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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION |
lu*
,1
* Department of Animal Science, Faculty of Agriculture, and Department of Embryology and Histology, Faculty of Medicine, Ege University, Izmir, Turkey; and Institute of Animal Sciences, Volcani Center, Bet Dagan, Israel
1 Corresponding author: pines{at}agri.huji.ac.il
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: collagen type II • alkaline phosphatase • osteopontin • heat-shock protein 90 • incubation temperature
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Various dietary (Sauveur, 1984; Rennie et al., 1993; Thorp et al., 1993), environmental (Wong-Valle et al., 1993), and genetic factors (Leach and Lilburn, 1992) have been found to be involved in the etiology of the disease. Nutritional factors that influence its incidence include electrolyte balance, calcium-to-phosphorus ratio (Rennie et al., 1993), 1,25-dihydroxy vitamin D3 and 25-hydroxycholecalciferol (Rennie and Whitehead, 1996; Ledwaba and Roberson, 2003), excessive levels of Cys and homocysteine (Bai and Cook, 1994), and ascorbic acid (Edwards 1989). The mycotoxin fusachromanone and the dithiocarbamates thiram and disulfuram induce the occurrence of severe TD lesions (Rath et al., 2005). The only treatments that consistently decrease the incidence of TD are those that restrict growth rate (Huff, 1980; Su et al., 1999) and high levels of vitamin D and its metabolites (Elliot and Edwards, 1997; Edwards, 2000; Ledwaba and Roberson, 2003; Whitehead et al., 2004).
One of the parameters known to affect chondrocyte proliferation and differentiation is heat stress. Heat stress causes the production of a wide range of heat-shock proteins, located at different zones of rat and chicken embryonic growth plates, which suggests that there are different activities at different stages of differentiation (Neri et al., 1992; Otsuka et al., 1996; Van Muylder et al., 1997). The new patterns of proteins synthesized by chondrocytes exposed to heat stress, such as the heat-shock proteins, are probably involved in the cell-cell interactions necessary for chondrocyte differentiation and cartilage differentiation. For example, degradation of the differentiation-dependent aggrecan proteoglycan in the extracellular matrix by chicken chondrocytes is temperature dependent (Alonso et al., 1996). Correlations between changes in temperature and leg abnormalities were also demonstrated in young rats (Kawashima and Yano, 1988) and in posthatch broilers (Hulan and Proudfoot, 1987; Bruno et al., 2000).
In recent years, there has been considerable interest in exposure of broiler embryos to changes in incubation temperatures, to enhance postnatal adaptation of growing broilers to different environmental temperatures (Tzschentke and Basta, 2002; Yahav et al., 2004; Yalç
n et al., 2005). Indeed, the incubation period has been characterized as one of the most critical determining factors of overall broiler performance, from hatching to the end of the growth period. The incubation temperature is typically 37.5°C for embryos of poultry species, and small deviations from the optimum can have significant impacts on chick weight and quality (Wilson, 1991; Decuypere and Michels, 1992; Tona et al., 2005). However, information regarding the effects of changes in incubation temperatures on skeletal development is very limited. Yalçn and Siegel (2003) showed that deviation from control incubation temperatures affected the development of different skeletal traits at different rates and resulted in large relative asymmetries, but the rates converged and resulted in developmental stability prior to hatching.
In the present study, we evaluated the effects of temperature during the early and late stages of bone formation, within the incubation period, on the differentiation of growth plate chondrocytes, as correlated with the incidence of TD.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Experimental Procedure
A total of 2,400 eggs were obtained from a Ross broiler breeder flock at 38 wk of age. The eggs were stored at 16°C and 75% RH for 4 d prior to incubation. They were then divided into 5 groups (480 eggs/treatment) and were incubated at the following temperatures in 5 incubators. In group 1, control eggs were incubated at 37.8°C; in group 2, a low incubation temperature (36.9°C for 6 h/ d) was used on d 0 to 8 of incubation; in group 3, a low incubation temperature (36.9°C for 6 h/d) was used on d 10 to 18 of incubation; in group 4, a high incubation temperature (39°C for 6 h/d) was used on d 0 to 8 of incubation; and in group 5, a high incubation temperature (39°C for 6 h/d) was used on d 10 to 18 of incubation. Relative humidity was maintained at 60%.
