PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION Comparison of Three Lines of Broiler Breeders Differing in Ascites Susceptibility or Growth Rate. 1. Relationship Between Acoustic Resonance Data and Embryonic or Hatching Parameters. K. Tona,* B. Kemps,† V. Bruggeman,* F. Bamelis,† L. De Smit,* O. Onagbesan,*,1 J. De Baerdemaeker,† and E. Decuypere* *Laboratory for Physiology and Immunology of Domestic Animals, and †Department of Agricultural Engineering, Kasteelpark Arenberg 30, Katholieke Universiteit Leuven, Heverlee, Belgium ABSTRACT Ascites is a prevalent cardiovascular dis- albumen pH, Haugh units (HU) at setting, and embryo ease among modern broilers with negative impacts on weights at d 11 and 18, at internal pipping (IP), and at production and animal welfare. The peak of mortality hatch. The durations of IP, external pipping (EP), and due to ascites occurs at the end of the growing period, but hatching were also determined. At 2 hourly periods dur- the etiology of this problem may start during embryonic ing incubation, egg RF and damping were also measured. development. A few recent reports have demonstrated There were differences in egg weights between DAR and that the signs of ascites susceptibility are manifested dur- SASL vs. DAS, but albumen HU, albumen pH, and the ing the late stages of incubation. In the current study, ratio of yolk weight to egg weight were similar. There we used a nondestructive method based on egg acoustic were differences in RF, damping, embryonic growth rates, resonance parameters [resonant frequency (RF) and and hatching events. Changes in resonant frequency and damping] to establish a relationship between embryo damping, which certainly suggest eggshell differences physiological events during early development in broiler among lines, were not totally related to variations in phys- eggs and susceptibility to ascites. The hatching eggs of 3 iological events during early and late embryonic develop- broiler lines differing in ascites susceptibility were used ment. A comparison between DAR and DAS, between for this study: ascites-resistant dam line (DAR), ascites- DAS and SASL, or DAR and SASL indicates that sensitiv- sensitive dam line (DAS), and ascites-sensitive sire line ity to ascites and selection for rapid growth rate in ascites- (SASL). These lines were selected on the basis of fast sensitive lines have different effects on embryonic param- growth, high breast meat yield, and ascites induction at eters. We concluded that the sensitivity of broiler breeders low temperatures such that the order of ascites suscepti- to ascites does not inﬂuence egg internal quality, but the bility in terms of mortality was SASL >> DAS > DAR. occurrence of ascites sensitivity in broilers could not be Eggs were incubated under standard conditions in forced- reliably predicted by early in ovo acoustic resonance pa- draft incubators. We measured egg weights at setting, rameters and hatching events. (Key words: broiler, hatching egg, resonance parameter, incubation parameter, ascites susceptibility) 2005 Poultry Science 84:1439–1445 INTRODUCTION of which ascites and sudden death syndrome are the most prevalent cardiovascular diseases among modern broiler Intensive and focused selection over many years has ﬂocks (Olkowski and Classen, 1998; Korte et al., 1999) signiﬁcantly improved broiler growth rate. Long-term se- with negative impacts on production and animal welfare. lection for production traits has also led to an increase in In a review, Balog (2003) reported that ascites syndrome the ratio of demand organs, such as skeletal muscles and results from physiological (e.g., vascular damage, fat mass, to supply organs, such as heart, lungs, spleen, blockage of the lymphatic system, decreased plasma on- and liver (Ricklefs, 1985; Nestor et al., 1995; Gavin and cotic pressure, and increase in vascular hydraulic pres- McDevitt, 1999). This selection leads to a number of meta- sure), environmental (e.g., altitude, ventilation or air qual- bolic problems such as disturbances in energy metabolism ity, and cold stress) parameters or nutritional factors. Ac- 2005 Poultry Science Association, Inc. Received for publication January 11, 2005. Abbreviation Key: DAR = ascites-resistant dam line; DAS = ascites- Accepted for publication May 5, 2005. sensitive dam line; ED11 = embryonic day 11; ED18 = embryonic day 1 To whom correspondence should be addressed: okanlawon. 