SUMMARY

Bone development can be adversely affected by stressful environmental conditions early in life. One experiment was conducted to evaluate the effects of low temperature during early incubation, high temperature during late incubation, and transportation conditions from hatchery to the farm on the long bone development and leg health of broilers. Bone development was evaluated at hatch before transportation. Gait scores and leg health disorders were recorded at 41 d of age. Although incubation conditions did not affect chick BW, hot temperatures during late incubation reduced the relative weight of femurs and shanks. At 41 d, males had more leg problems than females. Late high temperature and transportation stress increased the incidence of crooked toes and the percentage of chickens with a gait score of 2. Transportation stress, including elevated temperature, caused a greater incidence of twisted legs. We concluded that low early incubation temperature, high late incubation temperature, and transportation stress can increase the incidence of leg problems in commercial broilers.

Primary Audience: Hatchery Managers, Broiler Managers, Veterinarians, Researchers

DESCRIPTION OF PROBLEM

Bone development can be affected by stressful environmental conditions early in life [1, 2], especially by less than optimal incubation temperatures and oxygen concentrations [3, 4]. Prehatch stress impairs embryonic development and increases fluctuating asymmetry in chickens [3–5]. Fluctuating asymmetry between limbs and other bilateral phenotypic traits reflects the ability of individuals to cope with stressful conditions during ontogeny [6]. The relative asymmetry (RA) of long bones has been correlated with tibial dyschondroplasia, poorer gait scores, and increased tonic immobility in chickens [6].

Several factors that control endochondral ossification of long bones can be affected by incubation temperatures, mainly during the plateau stage of embryonic development. Incubation temperature has an important impact on the hormonal axis that controls bone development, which includes thyroid hormones, insulin-like growth factor 1, and growth hormone [7–9].

Increased incubator temperatures resulting in elevated embryonic temperatures and low oxygen concentrations can affect bone development by altering bone weight and length, changing chondrocyte cell density in the tibia proximal epiphyses, and altering the expression of important proteins for ossification, such as collagen type X and transforming growth factor β [3, 4]. Hatcher temperatures greater than 37°C and oxygen concentrations less than 21% should be avoided to ensure optimal bone development at hatching.

Very little is known about the effects of suboptimal conditions hours after hatch in either the chick holding room or during transportation. In early reports, newly hatched chicks were unresponsive to stress [10]. However, current commercial experiences [11–13] indicate that it is important to avoid high temperatures and maintain proper ventilation during transportation of chicks to reduce first-week mortality and obtain better performance. The optimal conditions for transportation of chicks remains unknown. In addition, very little is known about the effects of transportation on broiler health. The objective of this study was to evaluate the effects of embryonic incubation temperatures and posthatch transportation stress on long bone development at hatch and on the leg health of broilers at 41 d of age.

MATERIALS AND METHODS

This study was conducted under the Animal Care and Use guidelines established by the North Carolina State University and Virginia Polytechnic Institute and State University Animal Care and Use Committees. A total of 5,200 broiler hatching eggs from a Cobb 500 breeder flock [14] of 51 wk of age were incubated in Natureform machines [15] to achieve a low (L) eggshell temperature of 36.7°C or a standard (S) eggshell temperature of 37.5°C during the first week of incubation. During the third week of incubation, the eggs were incubated to achieve the S eggshell temperature (37°C) or a high (H) eggshell temperature of 39°C. All eggs were incubated at S (37°C) from d 8 to 17, with combinations of the other temperatures occurring on d 1 to 7 and d 18 to 21 to generate 4 incubation treatments: LS, LH, SS, and SH.

At hatch, a subsample of 15 chickens per treatment was removed to obtain BW and residual yolk weights. Postmortem, both legs were dissected and the femur, tibia, and shank weights, lengths, and thicknesses were recorded. The RA of each leg section was calculated [6]. After hatch, chicks were equally separated into 2 transportation groups: a control group (T1) and a stressed group (T2). The transportation stress consisted of a reduced ventilation rate, which resulted in an elevated temperature (40°C) compared with the control temperature (34°C), and most likely reduced oxygen concentrations (not measured). Chickens were exposed to the transportation conditions for 4 h.