Eggs were turned once per hour at an angle of 90° from 0 to 18 d of incubation. There were 4 replicate trays of 120 eggs for each temperature treatment. Eggs were transferred to a hatcher unit at 18 d of incubation and kept at 37.8°C and 70% RH until hatching. At 14 d of incubation, 10 eggs were sampled, weighed, and the embryos removed. Embryo weight was expressed as a percentage of the present egg weight. At hatch, 10 chicks were also sampled and weighed from each group. Embryos and chicks were killed by cervical dislocation, and the left tibia was immediately removed for histology. The right leg was removed, cleaned of any adhering tissue, and weighed, and the tibia was weighed and dried overnight at 110°C; samples were then ashed at 600°C for 12 h to determine the tibia ash content, which was expressed as the percentage of ash. The tibia calcium content was also determined by atomic absorption spectrophotometry.
During hatching, the number of chicks hatched was recorded and the percentage of hatchability was calculated on the basis of the number of chicks hatched as a percentage of the number of fertile eggs per treatment. Eggs that failed to hatch were opened, and infertile eggs and embryonic mortalities at early, mid, and late stages were determined. After hatching, 90 chicks per hatching temperature (a total of 450 chicks) were individually weighed, wing-banded, and placed into 15 floor pens containing 14 birds/m2. The poultry house was window-sided with controlled temperature and ventilation. The temperature was set at 32°C on the day of hatching and was reduced to 24°C at a rate of 2.5°C/wk. A continuous lighting schedule of 23:1 h (L:D) was operated during the 49-d rearing period. The birds were fed a broiler starter diet with 23% protein and ME of 3,120 kcal/kg from d 0 through 10, a grower diet with 22% protein and ME of 3,130 kcal/kg from d 11 through 21, and a finisher diet with 20% protein and ME of 3,240 kcal/kg from d 22 through 49. Water was available ad libitum. Body weights were measured individually on d 21 and 49, and sex was determined on d 49. Three males representing the average weight of the replicate (9 males per incubation temperature) were chosen on d 49 and killed by cervical dislocation. Tibia weight, and tibia ash and calcium contents were determined in the right tibia. At slaughter, all birds were examined for TD prevalence: the right tibia of each bird was removed and TD was determined by making a longitudinal cut across the metaphysis and determining the severity of TD according to Edwards and Veltmann (1983).
Preparation of Growth Plate Sections, Immunohistochemistry, and In Situ Hybridization
After the chicks had been killed by cervical dislocation, the tibias were removed immediately and fixed overnight in 4% paraformaldehyde in PBS at 4°C. Serial 5-µm sections were prepared after the samples had been dehydrated in graded ethanol solutions, cleared in chloroform, and embedded in Paraplast (Shandan, Runcorn, UK). For hybridization, the sections were deparaffinized in xylene, rehydrated through a series of graded ethanol solutions, rinsed for 5 min in distilled water, and incubated in 2x SSC (1x SSC contained 0.15 M NaCl and 0.015 M sodium citrate) at 70°C for 30 min. The sections were then rinsed in distilled water and treated with pronase (0.125 mg/ mL in 50 mM Tris-HCl, 5 mM EDTA, pH 7.5) for 10 min. After digestion, the slides were rinsed with distilled water, postfixed in 10% formalin in PBS, blocked in 0.2% Gly, rinsed in distilled water, rapidly dehydrated through graded ethanol solutions, and air-dried for several hours. Heat-shock protein 90 was detected by immunohistochemistry with Hsp90 antibodies at a 1:100 dilution. Parallel sections were stained for AP activity (Knopov et al., 1995) and hybridized with digoxigenin-labeled avian collagen type II and OPN probes (Knopov et al., 1997; Pines et al., 1999). In all hybridizations, no signal was observed with sense probes that were used as controls. All the preparations for in situ hybridization within each experiment were performed simultaneously, with the same probe and with the same specific activity, and all sections were dipped in emulsion and exposed for the same length of time.