18; EP = external pipping; IP = internal pipping; RF = resonant frequency; email@example.com. SASL = ascites-sensitive sire line. 1439 1440 TONA ET AL. cording to Decuypere and Verstegen (1999), almost 50% were stored for 5 d at 15°C and 70% relative humidity of normal, noninfectious mortality among broiler chicks before incubation. Before the beginning of incubation, all is due to ascites. Although the peak of mortality due to the eggs were numbered and weighed individually. Also, ascites occurs at the end of the growing period (Mogha- samples of eggs were used to determine resonant fre- dam et al., 2001), it is reported that the etiology of these quency and to measure albumen Haugh units (HU) and problems may start during embryonic development pH. In this study, each incubation setting consisted of 2 (Coleman and Coleman, 1991; Dewil et al., 1996). How- replications of 150 eggs per line. Eggs were set for incuba- ever, most of these reports concern the late stage of incu- tion in a forced-draft incubator3 at speciﬁc dry bulb tem- bation and are based on destructive methods. To our perature of 37.6°C and wet bulb temperature of 29°C. At knowledge, there is no information about the relationship embryonic stages of 11 d (ED11), 18 d (ED18), or internal between embryonic parameters during early stages of pipping (IP), a sample of 15 eggs per line and per incuba- incubation and ascites sensitivity etiological parameters. tion setting was opened to measure embryo weights. Coucke et al. (1997) and Coucke (1999) reported a relation- ship between acoustic resonance parameters [e.g., reso- Albumen Characteristics nant frequency (RF) and damping] and embryo physio- logical events during early development in chicken eggs. Before setting for incubation, samples of 30 eggs were Kemps et al. (2003) also pointed out a positive correlation weighed and broken to measure yolk weight, albumen, between the timing of decrease of RF during early stage HU, and pH of the albumen. For each broken egg, the of incubation and total incubation duration. Chineme et Egg Quality Measurement System4 was used to record al. (1995) reported a relationship between eggshell con- the egg weight and the height of thick albumen. After ductance during incubation and the occurrence of ascites calibration of the albumen height gauge, height of the in later life. Because sensitivity to ascites results in longer albumen was measured (±0.25 mm) with a vertically incubation (Dewil et al., 1996), acoustic resonance analysis mounted micrometer2 with an electronic path. Between at an early stage of incubation may be a tool to detect eggs, the micrometer was cleaned with wet and then dry posthatch sensitivity to ascites. Differential embryonic absorbing paper. The standard software program version development, as hypothesized to occur between lines dif- 2A2 calculates the albumen HU with the egg weight and fering in ascites susceptibility, may lead to differential albumen height. After HU measurement of each egg, the changes in early acoustic resonance parameters. There- yolk and albumen were separated for, respectively, fore, the aim of this study was to investigate the relation- weighing or pH measurement as quickly as possible. For ships between acoustic resonance parameters during pH measurement, the probe was cleaned with distilled early stages of incubation, embryonic growth, and hatch- water between eggs. ing parameters of 3 lines differing in susceptibility to ascites syndrome. The lines were ascites-resistant dam Acoustic Resonance Analysis line (DAR), ascites-sensitive dam line (DAS), and ascites- sensitive sire line (SASL). These lines were selected for For each incubation setting, a sample of 40 eggs per line fast growth on the basis of breast meat yield, and their was randomly selected for the determination of acoustic susceptibility to ascites was based on mortality due to properties. Because acoustic resonance parameters are ascites induction at low temperatures. The DAS and the linked to egg weights (Coucke et al., 1997), egg weights SASL have higher breast meat yield than the DAR line. were recorded to correct for their inﬂuence on RF and Under