT 38.85 39.65 39.95 40.75 40.75 39.05 38.35 39.62 ± 0.93

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Subcutaneous Temperature is a Useful Tool for Early Detection of Diseases 99

spread of disease (6).

Conclusion

We revealed a positive correlation between ST obtained with thermos-logger senor and RT in Holstein steers. The results suggest that subcutaneously implanted thermo-logger sensors can detect fever, which was confirmed by using the LPS challenge test and measuring RT in an artificially induced fever in steers. Therefore, temperature recorded by subcuta- neously implanted thermo-logger sensors can be useful for the early detection of pandemics in domestic animals.

Acknowledgements

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through Agri-Bio Industry Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (315090-3).

References

1. Bewley JM, Schutz MM. Recent studies using a reticular bolus system for monitoring dairy cattle core body tempera- ture. The First North American Conference on Precision

Dairy Management 2010.

2. Carpenter TE, O'Brien JM, Hagerman AD, McCarl BA.

Epidemic and economic impacts of delayed detection of foot- and-mouth disease: A case study of a simulated outbreak in California. J Vet Diagn Invest 2011; 23: 26-33.

3. Dalal S, Zhukovsky DS. Pathophysiology and management of fever. J Support Oncol 2006; 4: 9-16.

4. Lee Y, Bok JD, Lee HJ, Lee HG, Kim D, Lee I, Kang SK, Choi YJ. Body temperature monitoring using subcutaneously implanted thermo-loggers from Holstein steers. Asian-Australas J Anim Sci 2016; 29: 299-306.

5. Park JH, Lee KN, Ko YJ, Kim SM, Lee HS, Shin YK, Sohn HJ, Park JY, Yeh JY, Lee YH, Kim MJ, Joo YS, Yoon H, Yoon SS, Cho IS, Kim B. Control of foot-and-mouth disease during 2010-2011 epidemic, South Korea. Emerg Infect Dis 2013; 19: 655-659.

6. Reid ED, Fried K, Velasco JM, Dahl GE. Correlation of rectal temperature and peripheral temperature from implantable radio-frequency microchips in Holstein steers challenged with lipopolysaccharide under thermoneutral and high ambient temperatures. J Anim Sci 2012; 90: 4788-4794.

7. Steiner AA, Molchanova AY, Dogan MD, Patel S, Pétervári E, Balaskó M, Wanner SP, Eales J, Oliveira DL, Gavva NR, Almeida MC, Székely M, Romanovsky AA. The hypothermic response to bacterial lipopolysaccharide critically depends on brain CB1, but not CB2 or TRPV1, receptors. J Physiol 2011; 589: 2415-2431.

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