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Effects of Age and Sex on the Hematology and Blood Chemistry of Tibetan Macaques (<I>Macaca Thibetana</I>)

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Effects of Age and Sex on the Hematology and Blood Chemistry of Tibetan Macaques (<I>Macaca Thibetana</I>) Journal of the American Association for Laboratory Animal Science Vol 53, No 1 Copyright 2014 January 2014 by the American Association for Laboratory Animal Science Pages 12–17 Effects of Age and Sex on the Hematology and Blood Chemistry of Tibetan Macaques (Macaca thibetana) Di Wu,1 Yong Yi,4 Fei Sun,2 Liang Zhou,4 Feng Yang,4 Hongxing Wang,4 Guodong Zhang,5 Yu Alex Zhang,1 and Feng Yue3,* Tibetan macaques (Macaca thibetana), also known as Chinese stump-tailed macaques, are a threatened primate species. Although Tibetan macaques are Old World monkeys in the genus of Macaca, limited age- and sex-related physiologic data are available for this particular species. We used 69 apparently healthy Tibetan male and female macaques to explore the effect of age and sex on physiologic parameters. Somatometric measurements, biochemistry, and hematologic parameters were analyzed. Significant age-related differences were found for weight, BMI, RBC count, Hgb, Hct, neutrophils, eosinophil count, ALT, AST, ALP, GGT, creatine kinase (muscle and brain subtypes), LDH, α-amylase, creatinine, apolipoprotein A1, total protein, albumin, cholesterol, HDL, and potassium. Significant differences by sex were noted for weight, BMI, ALT, total bilirubin, and indirect bilirubin. An interaction between age and sex accounted for statistically significant differences in the values for weight, BMI, and lymphocyte and eosinophil counts. These physiologic data will provide veterinarians and researchers with important age- and sex-specific reference ranges for evaluating experimental results from Tibetan macaques. Hematologic and biochemical values are of great importance in modest correlations between age and various hematologic and evaluating the wellbeing or pathologic conditions of nonhuman biochemical parameters in Tibetan macaques younger than 10 y.33 primates. However, many factors including but not limited to However, statistical correlation in this relatively small group did not handling stress, relocation, fasting, and anesthesia can affect he- necessarily demonstrate the effect of age and sex on the physiologic matologic and biochemical parameters in marmosets, cynomolgus parameters in Tibetan macaques. and rhesus macaques, and chimpanzees.11,13,17,35 Changes in many The purpose of this study was to determine the effects of hematologic and biochemistry parameters have been reported age and sex on the hematologic and serum biochemical param- during normal development and maturation in various nonhuman eters of a laboratory colony of 69 apparently healthy Tibetan primates. A previous study reported that the albumin:globulin macaques and to establish clinically relevant reference ranges ratio, BUN, BUN:creatinine ratio, and triglyceride concentration for all ages of adults of both sexes. changed most with age in rhesus macaques, according to data from the Primate Aging Database.25 In addition, significant dif- Materials and Methods ferences by sex have been noted in many New World and Old Animals. In the current study, we used 69 apparently healthy 20,22,31 World primates. Understanding the effect of age and sex on Tibetan macaques that originated from wild macaques from south- hematologic and serum biochemical parameters will help us to west China and that were colony-bred at the Institute of Laboratory distinguish the boundaries between normal changes and diseases- Animal Sciences, Sichuan Academy of Medical Sciences (Chengdu, related changes and to pave the way to identify other factors or China). All animals were group-housed in clean indoor–outdoor conditions that may affect those parameters. primate facilities and fed commercial monkey chow (Foshan T and Tibetan macaques, an Old World primate belonging to the su- F Pet Food, Foshan City, China) twice daily, fruits daily, and freely perfamily of Cercopithecoidea, range from eastern Tibet east to available purified water supply. The sample population were was Guangdong and north to Shanxi in China and recently have been free of the following pathogenic microorganisms: Salmonella spp., 12 reported as far south as northeastern IndiaIndia. Tibetan macaques Shigella spp., Mycobacterium tuberculosis, pathogenic dermal fungi, are the largest species of macaque and one of the largest nonhuman helminths, ectoparasites, B virus, simian T lymphotropic virus, and primates known to live in Asia. Several features make these animals simian type D retrovirus. Testing for simian T lymphotropic virus potentially useful for experimental studies and include their long and simian type D retrovirus was done by Xishan Biotechnology lifespan (greater than 20 y), large body size, and calm temperament. (VRL China, Suzhou City, China). Macaques were housed in indi- They have been approved for use in scientific research by the State vidual cages for about 1 wk before blood sampling. All adult female Forestry Administration of the People’s Republic of China and have macaques were considered to be nonpregnant via daily observation been used in studies of intraocular pressure measurement and gene of menses in the morning prior to blood sampling. 