J Med Primatol doi:10.1111/jmp.12021
ORIGINAL ARTICLE
Evaluation of 25-hydroxy-vitamin D and parathyroid hormone in Callithrix penicillata primates living in their natural habitat in Brazil Danilo Simonini Teixeira1, Yanna Karla M. Nobrega2, Carlos Enrique Uribe Valencia3, Lenora Gandolfi2, Riccardo Pratesi2 & Luiz Claudio G. Castro2 1 Primatology Center, Institute of Biology, University of Brasilia, Brasilia, Brazil 2 Research Center for Celiac Disease and Pediatric Research Laboratory, University of Brasilia School of Medicine, Brasilia, Brazil 3 Department of Physiological Sciences, Institute of Biology, University of Brasilia, Brasilia, Brazil
Keywords Calltithrix penicillata – New World monkeys – parathyroid hormone – reference values – vitamin D Correspondence Luiz Claudio G. Castro, MD SHIS QI 11 Bloco S Sala 106, 71625-205 Brasilia, Brazil. Tel.: +55 61 3364 0753; fax: +55 61 3364 0753; e-mail:
[email protected] Accepted September 10, 2012.
Abstract Background Vitamin D is a secosteroid hormone with important roles in the control of bone and mineral metabolism of vertebrates and in the maintenance of systemic homeostasis. This study aimed (i) to evaluate the serum concentrations of 25-hydroxy-vitamin D levels [25(OH)D], parathyroid hormone (PTH) and ionized calcium (iCa) of wild Callithrix penicillata (blacktufted marmosets) and (ii) to propose reference ranges for those analytes for free-living marmosets. Methods Blood samples were collected from 15 wild animals and analyzed for 25(OH)D, PTH and iCa. Reference values were calculated following standard analytical criteria. Results The observed mean serum levels (±standard deviation) were 25(OH) D, 61.7 (±20.8) ng/ml; PTH, 275.2 (±34.1) pg/ml; iCai 4.0 (±0.6) mg/dl. Conclusions For free-living marmosets, the proposed physiological range for 25(OH)D is 20.1–103.3 ng/ml and for PTH is 207.0–343.3 pg/dl, with a confidence interval of 95%.
Introduction The vitamin D endocrine system is made up by a set of steroids molecules, enzymes and nuclear receptors acting in almost every cell and tissue of the vertebrate organisms, playing important roles in the regulation of the systemic homoeostasis. Although the vitamin D group of molecules is classically termed as vitamins, they are not, once they are mostly synthesized by the organisms themselves [4, 31]. The active molecule of the group, calcitriol [1,25-dihydroxy-vitamin D or 1,25 (OH)2D], is actually a secosteroid hormone, which is essential for the balance of bone and mineral metabolism, once it is the main regulatory system of calcium and phosphorus levels in the body [23]. It also takes part in the regulation of endogenous antibiotics synthesis by mammals’ defense cells [13], in the modulation of the 364
innate autoimmunity [5] and in the control of cell multiplication and differentiation processes [7]. Vitamin D precursors may be obtained from diet or synthesized by the organism itself. The diet sources of vitamin D are vitamin D2 (ergosterol, the plant-derived form obtainded mainly from eatable fungi) and vitamin D3 (cholecalciferol, the animal form, obtained from deep water fishes such as salmon and cod fish oil). Nevertheless, in humans, the diet-obtained precursors respond for only 10–15% of vitamin D needs [31], being its main source the self-synthesized one (vitamin D3), derived from cutaneous enzymatic reactions induced by ultra-violet B sunlight (UVB) on the skin [4]. New World monkeys present a more restrictive pattern of diet source of vitamin D because, differently from humans and Old World monkeys, they are unable to efficiently use the plant-derived vitamin D2, what makes J Med Primatol 41 (2012) 364–371 © 2012 John Wiley & Sons A/S