normal rearing conditions, mortality due to ascites damping. The measurements were done ﬁrst at 4 h after was not more than 1%, but at low temperatures or at high the beginning of incubation (data not shown) and were altitude mortality due to ascites among lines was DAR < repeated every 2 h between 68 and 122 h of incubation. DAS << SASL. Acoustic resonance analysis was performed using the technique described by Coucke et al. (1997), involving MATERIAL AND METHODS mechanical excitation of the egg by a mechanical im- pactor. The impactor hit the egg at its equator, and noise Experimental Design of the vibrating egg was recorded by a microphone, situ- ated at the equator at 90° to the impactor. The recorded We used 2 incubation settings each with 900 eggs pro- signal was sent to a data acquisition card and transformed vided by Hybro2 in our study. Eggs were produced by 3 by fast Fourier transformation to obtain the resonant fre- lines differing in ascites sensitivity or growth rate: DAR, quency for the ﬁrst spherical mode of the vibrating egg. DAS, and SASL. The DAR and DAS are slow feathering Four instantaneous excitations, with a phase shift of 90°, with relatively low 6-wk broiler body weight, whereas were applied at the equator zone as previously described SASL is fast feathering with high body weight. The eggs Coucke (1999). Hatching and Pipping Events 2 Hybro BV, Boxmeer, The Netherlands. 3 PasReform, Zeddam, The Netherlands. Between 472 and 510 h of incubation, transferred eggs 4 Futura, Lohne, Germany. were checked individually every 2 h for IP, EP, and hatch- EARLY SIGNS FOR ASCITES SUSCEPTIBILITY DURING INCUBATION 1441 1 TABLE 1. Egg weights and egg internal quality according to line Line Egg quality characteristic DAR DAS SASL Egg weights (g) 64.93 ± 0.38a 62.38 ± 0.31b 65.36 ± 0.36a Albumen HU 69.40 ± 2.07 68.34 ± 2.32 66.94 ± 1.36 Albumen pH 9.49 ± 0.02 9.49 ± 0.03 9.54 ± 0.01 Yolk weight (g) 20.80 ± 0.68 20.57 ± 0.72 20.60 ± 0.45 Ratio: yolk weight/egg weight (%) 30.79 ± 0.85 32.30 ± 0.73 31.14 ± 0.50 Data not sharing a common letter are different (P < 0.05). a,b 1 HU = Haugh unit; DAR = ascites-resistant dam line; DAS = ascites-susceptible dam line; SASL = ascites- susceptible sire line. ing event occurrences. At IP, EP, or hatching stage, incu- in Table 2. At ED11, embryos of the SASL had lower body bation duration was deﬁned as the time between setting weight (P < 0.05) and lower body weight/egg weight and the occurrences of these events for an egg. Then ratio (P < 0.05) than those of DAS. At this incubation the times of occurrence of hatching events were used stage, embryo weights and embryo body weight/egg to calculate their durations as: IP duration = duration weight ratios of DAR were comparable with those of between occurrences IP and EP, EP duration = duration embryos from SASL and DAS. At ED18, embryo weights between EP and hatching, and hatching duration = dura- and embryo weight/egg weight ratios were similar tion between IP and hatching. The spreads of IP, EP, or among lines but at IP, embryos from SASL were heavier (P hatch were deﬁned as the dispersion around the average < 0.01) than those from DAS and DAR, although embryo incubation duration. weight/egg weight ratios were similar among the 3 lines. At hatch, chick weights were signiﬁcantly heavier but Statistical Analysis similar for DAR and SASL compared with DAS. The data were processed with the statistical software Effects of Lines on Resonant package SAS version 8.2.5 Because the conditions for incu- Frequency and Damping bation settings were kept constant for each repeated ex- periment, data were pooled for analysis. The GLM proce- Mean weights of eggs used for measurement of RF and dure was used to analyze the effects of lines on egg and damping were 64.78 ± 0.58 g, 64.17 ± 0.39 g, and 64.60 ± embryo weights, albumen pH, albumen HU, yolk weight, 0.49 g for DAR, DAS, and SASL respectively. Figure 1 resonant frequency, spectra data, and durations of IP, shows RF variations, from 68 to 122 h of incubation, EP, and hatching. In a second analysis, the Kolmogorov- among lines in relation to incubation duration. From 4 h Smirnov test was used to assess the normality of the of incubation until 68 h, the RF of all egg lines remained distribution of pipping and hatching