29,34 analysis. In a previous report, we found strongly positive cor- All experiments were conducted in compliance with national relations between age and various somatometric parameters and and provincial guidelines and in accordance with the Guide for the Care and Use of Laboratory Animals,8 as sanctioned by the Received: 31 Jan 2013. Revision requested: 16 Mar 2013. Accepted: 24 Jun 2013. Institute of Laboratory Animal Sciences, Sichuan Academy of 1Cell Therapy Center, 2Beijing Geriatric Healthcare Center, and 3Department of Neuro- Medical Sciences. This study was approved by the Animal Use biology, Beijing Institute of Geriatrics, Xuanwu Hospital, Capital Medical University, and Care Board of the Institute of Laboratory Animal Sciences, 4 Beijing, China; Institute of Laboratory Animals of Sichuan Academy of Medical Sciences Sichuan Academy of Medical Sciences. and Sichuan Provincial People’s Hospital, Chengdu, Sichuan Province, China; 5Wincon Laboratory, Wincon TheraCells Biotechnologies, Nanning, Guangxi Province, China. *Corresponding author. Email: [email protected] 12 Physiologic parameters of Tibetan macaques Table 1. Demographics of adult Tibetan macaques Female Male Young Mature Old Young Mature Old Number 13 15 5 13 11 12 Age (y) 3.62 ± 0.65 10.1 ± 1.5 17.4 ± 2.0 3.62 ± 0.78 12.3 ± 1.0 19.2 ± 4.0 Age range (y) 3–5 8–13 15–20 3–5 10–13 15–28 Weight (kg)a,b 3.95 ± 0.76 11.0 ± 1.5 9.6 ± 1.0 4.46 ± 1.52 18.0 ± 3.8 17.2 ± 3.3 BMIa,b 18.3 ± 2.4 32.3 ± 4.9 27.9 ± 3.6 19.4 ± 4.0 40.6 ± 5.3 38.6 ± 8.0 aSignificant (P < 0.05) difference according to age. bSignificant (P < 0.05) difference according to sex. One monkey year is approximately equal to 3 human years Results 15 in terms of skeletal changes. However, limited data about de- Demographic information, hematology and biochemistry velopment and maturation was available for Tibetan macaques. values are presented in Tables 1, 2, and 3, respectively. The Based on relevant information for cynomolgus and rhesus results of statistical analyses according to age, sex, and their 9,32 monkeys, Tibetan macaques were divided into 3 age groups interaction are shown in Table 4. in this study: young adults (3 to 5 y old), mature adults (8 to 13 Significant (P < 0.05) age-related and sex-associated differ- y old), and old adults (older than 15 y; Table 1). ences were found for both weight and BMI. For hematologic Somatometric measurements and blood sample collection. parameters, significant (P < 0.05) age-related differences were Somatometric measurements were done while monkeys were found for RBC count, Hgb, Hct, and neutrophil and eosinophil anesthetized with ketamine (10 mg/kg IM). BMI was calcu- counts. For biochemistry parameters, significant (P < 0.05) age- lated according to body weight (in kilograms) divided by related differences were noted for AST, ALT, ALP, GGT, creatine the square of the crown–rump length (in square meters), as kinase (muscle and brain subtypes), LDH, α-amylase, creatinine, 10 done for rhesus macaques. To avoid any potential influence apolipoprotein A1, total protein, albumin, cholesterol, HDL, and of handling-associated stress on chemistry and hematologic K concentrations. Significant (P < 0.05) differences by sex were parameters, blood samples were drawn during somatometric present for ALT and total and indirect bilirubin. An interac- measurements. Blood samples were obtained from the saphen- tion (P < 0.05) between age and sex accounted for significant ous vein of macaques after a 16-h fasting period. Tubes coated differences in the values for weight, BMI, lymphocytes, and with K2-EDTA were used to collect samples for CBC analysis, eosinophils. trisodium citrate tubes were used to assess coagulation, and Compared with young adults, mature and old Tibetan serum separation tubes were used for chemistry parameters, macaques had higher (P < 0.05) values for weight, BMI, neu- electrolytes, and hormones. trophils, and creatinine and lower (P < 0.05) values for RBC, Analysis of biochemistry and hematologic parameters. Bio- Hgb, Hct, AST, ALT, ALP, GGT, creatine kinase (muscle and chemistry measurements were performed on serum samples brain subtypes), LDH, and albumin. Young and mature adult by using an autoanalyzer (model BS 420, Mindray DS, Shen- Tibetan macaques had more (P < 0.05) eosinophils values than zhen, China) and included total bilirubin, direct bilirubin, did old macaques. Cholesterol, HDL, α-amylase, and
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