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their self-synthesized and/or diet-obtained vitamin D3 essential for their metabolism [20]. The endogenously synthesized vitamin D3 comes from a cascade of biochemical enzymatic reactions. The first pathway of this cascade is a photochemical reaction occurring inside the innermost strata of the epidermis in which the UVB radiation (wavelengths 295–310 nm) breaks the B ring of the resting 7-dehydrocholesterol (7DHC) molecule. 7DHC is transformed in pre-vitamin D3, an unstable molecule that becomes stable after being isomerized to vitamin D3. Vitamin D3 is then released from the skin into blood circulation and is transported bound to vitamin D-binding protein (VDBP) to the liver, where it receives a hydroxyl radical on carbon 25, becoming 25(OH)D. This last reaction is catalyzed by a cytochrome P450 microsomal enzyme (25-hydroxylase, CYP2R1). This product is released into blood also bound to VDBP and reaches the kidneys and other tissues, where another cytochrome P450 enzyme (1-alpha-hyrdroxylase, CYP27B1) promotes the hydroxylation on carbon 1, producing the active metabolite 1,25(OH)2D. This active molecule moves across the cell membrane and binds to its receptor (VDR) in the cytoplasm, which is a member of the nuclear receptor family of transcription factors [22]. This ligand–receptor complex [1,25(OH)2D-VDR] is transported through the nuclear membrane, where it dimerizes with retinoid X receptor (RXR), becoming a heterodimer, 1,25(OH)2 D-VDR-RXR [26]. When this heterodimerized molecule attaches to the vitamin D-responsive element (VDRE) in the DNA strand, some signaling pathways are set off, leading to gene expression or gene repression processes, such as cell multiplication, cell differentiation, protein synthesis and their respective biologic responses. Nevertheless, 1,25(OH)2D presents also fast nongenomic actions, lasting from a few seconds to 60 minutes after its biding to the VDR strategically placed in lipid-enriched cell membrane invaginations called caveolae [16]. Cellular signaling for this type of response occurs through induction of transmembrane voltagedependent ion channels (Ca2+, Cl ), control of Ca2+ influx into cytoplasm and activation of second messengers such as cyclic AMP and phospholipase C [24]. Some examples of these responses are the rapid calcium absorption on the duodenal epithelial cells and insulin exocytosis from pancreatic b-cells to control glucose blood levels. Although 1,25(OH)2D is the active metabolite, its immediate precursor, named calcidiol [25-hydroxyvitamin D or 25(OH)D], has been established as the gold standard for evaluating the body store of vitamin D [10].
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When evaluating the vitamin D metabolism of an organism, it is also important to have in mind the close interaction between the serum levels of 25(OH) D, parathyroid hormone (PTH) and calcium. Lower levels of 25(OH)D lead to decreased intestinal calcium absorption, promoting low serum calcium (hypocalcemia), which is a potent stimulus for PTH release from parathyroid glands. The increased PTH levels take calcium out from bone, the main storage of calcium in the organism, and increase calcium resorption in renal tubules, both mechanisms in an attempt to normalize serum calcium levels, once hypocalcemia may predispose to cardiopulmonary and neurologic disturbances and be life-threatening. During some periods, hypovitaminosis D may not be associated with hypocalcemia but just with higher levels of PTH, once serum levels of calcium have momentaneously been restored to the lower normal range due to the increased PTH. For this reason, measuring 25(OH)D and PTH simultaneously more precise the biochemical evaluation is expected to be. Another aspect to be highlighted is that measurement of ionized calcium (iCa) is a more precise biochemical evaluation than total calcium, once it represents the biological active component of blood calcium. Studies have shown that New World monkeys present a distinct balance of the vitamin D endocrine system, with circulating serum levels of 25(OH)D and 1,25 (OH)2D two to 10 times higher than those found in humans and Old World primates [1, 11], due to an innate end-organ resistance. These animals synthesize and overexpress a nuclear ribonucleoprotein A family called vitamin D response element-binding protein (VDRE-BP), which competes with the heterodimer 1,25 (OH)2D-VDR-RXR for binding to the VDRE in the DNA strand [1, 6]. Consequently, higher levels of 1,25 (OH)2D are necessary to displace the overabundant VDRE-BP and allow the binding of the heterodimer to the VDRE in DNA and set off its signaling pathways and its biologic responses. Interestingly, as gut calcium absorption does not depend on the genomic response, it is well documented in the literature that the higher levels of vitamin D these animals present are not followed by hypercalcemia nor by other metabolic consequences of hypervitaminosis D [25]. Some studies also registered that although the New World monkeys raised in captivity present higher levels of 25(OH)D and 1,25(OH)2D than humans, they might be more vulnerable to rickets, osteomalacia and fractures [1, 33]. This may suggest that their vitamin D levels are not sufficient for an adequate bone mineralization and/or that if the end-organ resistance to 1,25(OH)2D is