After transportation, 46 chicks (23 male and 23 female) per treatment were assigned to 4 × 8 ft floor pens (0.7 ft2/chick) with clean pine shavings, nipple drinkers, and hanging feeders. The commercial lighting program and ventilation were monitored continuously from the day of hatch to d 42. Each treatment was replicated with 7 pens for the 42-d trial. All birds were provided with feed and water ad libitum throughout the grow-out period. At 41 d of age, the legs of each broiler were inspected for crooked toes, valgus and varus deformities of the intertarsal joint, hock burns, footpad dermatitis, and gait scores. Walking ability was divided into 6 categories of gait scores, ranging from completely normal (score 0) to immobile (score 5) according to the Kestin method of gait scoring [16].

Percentages of incidence per pen were calculated. All percentage data were transformed to arcsine square root n + 1. Bone data at hatch were analyzed as a 2 × 2 factorial design with early incubation (L vs. S) and late incubation (S vs. H) as main effects. The incidence of leg problems and the gait scores at 41 d of age were analyzed as a 2 × 2 × 2 factorial design that included transportation conditions (T1 vs. T2) as an additional main effect (Table 1). All data were analyzed using the GLM procedures of SAS [17]. Treatment means were separated using the LSM procedure of SAS [17], with a level of significance of P ≤ 0.05 unless otherwise stated.

Treatments assigned to fertile eggs during early and late incubation1 and to hatching chicks during transportation from the hatchery to the farm

Table 1
Treatments assigned to fertile eggs during early and late incubation1 and to hatching chicks during transportation from the hatchery to the farm
Treatment  Early incubation Late incubation Chick transport 
LST1  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
LST2  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
LHT1  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
LHT2  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
SST1  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
SST2  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
SHT1  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
SHT2  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
Treatment  Early incubation Late incubation Chick transport 
LST1  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
LST2  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
LHT1  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
LHT2  Low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
SST1  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
SST2  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation Standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 
SHT1  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Control (T1) transport, with a ventilation temperature of 34°C 
SHT2  Standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation High (H) eggshell temperature of 39°C from d 18 to 21 of incubation Stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C 

1All eggs were incubated at a standard temperature (37°C) from d 8 to 17.

RESULTS AND DISCUSSION

Bone Development at Hatch and Grow Out

There were no differences in BW in a subsample of 15 birds per interaction cell taken for bone development analyses (Table 2). The incubation temperature had significant effects (P < 0.05) on yolk utilization, and the residual yolk (P < 0.01) was higher in chicks incubated under an L early temperature (8.6 ± 0.3%) compared with those incubated under S conditions (7.7 ± 0.3%). Bone weights relative (%) to BW without yolk were affected mainly by late incubation temperatures. The H temperature during late incubation reduced (P < 0.05) the relative weights (%) of femurs and shanks (Table 2). Relative weights of tibias were reduced (P < 0.01) by the combination of L early and H late temperatures. The RA of tibia and shank weights was increased (P < 0.01) by early L temperatures. The shanks of chicks from the H late incubation temperature group were longer (23 ± 0.1 mm) compared with the shanks of those from the S temperature (22.6 ± 0.1 mm) group (P < 0.01; data not shown). Similar effects of late incubation temperatures have been observed in previous experiments [3, 4] in our laboratory with other genetic lines of chickens and turkeys. It is interesting to note the effects of temperature on bone development during the first 7 d of incubation. Embryonic bone development can be affected by changes in temperature at any stage of development [1, 2], but little research has been done on the very early stages of limb development occurring between 2 and 3 d of age [18].

Effect of early and late incubation temperatures on BW (g), residual yolk (%), relative weights1 (%), and relative asymmetry2 (RA) of bones at day of hatch