Statistical Analyses
The GLM procedure of SAS (SAS Institute, 1999) was used to analyze the data. One-way ANOVA was applied to the prehatching bone data. Effects of incubation temperature, sex, and their interaction were included in the model to analyze the data on BW and bone parameters at 49 d. Means were separated by Tukey’s test when appropriate. Because there were birds with differing TD scores, the data were reclassified as 0 (normal) and 1 (with TD) prior to the analysis. The chi-squared test was applied to the data on TD incidence, as separated among incubation temperature groups and between sexes; when found significant, the chi-squared test was also used in pairwise comparisons of treatments. The level of significance used in all results was P < 0.05. Evaluation of growth plate chondrocyte differentiation markers was performed by counting the number of cells per column expressing them (10 columns/slide, 5 slides/chick from 5 different chicks). Data were subjected to 1-way ANOVA and the results are represented as the mean ± SE according to Duncan’s multiple range test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Effect of Incubation Temperature on BW
Changing the incubation temperature, by cooling during the early or late stage or by heating at the late stage of embryo development, did not depress embryo weight on d 14 of embryo development. Only the effect of increased incubation temperature in the early stages of embryo development reached statistical significance on d 14 of incubation. At hatch, chick weight in all treatment groups increased compared with the control. At 21 and 49 d of age, control chicks exhibited the highest weight among all treatments. Body weight gain was 36.5 g/d from 0 to 21 d for control broilers, whereas the treatment groups gained an average of 30.5 g/d. At 49 d of age, although the control chicks were still the heaviest, the differences were not statistically significant (Table 1
). A significant incubation temperature x sex interaction showed that in females, the reduced growth was fully compensated for by d 49. Males from eggs cooled from d 10 through 18 of incubation had BW similar to the controls, whereas males from eggs cooled or heated from d 0 through 8, or heated from d 10 through 18 of incubation had lower BW (Table 2).
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). At hatch, control embryos had the heaviest tibia weights. The lightest tibia weights were found in chicks exposed to heat from d 10 through 18.
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The incidence of TD at 49 d posthatch was affected by the incubation temperature. Only cooling or heating from d 0 through 8 in the early stages of embryo development was associated with a higher prevalence of TD. No effect of incubation temperature on the frequency of TD incidence was noticeable when eggs were cooled or heated from d 10 through 18 of incubation (Table 3
). The effect of sex on TD incidence was not significant: 9.6% (28 out of 292) for males and 7.2% (23 out of 321) for females.
Effect of Incubation Temperature on Growth Plate Chondrocyte Differentiation
Tibial dyschondroplasia has been suggested to result from the failure of chondrocytes to undergo the complete differentiation necessary for cartilage vascularization and mineralization (Praul et al., 2000). Therefore, activities of 3 differentiation markers, namely, collagen type II, OPN, and AP, were used to assess the effect of incubation temperature on the differentiation status of the growth plate chondrocytes at hatch (Figures 1 to 3).
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). In the control growth plate, very low expression of collagen type II was observed in the articular cartilage (AC), and the PZ was populated with a small number of chondrocytes expressing collagen type II in each column (45 ± 6 cells/column), resulting in a narrow zone. Reducing or elevating the incubation temperature in the early stages of embryo development caused a major increase in collagen type II gene expression by the AC. In addition, the PZ of the growth plate was wider than that in the controls and the number of chondrocytes populating each column was much higher (85 ± 5 vs. 79 ± 6 cells/column, respectively), suggesting that the cells did not undergo differentiation. No such changes in collagen type II expression by AC or PZ chondrocytes were observed at the time the temperature was altered at a later stage of embryo development, even though a slight decrease compared with the control was observed in the growth plate chondrocytes (35 ± 4 vs. 30 ± 5 cells/column after a decrease or increase in incubation temperature, respectively).
Alkaline phosphatase activity is exhibited exclusively by differentiated and mature chondrocytes; it marks the hypertrophic zone (HZ) of the growth plate. A high level of AP activity was observed in the HZ, but not in the PZ, of growth plates of chicks hatched from eggs incubated at the control temperature and evaluated at hatch. The HZ of the control chicks were populated with long columns of chondrocytes that exhibited AP activity (120 ± 11 cells/ column). Altering the incubation temperature in the early stages of embryo development caused a major reduction in AP activity, again suggesting a delay in chondrocyte differentiation. The effect was more pronounced when the incubation temperature was reduced than when it was elevated (35 ± 6 vs. 61 ± 8 cells/column, respectively). Although in the control growth plates most, if not all, of the cells of the HZ exhibited AP activity, very few did so after the reduction in incubation temperature (Figure 2). Altering the incubation temperature during the late stages of embryo development did not cause changes in AP activity in the chondrocytes of the HZ (111 ± 10 vs. 107 ± 11 cells/column after a decrease or increase in the incubation temperature, respectively).
Another gene that marks the onset of differentiation and calcification is OPN (Figure 3). Compared with the controls (66 ± 8 cells/column), much longer columns, populated by chondrocytes exhibiting the OPN gene, were observed in the growth plates exposed to the changed temperature in the early stages of development (114 ± 11 vs. 109 ± 14 cells/column after a decrease or increase in the incubation temperature, respectively), whereas almost no changes were observed when the incubation temperature was altered at a later stage (71 ± 8 vs. 77 ± 9 cells/column after a decrease or increase in the incubation temperature, respectively).