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not outmatched, it may somehow impair some metabolic pathways necessary to assure bone strength. According to the most recent platyrrhini systematics and classification [27], the New World primate genera Callithrix belongs to the Tribe Callitrichini from the subfamily Callitrichinae, which in turn belongs to the family Cebidae. The genera Callithrix is found in some biomes of Southeastern, Central and Northeastern Brazil [21, 29]. Due to their small size, easy management and close genetic relationship to humans, callitrichids frequently take part in biomedicine and behavioral sciences researches [30, 34]. Callithrix penicilata species, also known as black-tufted common marmoset, is a small arboreal primate weighting from 300 to 450 g in adulthood and inhabits Central Brazil [12]. This species lives in social groups of 3–5 individuals consisting of the couple and their offspring [8]. In their natural environment, they move constantly throughout a variable area of 0.5–6.5 hectares, roaming daily between 500 and 1000 m [28]. They are omnivorous and their diet is based on fruit, nectar, invertebrates and small vertebrates. They also feed themselves with gum and other plant exudates, which easily obtained once they have anatomic craniofacial and dental adaptations allowing them to gouge trees [9]. Several studies have attempted to establish the normal range for 25(OH)D serum concentrations of for captive callitrichids [11, 32, 37], but there are significant discrepancies among the suggested values. Those differences are probably the result of distinct environmental conditions the studied animals were subjected to, such as length of UVB radiation exposure and concentration of vitamin D3 in their diets. Due to those discrepancies concerning 25(OH)D serum levels for captive callitrichids and to the scarcity of data about its levels in wild animals, this study was designed to recognize the 25(OH)D, PTH and iCa levels in free-living black-tufted marmosets; obtain data to support the proposal of reference range of 25(OH)D, PTH and iCa serum levels for wild callitrichids; and compare the 25(OH)D levels between free-living and captivity-raised animals. The simultaneous measurement of those three analytes (25OHD, PTH and iCa) strengthens a more precise biochemical evaluation, once they are continuously interacting to each other to keep balanced the osteomineral metabolism of the organism. Materials and methods This study was conducted in accordance with all legal requirements of the Brazilian Government for research on animals and was approved by the Ethics Committee of the Institute of Biology of the University of Brasilia. 366
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Subjects of the study For this research, 15 wild black-tufted marmosets were studied. They belong to two different social groups, representing two distinct conservation areas that are part of a wider environmental protection area that spans 25,000 hectares and are located in Brası´ lia, Distrito Federal (DF), Midwest Region of Brazil. Seven animals were from Fazenda Agua Limpa, a 4500-hectare ecologic farm belonging to the University of Brasilia and located between the coordinates 15°31–16°03′S and 47° 42′–48°14′W. The other eight animals were from the Estac¸a˜o Ecolo´gica Jardim Botanico, a 4518-hectare ecologic station area belonging to the Distrito Federal Government, localized between coordinates 15°50′–15°55′S and 47°49′–47°55′W. Both areas are part of the Brazilian highlands which encompasses Distrito Federal and the States of Minas Gerais