Table 2
Effect of early and late incubation temperatures on BW (g), residual yolk (%), relative weights1 (%), and relative asymmetry2 (RA) of bones at day of hatch
Item BW of 0-d sample (g) Residual yolk (%) Femur  Tibia  Shank 
RA RA RA 
Treatment3           
 LH 49.8 9.01 0.94 6.12  1.66b 8.22  5.87 4.30 
 LS 48.4 8.23 0.99 6.56  1.78a 9.26  6.09 3.32 
 Mean 49.1 8.62a 0.97 6.34  1.72 8.74a  5.98 3.81a 
 SH 48.9 7.92 0.98 6.72  1.77ab 5.94  5.81 2.12 
 SS 48.0 7.56 0.99 5.85  1.76ab 4.59  5.94 1.67 
 Mean 48.5 7.74b 0.98 6.28  1.76 5.26b  5.87 1.89b 
Late incubation treatment mean4           
 High temperature 49.3 8.46 0.96b 6.42  1.71 7.08  5.84b 3.21 
 Standard temperature 48.2 7.89 0.99a 6.21  1.77 6.93  6.01a 2.50 
 SEM 0.6 0.25 0.16 0.75  0.31 0.93  0.75 0.38 
           
Source of variation ———————————————————P-value——————————————————————— 
 Early incubation 0.489 0.004 0.305 0.959  0.079 0.010  0.659 <0.01 
 Late incubation 0.183 0.189 0.047 0.844  0.066 0.909  0.013 0.192 
 Early incubation × late incubation 0.765 0.531 0.151 0.549  0.002 0.368  0.505 0.624 
Item BW of 0-d sample (g) Residual yolk (%) Femur  Tibia  Shank 
RA RA RA 
Treatment3           
 LH 49.8 9.01 0.94 6.12  1.66b 8.22  5.87 4.30 
 LS 48.4 8.23 0.99 6.56  1.78a 9.26  6.09 3.32 
 Mean 49.1 8.62a 0.97 6.34  1.72 8.74a  5.98 3.81a 
 SH 48.9 7.92 0.98 6.72  1.77ab 5.94  5.81 2.12 
 SS 48.0 7.56 0.99 5.85  1.76ab 4.59  5.94 1.67 
 Mean 48.5 7.74b 0.98 6.28  1.76 5.26b  5.87 1.89b 
Late incubation treatment mean4           
 High temperature 49.3 8.46 0.96b 6.42  1.71 7.08  5.84b 3.21 
 Standard temperature 48.2 7.89 0.99a 6.21  1.77 6.93  6.01a 2.50 
 SEM 0.6 0.25 0.16 0.75  0.31 0.93  0.75 0.38 
           
Source of variation ———————————————————P-value——————————————————————— 
 Early incubation 0.489 0.004 0.305 0.959  0.079 0.010  0.659 <0.01 
 Late incubation 0.183 0.189 0.047 0.844  0.066 0.909  0.013 0.192 
 Early incubation × late incubation 0.765 0.531 0.151 0.549  0.002 0.368  0.505 0.624 

a,bMeans in a column without a common superscript are significantly different (P < 0.05).

1Bone weight relative to BW without yolk at hatch.

2Relative asymmetry of limbs at hatch.

3Treatment: LH = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation and high (H) eggshell temperature of 39°C from d 18 to 21 of incubation; LS = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation and standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation; SH = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation and high (H) eggshell temperature of 39°C from d 18 to 21 of incubation; SS = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation and standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation. All eggs were incubated at a standard temperature (37°C) from d 8 to 17.

4High temperature = high eggshell temperature of 39°C from d 18 to 21 of incubation; standard temperature = standard eggshell temperature of 37°C from d 18 to 21 of incubation.