events. From the consistently unaltered (data not shown). A similar trend hatching events distribution, incubation duration of me- was maintained until 98 h but the RF in the DAS line dian and 5, 25, 75, and 95% quartiles were calculated. was signiﬁcantly lower (P < 0.01) than those of DAR A 2-tailed test for comparison of variances was used to and SASL lines, which were similar. There was a sharp analyze the effect of line on spread of pipping or hatch- decrease in RF in all lines from 98 to 106 h of incubation. ing events. Although the heights of decrease of RF were similar be- tween lines, the start of the decrease during the incubation RESULTS period was later (P < 0.05) for eggs from SASL (106 h) compared with those for eggs from DAS (99 h) and DAR Effects of Lines on Albumen (100 h), which were similar. Characteristics and Embryo Growth Figure 2 shows variations of damping according to the lines in relation to incubation duration. During incuba- Table 1 shows the values of albumen HU and pH, tion, damping increased at about 92 h for DAR and DAS yolk weight, and egg weights at setting according to line. but around 100 h for SASL and reached a maximum level Albumen HU and pH, yolk weights and ratio of yolk around 110 h for all the lines. Damping, from 68 h to 122 weights to egg weights were similar between lines. How- h of incubation of eggs, of SASL eggs was lower than ever, eggs of DAS were lighter (P < 0.05) than those of that of eggs from DAS. Also, the timing of the increase DAR and SASL. in damping during incubation was similar to the time at Embryo body weights and embryo weight/egg weight which RF decreased. ratios according to lines and incubation stages are shown Effects of Line on Hatching Events Figure 3 shows the spread of hatching in relation to 5 SAS User’s Guide, version 8.2, SAS Institute Inc., Cary, NC. incubation duration and according to line. At 472 h of 1442 TONA ET AL. TABLE 2. Embryo body weight and relative body weight relative to initial egg weight according to incubation stage and weights of 1-d-old chicks of the 3 lines1 Incubation stage Line Body weight (g) Relative body weight (%) ED11 DAR 3.961 ± 0.128 ab 6.072 ± 0.205ab DAS 4.152 ± 0.077a 6.663 ± 0.166a SASL 3.629 ± 0.122b 5.453 ± 0.198b ED18 DAR 28.220 ± 0.675a 44.075 ± 1.761a DAS 27.485 ± 0.762a 44.130 ± 0.795a SASL 27.829 ± 0.623a 41.974 ± 1.181a IP DAR 46.628 ± 0.574b 72.466 ± 0.402a DAS 44.003 ± 0.749b 72.715 ± 0.500a SASL 49.755 ± 0.957a 73.149 ± 0.658a Hatch DAR 47.46 ± 0.37a 73.69 ± 0.22a DAS 45.41 ± 0.30b 72.57 ± 0.28b SASL 48.33 ± 0.36a 74.00 ± 0.22a Data not sharing a common letter are different (P < 0.05). a,b 1 ED11 = embryonic d 11; ED18 = embryonic d 18; IP = internal pipping; DAR = ascites-resistant dam line; DAS = ascites-susceptible dam line; SASL = ascites-susceptible sire line. incubation, 27.20, 22.73, and 19.46% of eggs were at IP for DAR, DAS, and SASL, respectively. At the same time, 9.02, 5.43, and 5.79% of eggs were at EP for DAR, DAS, and SASL, respectively. Durations of IP, EP, and hatching were longer in eggs of SASL (P < 0.05) compared with those of DAR and DAS, which were similar (Table 3). The duration of IP or EP of eggs of SASL was almost 2 h longer than those from DAR and DAS. On average, 50% of IP occurred 2 h earlier in eggs from DAR compared with those from DAS and SASL (P < 0.05). The peak of EP (50% of EP) occurred almost 4 h earlier in the eggs from DAR compared with those from SASL and DAS for which the peak of EP occurred at the same time (P < 0.05). Although 50% of the hatch in DAR was obtained 2 h earlier than those of FIGURE 2. Relationship between damping and incubation duration according to line. DAR = ascites-resistant dam line; DAS = ascites- susceptible dam line; SASL = ascites-susceptible sire line. FIGURE 1. Relationship between resonance frequency and incuba- FIGURE 3. Number of chicks hatched according to incubation dura- tion duration according to line. DAR = ascites-resistant dam line; DAS = tion and line. DAR = ascites-resistant dam line; DAS = ascites-susceptible ascites-susceptible dam line; SASL = ascites-susceptible sire line. dam line; SASL = ascites-susceptible sire line. EARLY SIGNS FOR ASCITES SUSCEPTIBILITY DURING INCUBATION 1443 TABLE 3. Effects of line on internal pipping, external pipping, and