and Goias. This extensive ecoregion named ‘cerrado’ is the second most important Brazilian biome, with an average altitude of 1000 m and typical tropical savanna vegetation. Its climate is characterized by an average temperature of 25°C, seasonal periods of rain and drought and a mean annual rainfall precipitation of 1600 mm. In February 2011, the animals were caught using automatic Tomahawk-model traps and anesthetized with intramuscular administered 10 mg of ketamine per kilogram of body weight and 1 mg of xylazine hydrochloride per kilogram of body weight. Two milliliters of blood was drawn from the femoral vein of each animal. The blood was centrifuged at 1957 g for 5 minutes, and the resulting serum was collected and frozen at 20°C until use. The serum samples were subsequently processed at the Laboratory of Clinical Analysis of the Hospital das Forc¸as Armadas, in Brası´ lia – DF. Sample analysis The samples obtained from the animals were analyzed for 25(OH)D, PTH and iCa. 25(OH)D levels were measured using chemiluminescence method with Liaison (DiaSorin®: Indianapolis, IN, USA) equipment; PTH levels were evaluated using the Modular (Roche Diagnostics®: Indianapolis, IN, USA) platform, which uses the same methodology; both methods are fully automated. To establish the level of ionized calcium (iCa), the AVL 9180 Electrolyte Analyzer (Roche Diagnostics®) was used, which utilizes the ion-selective electrode methodology. All the used equipment, methods and kits were the same for human samples evaluations, because there is no specific kit for veterinary analysis for those analytes. No reference values for the studied analytes have been established for marmosets yet. J Med Primatol 41 (2012) 364–371 © 2012 John Wiley & Sons A/S
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Statistical analysis Initially, PTH, iCa and 25(OH)D serum levels were analyzed individually for each group, and then data from both groups were compared in terms of means (and standard deviation) and measures of dispersion (percentiles) to investigate whether they were homogeneous or there was any specific interfering factor in one of the groups that would hinder analyzing them altogether, because each group came from two distinct geographical areas. As data from both groups presented similar behavior, all animals were posteriorly analyzed together as whole group. Statistically significant difference was assumed for P values 0.111), age maturity (P > 0.203) neither areas of capture (P > 0.679). As none of the factors (age, gender, location) had any significant effect on the variables, data from both groups were pooled. Pearson’s coefficient showed no statistically significant correlation between PTH and 25 (OH)D (r = 0.004; P = 0.989), PTH and iCa (r = 0.084; P = 0.766), neither between 25(OH)D and iCa (r = 0.469; P = 0.078). Mean values, range of variation (with confidence interval of 95%) and measures of dispersion (in percentiles) for the whole group for PTH, 25(OH)D and iCa levels are shown on Table 2. Figure 2 shows the individual serum levels of 25(OH)D and PTH clustered around their respective means. Table 3 shows the results of the tests for precision and accuracy for the obtained values of PTH, iCa and 25(OH)D, based on %CV, %BIAS and %TE. To analyze the data from the studied animals and as current literature does not register reference values of %BIAS, % CV neither %TE for 25(OH)D, PTH and iCa for wild Table 1 Description of the studied marmosets, grouped according to age and sex
Results For analyzing the outcomes, precision and accuracy evaluations were used to minimize the effect of absent veterinary reference data. Precision and accuracy allow validating the data found in the studied samples using the same validation methodology for human samples. For this methodology of validation, it was used the J Med Primatol 41 (2012) 364–371 © 2012 John Wiley & Sons A/S
Age
Sex Female Male Total
Adult
Juvenile
Total
9 3 12
2 1 3
11 4 15
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Fig. 1 Parathyroid hormone (PTH), 25(OH)D and ionized calcium (iCa) serum levels of each animal, grouped according to the place of origin: Fazenda Agua Limpa (FAL); Estac¸a˜o Ecolo´gica Jardim Botaˆnico (EEJB).