Leg Health at 41 d of Age

At 41 d of age, males had more (P < 0.001) leg problems, such as crooked toes, hock burns, and valgus deformations, than females (Table 3). The prevalence of footpad dermatitis was low (2.5 ± 1.6%) and was not related (P > 0.05) to sex or any of the factors evaluated. A significant 3-way interaction was observed for crooked toes (Table 3). The prevalence of crooked toes in broilers was higher when embryos during incubation or hatchlings during transportation were exposed to the treatment combinations SHT1, LHT2, SST2, and SHT2 compared with broilers in the treatment combinations LST1, SST1, LST2, and LHT1. This trend led us to the conclusion that late H temperatures and T2 conditions together increased (P < 0.01) the incidence of crooked toes. Late incubation and transportation conditions together affected (P < 0.05) the percentage of broilers that received gait scores of 2 (Table 4). However, only broilers under the late H temperatures with T1 conditions had a higher (P < 0.05) percentage (17.7 ± 2.1%) of gait scores of 2 compared with broilers in the ST1 treatment combination (8.0 ± 2.0%; interaction means not shown in Table 4). Broilers in the HT2 and ST2 treatments, independently of early incubation temperature, had similar percentages of broilers with gait scores of 2 (11.4 ± 2.1% and 10.7 ± 2.2%, respectively) compared with the other groups. Transportation stress (T2) caused a higher (P < 0.05) prevalence of twisted legs at 41 d of age (Table 3) and, consequently, a higher percentage of broilers (P < 0.05) with gait scores of 4 (Table 4). When the total percentage of broilers with gait scores of 3 and 4 was analyzed (Table 4), the treatment combination SHT2 had the highest percentage of broilers with severe locomotion problems, which was more than 2-fold (5.75 ± 0.55%) higher (P < 0.05) than the SST2 combination (2.55 ± 0.55%). The complete etiology of some bone developmental disorders is not completely understood [9, 16, 19–21]. However, there is evidence that these problems can begin very early in life, when broilers have the fastest rate of bone growth.

Leg health parameters of chickens at 41 d of age, exposed to 2 early and late incubation temperatures and 2 chick transportation conditions

Table 3
Leg health parameters of chickens at 41 d of age, exposed to 2 early and late incubation temperatures and 2 chick transportation conditions
Item Crooked toes (%) Footpad dermatitis (%) Hock burns (%) Valgus (%) Twisted legs (%) 
Treatment1      
 LST1 9.0c 3.8 40.0 51.5 0.6 
 LST2 6.1c 0.0 37.7 60.6 2.3 
 Mean 7.5 1.9 38.9 56.0 1.4 
 LHT1 4.2c 2.2 47.5 58.8 0.5 
 LHT2 17.7ab 4.1 57.6 48.7 2.0 
 Mean 10.9 3.1 52.7 53.8 1.2 
 SST1 7.5c 2.1 53.5 59.4 1.6 
 SST2 16.2ab 0.7 48.19 57.8 1.9 
 Mean 11.8 1.4 50.8 58.6 1.8 
 SHT1 20.2a 3.5 60.1 56.4 1.5 
 SHT2 15.3ab 3.5 52.1 56.9 3.1 
 Mean 17.7 3.5 56.1 56.6 2.3 
Early incubation treatment mean      
 Low temperature 9.4 2.5 45.7 54.9 1.3 
 Standard temperature 14.7 2.4 53.4 57.6 2.0 
Effect      
 Late incubation temperature      
  Standard 9.7 1.6 44.8 55.2 1.6 
  High 14.3 3.3 54.3 57.3 1.8 
 Transportation      
  Control 10.4 2.9 50.3 56.5 1.1b 
  Stressed 13.8 2.0 48.9 56.0 2.3a 
 Sex      
  Male 15.8a 2.5 55.1a 67.1a 1.7 
  Female 7.2b 2.4 44.1b 45.4b 1.7 
 SEM 2.1 0.8 4.1 2.4 0.7 
      
Source of variation ——————————————————P-value———————————————— 
 Sex 0.0003 0.9490 0.0536 <0.0001 0.9969 
 Early incubation 0.0427 0.9425 0.2963 0.4023 0.5427 
 Late incubation 0.2514 0.1472 0.1171 0.6082 0.7354 
 Chick transportation 0.8488 0.4641 0.4065 0.9130 0.0366 
 Early incubation × late incubation 0.2123 0.7212 0.7503 0.9877 0.5172 
 Early incubation × transportation 0.8018 0.9243 0.4065 0.9703 0.6556 
 Late incubation × transportation 0.6656 0.1279 0.8446 0.2011 0.9720 
 Early incubation × late incubation × transportation 0.0043 0.3647 0.5702 0.1153 0.9250 
Item Crooked toes (%) Footpad dermatitis (%) Hock burns (%) Valgus (%) Twisted legs (%) 
Treatment1      
 LST1 9.0c 3.8 40.0 51.5 0.6 
 LST2 6.1c 0.0 37.7 60.6 2.3 
 Mean 7.5 1.9 38.9 56.0 1.4 
 LHT1 4.2c 2.2 47.5 58.8 0.5 
 LHT2 17.7ab 4.1 57.6 48.7 2.0 
 Mean 10.9 3.1 52.7 53.8 1.2 
 SST1 7.5c 2.1 53.5 59.4 1.6 
 SST2 16.2ab 0.7 48.19 57.8 1.9 
 Mean 11.8 1.4 50.8 58.6 1.8 
 SHT1 20.2a 3.5 60.1 56.4 1.5 
 SHT2 15.3ab 3.5 52.1 56.9 3.1 
 Mean 17.7 3.5 56.1 56.6 2.3 
Early incubation treatment mean      
 Low temperature 9.4 2.5 45.7 54.9 1.3 
 Standard temperature 14.7 2.4 53.4 57.6 2.0 
Effect      
 Late incubation temperature      
  Standard 9.7 1.6 44.8 55.2 1.6 
  High 14.3 3.3 54.3 57.3 1.8 
 Transportation      
  Control 10.4 2.9 50.3 56.5 1.1b 
  Stressed 13.8 2.0 48.9 56.0 2.3a 
 Sex      
  Male 15.8a 2.5 55.1a 67.1a 1.7 
  Female 7.2b 2.4 44.1b 45.4b 1.7 
 SEM 2.1 0.8 4.1 2.4 0.7 
      