hatching duration Duration of hatching events (h) Line IP EP Hatching DAR 9.67 ± 0.52b 11.43 ± 0.46b 20.36 ± 0.36b DAS 10.14 ± 0.51b 11.35 ± 0.47b 20.42 ± 0.46b SASL 12.02 ± 0.60a 13.17 ± 0.79a 23.74 ± 0.76a Within a column, data not sharing a common letter are different (P < 0.05). a,b 1 DAR = ascites-resistant dam line; DAS = ascites-susceptible dam line; SASL = ascites-susceptible sire line; IP = internal pipping; EP = external pipping. DAS, incubation duration was not signiﬁcantly different than ascites sensitivity. Similarly, there was no difference between these 2 lines. Eggs from SASL had signiﬁcantly between the DAR and SASL in RF or body weights, even longer incubations and hatched 4 or 6 h later than those though the SASL is supposed to be fast growing and of DAS or DAR, respectively (P < 0.01). Overall, eggs extremely ascites susceptible. The changes in body from DAR hatched earlier than those of the ascites-sensi- weights at ED18 or at IP could not be related to the RF tive lines. Also, the spread of IP and EP were different data, even though SASL had a better rate of growth to among lines (P < 0.05) and were in the following order: IP than DAR or DAS. The only period when RF had any DAR = DAS < SASL. Hatching spread differed between correlation with body weight was at hatch, when DAS lines (P < 0.05). had the lowest RF and body weight. Again, there was no difference between DAR and SASL. This lack of consis- DISCUSSION tency between RF and embryo body weights among lines suggests that the values of RF may not be a useful pre- In this study, we attempted to characterize the parame- dictor for ascites susceptibility. A common factor in the ters that might be associated with ascites susceptibility dam line was the similarity of timing of the general de- during embryonic development. In doing so, we looked crease in RF after the 90th hour of incubation, whereas for associations between egg RF, damping, embryo body this decline was delayed for some 6 h in the SASL geno- weights at different ages, and hatching parameters to type. The decrease of RF around 100 h of incubation has relate these with ascites susceptibility of the DAR, DAS, been shown to occur as a result of subembryonic ﬂuid and SASL genotypes. The results showed that selection of formation by Bamelis et al.(2002), and it was suggested broiler breeders for ascites susceptibility may not directly to be an indication of a well-deﬁned physiological event at inﬂuence aspects of egg parameters or early embryonic a chronological age, depending on incubation conditions development or hatching events. A comparison between and genetic variation in speed of early development. DAR and DAS, on the one hand, and, on the other hand, The damping results had lower values for SASL com- between DAS and SASL or DAR and SASL indicated that pared with the dam lines during early incubation and a sensitivity to ascites and selection for rapid growth rate late increase that mimicked the late decrease observed in ascites sensitive lines might have different effects on for RF in Figure 1. In the absence of an ascites-resistant embryonic parameters. The differences identiﬁed among sire line genotype in this study, it is difﬁcult to conclude lines seemed mainly to be due to genotypic differences that this ﬁnding could be an early indication of ascites that are unrelated to ascites sensitivity. susceptibility. However, the clear divergence in damping Among genotypes, the albumen HU, albumen pH, and after 90 h among lines indicates signiﬁcant differences ratio of yolk weight to egg weight were not different for between the SASL and DAS genotypes and the DAR geno- the 3 lines studied. Therefore, the differences observed type. These damping data from 100 h clearly suggest a in RF, embryonic growth, and hatching events could not link to ED11 body weights. This trend of body weights be explained by egg size or albumen quality parameters. was reversed at hatch. Although damping measures have Overall, the differences in egg weights between lines, not been associated with any embryo physiological pro- although yolk weights were similar, might have been due cesses, it certainly suggests eggshell differences between to differences in albumen or shell weight. lines. Chineme et al. (1995) and Odom et al. (1995) pre- Coucke