C. penicillata species, it was used the previously validated biological variations of these parameters for humans: the Westgard table [36]. Comparing the values from the free-living animals with the expected values for humans and taking into account the allowed variations for humans, it was observed that PTH measurement showed good precision and accuracy, but iCa values revealed imprecision and inaccuracy. No comparison was possible for 25(OH)D, because values of %CV, % BIAS and %TE for this analyte for humans have not been established yet. Discussion Despite the fact that several publications have investigated vitamin D levels in captive New World monkeys [1, 33], conflicting results are still on debate. In our previous study [32], we measured the levels of 25(OH)D in three different groups of captive C. penicilata with different patterns of sunlight exposure and vitamin D dietary supplementation. The first group had free access to sunlight, but no dietary vitamin D supplementation
and their average levels of 25(OH)D was 121.2 ± 33.3 ng/ml. The second group, receiving limited sunlight exposure (early morning and late afternoon) and vitamin D dietary supplementation, presented an average 25(OH)D level of 115.2 ± 32.1 ng/ml. The third group had no exposure to sunlight but received dietary vitamin D supplementation, and their average 25(OH)D was 53.3 ± 10.4 ng/ml. That study showed that sunlight exposure had more impact than diet supplementation on vitamin D levels. In this recent study of free-living animals, our results showed a mean 25(OH)D value of 61.7 ng/ml (range: 20.1–103.3), lower than the ones found in the groups exposed to sunlight on the previous study. Due to the end-organ resistance to vitamin D presented by New World primates, it would be expected high circulating levels of 25(OH)D to be found in both captive and wild marmosets. Nevertheless, our previous data [32] and some other published data [33] showed higher levels of 25(OH)D in captive marmosets when compared to the wild ones. The outcomes of this current paper is also in agreement with the average 25(OH)D levels of 76.4 ng/ ml (range: 25.5–120) found by Power et al. [25] in wild marmosets (cotton-top tamarins) from Colombia. In some studies, the described higher levels of 25(OH) D for captive animals might have resulted from the vitamin D supplementation those animals received (generally it was used approximately 2500 UI of D3 per kilogram of ration). Nevertheless, as animals receiving non-vitamin D3-supplemented ration also presented higher 25(OH)D levels, another possible reason for this difference may be the safe sunlight exposure captive animals can have, allowing them to synthesize their full potential of 25(OH)D, while wild animals may have to hide inside the vegetation to escape from predators, making them less exposed to UVB sunlight than they should be, compromising their full synthesis potential of 25(OH)D. Those levels might represent their metabolic balance in the natural habitat. From the physiology of vitamin D metabolism, it is known that inappropriate higher levels of 25(OH)D of an organism cannot be attributed to an excessive sunlight exposure, once this excess is controlled through a
Table 2 Mean, range of variation and measures of dispersion for each studied analyte for the whole group (n = 15) Percentiles Analyte
Mean
SD
CI 95%
PTH 25(OH)D iCa
275.2 61.7 4.0
34.1 20.8 0.6
256.3 50.2 3.6
294.0 73.2 4.3
10
25
50
75
100
223.0 32.1 3.4
248.6 45.1 3.6
281.9 60.7 3.8
300.0 80.4 4.2
326.4 94.9 5.0
PTH, parathyroid hormone (in pg/ml); 25(OH)D (in ng/ml); iCa, ionized calcium (in mg/dl); SD, standard deviation; CI, confidence interval.
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Fig. 2 Distribution 25(OH)D and parathyroid hormone (PTH) serum levels clustered around the respective mean values (±SD).