Source of variation ——————————————————P-value———————————————— 
 Sex 0.0003 0.9490 0.0536 <0.0001 0.9969 
 Early incubation 0.0427 0.9425 0.2963 0.4023 0.5427 
 Late incubation 0.2514 0.1472 0.1171 0.6082 0.7354 
 Chick transportation 0.8488 0.4641 0.4065 0.9130 0.0366 
 Early incubation × late incubation 0.2123 0.7212 0.7503 0.9877 0.5172 
 Early incubation × transportation 0.8018 0.9243 0.4065 0.9703 0.6556 
 Late incubation × transportation 0.6656 0.1279 0.8446 0.2011 0.9720 
 Early incubation × late incubation × transportation 0.0043 0.3647 0.5702 0.1153 0.9250 

a–cMeans in a column without a common superscript are significantly different (P < 0.05).

1Treatment: LST1 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; LST2 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C; LHT1 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; LHT2 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C; SST1 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; SST2 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C; SHT1 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; SHT2 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C. All eggs were incubated at a standard temperature (37°C) from d 8 to 17.

Percentage of chickens within each gait score category1 at 41 d of age, exposed to 2 early and late incubation temperatures and 2 chick transportation conditions

Table 4
Percentage of chickens within each gait score category1 at 41 d of age, exposed to 2 early and late incubation temperatures and 2 chick transportation conditions
Item Gait score (%) 
Treatment2      
 LST1 14.44 73.54 10.25 1.77 0.00 
 LST2 8.47 79.87 10.61 1.06 0.00 
 Mean 11.45 76.70 10.43 1.41 0.00 
 LHT1 8.61 71.30 19.08 1.01 0.00 
 LHT2 15.47 71.51 10.94 0.53 1.56 
 Mean 12.04 71.41 15.01 0.77 0.78 
 SST1 6.87 85.87 5.82 1.00 0.43 
 SST2 7.78 78.18 10.92 1.86 0.69 
 Mean 7.33 82.02 8.37 1.43 0.56 
 SHT1 7.49 75.59 16.40 0.53 0.00 
 SHT2 6.33 75.98 11.95 4.17 1.58 
 Mean 6.91 75.78 14.18 2.35 0.79 
Early incubation treatment mean      
 Low temperature 11.75 74.06 12.72 1.09 0.39 
 Standard temperature 7.11 78.90 11.27 1.89 0.68 
Effect      
 Late incubation temperature      
  Standard 9.39 79.36 9.40b 1.42 0.28 
  High 9.47 73.59 14.59a 1.56 0.78 
 Transportation      
  Control 9.35 76.57 12.89 1.08 0.11b 
  Stressed 9.51 76.38 11.10 1.90 0.96a 
 Sex      
  Male 4.59b 76.32 17.28a 0.99 0.69 
  Female 14.28a 73.64 6.71b 1.98 0.38 
 SEM 1.88 2.31 1.49 0.55 0.28 
 N 80 80 80 80 80 
  