et al. (1997) showed that changes in RF and viously showed that eggshell conductance may inﬂuence damping could be related to variations in physiological ascites susceptibility, and, therefore, differences in egg- events during early embryonic development. Early occur- shell characteristics among lines as revealed by RF and rence of the decrease in RF in DAS and DAR vs. SASL damping may be relevant in this respect. However, these should have indicated a more rapid early development authors did not study the implications of the measured in the embryo weights of the DAR and DAS at ED11, but parameters on embryonic development. At IP and hatch, this was not the case. Surprisingly, the ascites-susceptible embryo and chick weights were negatively correlated genotypes were different in RF and body weights, which with the early acoustic data in the DAR vs. SASL and suggests a major difference between the sire and dam between DAS and SASL. Accelerated embryonic growth lines that may be ascribed to genotype differences rather rate in the second half of incubation of the SASL genotype 1444 TONA ET AL. compared with the DAR indicated an early sign of high between DAS and DAR and between DAS and SASL growth rate potential. On the other hand, the DAS geno- or DAR and SASL suggests that, on top of an inherent type had a lower growth rate in the last incubation period sensitivity to ascites, it is selection for rapid posthatch compared with DAR. This ﬁnding suggests that predispo- growth that increases broiler sensitivity to ascites, as is sition to ascites is not necessarily linked to embryonic the case for SASL. growth speed or to growth rate at all but can be related It is concluded that the sensitivity of broiler breeders to completely other physiological functioning as sug- to ascites do not inﬂuence egg internal quality as mea- gested by Scheele et al. (2003a,b). sured by the pH and HU. The inconsistency in the rela- At median (50%) occurrence of IP, EP, or hatch, al- tionship between the values of RF or the timing of its though the eggs from DAS hatched 2 h later than those decrease and embryo development did not permit a reli- from DAR, there was no signiﬁcant difference between able association of egg acoustic data with ascites suscepti- these lines. This ﬁnding agrees with the timing of the bility. Although the timing of the decrease in RF or in- RF decrease and damping increase between the 2 lines. crease in damping could be partly associated with incuba- Timing of the decrease in RF has also been used as an early tion duration in the SASL, it could not be speciﬁcally indication for predicting incubation duration. Kemps et associated with ascites susceptibility. Therefore differ- al. (2003) previously reported a positive correlation be- ences observed in acoustics, body weights, or hatching tween the timing of RF decrease during early incubation parameters among lines might be partly due to genotype and hatching time. The lack of difference in durations of differences that are secondary (associated responses) to hatching events between the DAR and DAS suggests that the primary selection goal, which was fast growth with although DAS is ascites sensitive, it can cope better with high breast meat yield. relatively mild hypoxia during the last stage of incubation than SASL. ACKNOWLEDGMENTS As for the comparison between DAR and SASL, the results of this study are in the line with those of Dewil et This study was supported by FWO, Belgium (grant al. (1996), who reported a similar delay of approximately 5 number G.0286.04). K. Tona received a postdoctoral h in hatching of eggs from SASL compared with those award (KU Leuven) and V. Bruggeman had a postdoc- of DAR. Although 50% of the eggs of all 3 lines were at toral funding from Funds for Scientiﬁc Research (FWO, IP at almost the same incubation duration, eggs of DAR Flanders, Belgium). The authors are grateful to G. A. hatched 6 h earlier than those from SASL due to longer Albers of Hybro BV for the supply of experimental durations of IP, EP, and hatching time. This delay is hy- animals. pothesized to be linked with the delay in early RF de- crease and damping increase in the SASL eggs and, per- REFERENCES haps, also with early lower damping. 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