photodegradation process, avoiding self-intoxication [35]. If an animal is exposed to longer periods of sunlight, pre-vitamin D is photodegradated (through UVB foton radiation) to inactive molecules (lumisterol and tachysterol) and vitamin D3 is catabolized to transvitamin D and suprasterol (also inactive compounds). This way the higher 25(OH)D levels found for captive callitrichids in our previous work reflect their innate full and physiological potential to synthesize vitamin D, once they did not receive vitamin D3 supplementation in their ration. This fact would corroborate the hypothesis that the lower 25(OH)D levels found in wild animals would be, at least in part, a consequence of shorter periods of sunlight exposure, although living in their natural habitat. Bone and mineral metabolism is characterized by dynamic and interactive biochemical pathways. 25(OH) D controls intestinal calcium absorption and its serum levels, which, in turn, strongly regulates PTH concentrations. Due to this well-known complementarity among these hormones [PTH and 25(OH)D] and the electrolyte (iCa), they were simultaneously assayed in each sample, attempting to exclude any possible discordance between their concentrations. For humans, PTH and calcium reference levels are well established in the literature [18, 19] but not for calli-
trichids. Data precision and accuracy are necessary for establishing reference ranges for analytes, and these characteristics are evaluated according to the values of %CV, %BIAS and %TE. The observed %CV, %BIAS and %TE for PTH for the marmosets from this study were similar to the ones defined for humans (Table 3), making it suitable to infer that the observed range of PTH (207.0–343.3 pg/ml) would be acceptable as a reliable reference range for these animals. Nevertheless, %CV, %BIAS and %TE values for iCa were very different from the ones defined for humans, with variation greater than the maximum allowed values, suggesting low precision and accuracy for this electrolyte. Serum calcium is sharply controlled in humans and small variations in its levels trigger mechanisms of immediate readjustment, making their biologic variations very narrow. So, it would be necessary more data to find out if marmosets actually present a physiologically wider range for this ion before establishing a reliable reference range. Humans 25(OH)D reference levels are still on debate. Some authors suggest that 25(OH)D sufficiency should be defined for levels >20 ng/ml [3, 23], while others preconize the cut-off point for sufficiency being 30 ng/ml [14]. The upper normal limit is also non-defined. Some studies propose that intoxication is more likely to happen when 25(OH)D levels are >140 ng/ml [17], but data are not consistent overall. For this, %CV, %BIAS and %TE for this analyte for humans are not established yet, not allowing their comparison with the values obtained for the marmosets of this study. Parathyroid hormone levels for marmosets (207.0– 343.3 pg/ml, 95% CI) were much higher than the ones found in humans (12–72 pg/ml, or approximately that in most laboratories kits). The range of iCa (2.8– 5.1 mg/dl, 95% CI) found in those marmosets was wider than the ones established for humans (4.4–5.2 mg/dl, or approximately in most laboratories kits). In conclusion, using the same criteria and analytical procedures routinely established for defining reference
Table 3 Evaluation of precision and accuracy of parathyroid hormone (PTH), 25(OH)D and iCa and comparison between them and the maximum allowable human biological variation counterparts Callithrix penicillata
Humans
Analyte
Expected1
Observed1
Reference2
%CV
%BIAS
%TE
%CV
%BIAS
%TE
PTH (pg/ml) 25(OH)D (ng/ml) iCa (mg/dl)
307.1 67.9 4.0
275.2 61.7 4.0
207.0–343.3 20.1–103.3 2.8–5.1
12.4 33.7 14.3
8.8 9.1 1.5
29.2 64.7 25.1
13.0 – 0.9
8.8 – 0.6
30.2 – 2.1
%BIAS and %TE (total error) for C. penicilata and for humans. %CV, coefficient of variation. 1 Expected and observed mean values of analytes for the studied C. penicillata. 2 Reference range (mean ± 2 SD) of the analytes for the studied C. penicillata. J Med Primatol 41 (2012) 364–371 © 2012 John Wiley & Sons A/S
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values for humans and based on the values found in this current study, we propose that for wild C. penicillata species, independently of gender or age, the reference range of 25(OH)D vary between 20.1 and to 103.3 ng/ ml (mean 61.7 ng/ml) and for PTH between 207.0 and 343.3 pg/dl, with 95% of confidence interval.
Acknowledgments The authors have no conflict of interest to declare. The Celiac Disease and Pediatric Research Laboratory of the University of Brasilia School of Medicine provided the funds for developing this research.
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25(OH)Vitamin D and PTH levels in callitrichids
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