Effect of Incubation Temperature on Hsp90 in the Tibia Growth Plate
Heat-shock protein 90 is the most abundant cytoplasmic chaperone of eukaryotic cells; as such, it is involved in developmental regulatory networks and in communication within and between cells. It conceals developmental and stochastic variations that otherwise cause abrupt morphological changes in a large variety of organisms (Rutherford et al., 2007). At hatch, very low levels of Hsp90 were detected in chondrocytes of the maturation zone of the growth plates from chicks incubated at the control temperature (Figure 4). A major increase in Hsp90 levels was observed in growth plates of chicks kept at a high incubation temperature in the early stages of development. In these growth plates, the articular chondrocytes, chondrocytes of the HZ, and some of the chondrocytes of the PZ exhibited Hsp90. In the PZ, the chondrocytes that exhibited Hsp90 were not scattered randomly but were organized in columns. On the other hand, when eggs were incubated at a high temperature at a later stage of differentiation, only a slight increase in Hsp90 was observed, and was seen exclusively in cells of the HZ. The lower incubation temperature caused almost no changes in the levels of Hsp90 compared with the controls. At d 14 of incubation, early changes in the incubation temperature in either direction caused increased Hsp90, especially among hypertrophic chondro-cytes and adjacent proliferating chondrocytes (Figure 5). Changes in the incubation temperature from d 10 through 14 of incubation did not alter Hsp90 levels.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The results demonstrated that broiler embryos were more sensitive to temperatures changes during the early stages of embryo development, although hatching success was similar among groups. These results are in agreement with the report of French (1997), who concluded that embryos appear to be more sensitive to suboptimal temperatures at the beginning of the incubation period. The results clearly showed that any deviation from the control incubation temperature caused a reduction in BW at 21 d of age, although growth retardation was compensated for by d 49. Growth retardation obtained at 21 d was consistent between sexes, because there was no significant incubation temperature x sex interaction on d 21. The results suggested that male chicks incubated at a higher temperature and subsequently placed in standard brooding conditions had the lowest BW at 49 d, whereas male chicks that were incubated at a lower temperature had BW similar to the controls. This is consistent with the conclusions of Yalçn et al. (2005) that, at standard rearing temperatures, chicks from either younger or older parent stocks that had survived exposure to higher incubation temperatures had lower BW.
The incidence of TD at 49 d of age was correlated with incubation at an altered temperature during the early stages of embryo development, which suggests the existence of a critical stage for growth plate development and differentiation (Table 3). Altering the incubation temperature at a late stage, but not at an early stage, of embryo development affected tibia weight (Table 3), suggesting that growth plate differentiation and tibia growth do not share the same critical stage. It is interesting to note that although TD is characterized by a decrease in growth plate calcification (Leach and Lilburn, 1992), TD incidence was correlated with increased tibia ash at hatch but not with tibia calcium in this study (Table 3). At hatch, increased tibia calcium was observed in all treatments, but at d 49 of age no differences were observed between the control and treated chicks.
In the growth plate, the rate of division of the stem cells that give rise to chondrocytes, the proliferation rate of the chondrocytes, the size of the PZ, and the degree of cellular hypertrophy are precisely controlled, as manifested in the near symmetry of the limbs and the hereditary element of adult stature. Any deviation from the normal pattern of chondrocyte proliferation, chondrocyte differentiation, or both may lead to bone abnormalities (Farquharson et al., 1995; Di Nino et al., 2001). Tibial dyschondroplasia is defined as the result of incomplete growth plate chondrocyte differentiation, as evaluated according to various differentiation markers (Pines et al., 2005). In TD lesions, abnormal collagen type II gene expression at 8 d posthatching was previously reported (Pines et al., 1999). In addition to its expression in the AC and PZ of the growth plate, collagen type II was expressed by cells in the lower part of the growth plate surrounding the TD lesion before any external signs of TD were observed. At this stage, cells expressing the collagen type II gene, which is characteristic of the proliferative chon-drocytes, were also found within the HZ. These results suggest that the primary events leading to TD occur because of altered spatial and temporal control of cell division, which may be due to abnormal growth factor(s) expression, and which suggests an important role for collagen type II in the differentiation process leading to TD. Altering the incubation temperature in the early stages of embryo bone formation, but not in the later stages, caused increases in the number of growth plate chondrocytes expressing the collagen type II gene in each column, suggesting an increase in cell proliferation and a delay in cell differentiation (Figure 1). In parallel, a decrease in AP activity was observed only in growth plates of chicks incubated at temperatures other than that of the controls during the early stages of bone formation, which supports the notion that temperature manipulation in the early stages of bone formation causes delayed cell differentiation (Figure 2).
Another gene expressed in the HZ and marking the onset of differentiation is OPN. The suggestion that OPN is involved in growth plate cartilage differentiation and calcification was based on its tissue distribution, its affinity for calcium (Oldberg et al., 1986), its immunolocalization to electron-dense regions of mineralization (Ikeda et al., 1992), and the regulation of its gene expression by calcitrophic hormones such as 1,25-dihydroxy vitamin D3 (Prince and Butler 1987; Noda et al., 1990) and parathyroid hormone (Noda and Rodan, 1989). The association of OPN with mineralized regions of the extracellular matrices of bone and cartilage, and its accumulation at tissue surfaces and interfaces are consistent with the hypothesis that OPN plays a role in the extracellular mineralization process (McKee et al., 1992). Thus, it was of interest that an increase was found in the number of cells expressing the OPN gene, and so causing a wider HZ (Figure 3), together with increased collagen type II expression and decreased AP activity (Figures 1 and 2) in chicks incubated at a temperature other than the control during the early stages of bone formation. The mammalian and the avian OPN are highly phosphorylated (Prince et al., 1987; Gotoh et al., 1990). Previously, we demonstrated that OPN gene expression and phosphorylation in avian growth plate chondrocytes are regulated by separate mechanisms involving local growth factors, and that the responses to the various controlling agents varied with the state of differentiation (Barak-Shalom et al., 1995). Thus, one explanation for this disparity might be that the OPN state of phophorylation, which is of utmost importance to its physiological role, is involved in the increase in TD incidence observed in these chicks (Table 3). This would be consistent with the suggestion that that the primary events of the TD lesion occur in cells of proliferative phenotype within the HZ (Pines et al., 1999). It should be noted that even though a correlation was found between temperature-dependent changes in the differentiation markers and TD, they cannot be used alone as tools for TD prediction because not all chicks exhibiting these changes develop TD.
A large body of work spanning the past decade has identified the molecular chaperone Hsp90 as a critical modulator of an extensive network of cellular signaling pathways, including cell cycle control, gene transcription, and apoptotic signaling (Cullinan and Whitesell, 2006). Once chondrocytes began to synthesize Hsp90 in response to a temperature change, they continued to do so long after the temperature returned to the control levels (Figures 4 and 5). These results are consistent with the ability of chickens to acquire thermotolerance (Yahav, 2000). The increase in incubation temperature had a stronger effect on Hsp90 synthesis than its decrease and persisted for a longer period of time. This occurred when the alteration in incubation temperature was applied during the early stages of embryo development, which again indicates the critical importance of this period. Of major interest is the observation that after exposure to an increased incubation temperature, high levels of Hsp90 were exhibited not only by the articular chondrocytes and chondrocytes of the HZ, but also by some of the proliferative chondrocytes arranged in columns. All the cells in each column derive from a single cell of the reserve zone; therefore, the observation that only some, but not all, of the columns exhibited Hsp90 suggests that the proliferative chondrocytes probably are not a uniform population. This has major implications, because TD is always initiated in a discrete location of the growth plate, which suggests the involvement of a specific subset of chondrocytes of the reserve zone. It will be of great interest to determine whether a correlation exists between Hsp90 and the incidence of TD induced by other means, including administration of various dithiocarbamates (Ben-Bassat et al., 1999; Rath et al., 2004), excessive levels of Cys and homocysteine (Bai and Cook, 1994), and changes in the calcium-phosphorus ratio. If such a correlation should be confirmed, Hsp90 signaling and pathways could be targeted to decrease the incidence of TD. However, at the present stage, the involvement of heat-shock proteins other than Hsp90 cannot be ruled out.
In summary, the early stages of embryo development and bone formation are crucial for growth plate differentiation, and any temperature deviation from the normal will increase the incidence of TD at a later stage. This increase in TD incidence was correlated with delayed chondrocyte differentiation, probably driven by Hsp90, which supports the hypothesis that TD is the result of abnormal chondrocyte differentiation.
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ACKNOWLEDGMENTS |
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Received for publication March 17, 2007. Accepted for publication April 17, 2007.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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