Source of variation ——————————————P-value———————————— 
 Sex 0.0001 0.7236 <0.0001 0.1750 0.5390 
 Early incubation 0.1471 0.0930 0.6222 0.5805 0.5371 
 Late incubation 0.8423 0.0877 0.0232 0.7514 0.2288 
 Chick transportation 0.5126 0.7213 0.6033 0.5645 0.0322 
 Early incubation × late incubation 0.9576 0.8682 0.7103 0.4526 0.3035 
 Early incubation × transportation 0.8555 0.1711 0.1521 0.1118 0.9480 
 Late incubation × transportation 0.0772 0.9510 0.0292 0.4669 0.0615 
 Early incubation × late incubation × transportation 0.1396 0.2078 0.8373 0.1750 0.7268 
Item Gait score (%) 
Treatment2      
 LST1 14.44 73.54 10.25 1.77 0.00 
 LST2 8.47 79.87 10.61 1.06 0.00 
 Mean 11.45 76.70 10.43 1.41 0.00 
 LHT1 8.61 71.30 19.08 1.01 0.00 
 LHT2 15.47 71.51 10.94 0.53 1.56 
 Mean 12.04 71.41 15.01 0.77 0.78 
 SST1 6.87 85.87 5.82 1.00 0.43 
 SST2 7.78 78.18 10.92 1.86 0.69 
 Mean 7.33 82.02 8.37 1.43 0.56 
 SHT1 7.49 75.59 16.40 0.53 0.00 
 SHT2 6.33 75.98 11.95 4.17 1.58 
 Mean 6.91 75.78 14.18 2.35 0.79 
Early incubation treatment mean      
 Low temperature 11.75 74.06 12.72 1.09 0.39 
 Standard temperature 7.11 78.90 11.27 1.89 0.68 
Effect      
 Late incubation temperature      
  Standard 9.39 79.36 9.40b 1.42 0.28 
  High 9.47 73.59 14.59a 1.56 0.78 
 Transportation      
  Control 9.35 76.57 12.89 1.08 0.11b 
  Stressed 9.51 76.38 11.10 1.90 0.96a 
 Sex      
  Male 4.59b 76.32 17.28a 0.99 0.69 
  Female 14.28a 73.64 6.71b 1.98 0.38 
 SEM 1.88 2.31 1.49 0.55 0.28 
 N 80 80 80 80 80 
  
Source of variation ——————————————P-value———————————— 
 Sex 0.0001 0.7236 <0.0001 0.1750 0.5390 
 Early incubation 0.1471 0.0930 0.6222 0.5805 0.5371 
 Late incubation 0.8423 0.0877 0.0232 0.7514 0.2288 
 Chick transportation 0.5126 0.7213 0.6033 0.5645 0.0322 
 Early incubation × late incubation 0.9576 0.8682 0.7103 0.4526 0.3035 
 Early incubation × transportation 0.8555 0.1711 0.1521 0.1118 0.9480 
 Late incubation × transportation 0.0772 0.9510 0.0292 0.4669 0.0615 
 Early incubation × late incubation × transportation 0.1396 0.2078 0.8373 0.1750 0.7268 

a,bMeans in a column without a common superscript are significantly different (P < 0.05).

1Kestin gait score [16], ranging from completely normal (score 0) to immobile (score 5).

2Treatment: LST1 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; LST2 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C; LHT1 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; LHT2 = low (L) eggshell temperature of 36.7°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C; SST1 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; SST2 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, standard (S) eggshell temperature of 37°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C; SHT1 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and control (T1) transport, with a ventilation temperature of 34°C; SHT2 = standard (S) eggshell temperature of 37.5°C from d 1 to 7 of incubation, high (H) eggshell temperature of 39°C from d 18 to 21 of incubation, and stressed (T2) transport, with a reduced ventilation rate resulting in an elevated temperature of 40°C. All eggs were incubated at a standard temperature (37°C) from d 8 to 17.

Currently, under commercial poultry production conditions, most incubators are challenged to provide sufficient heating early in incubation for the newly set eggs and to offer enough cooling capacity to reduce overheating of fast-growing embryos later in incubation [22–24]. These effects of incubation should not be overlooked because of the impact they might have on the bone development of chicks and on broiler leg health. We suggest, based on the observations in this study, that short periods of temperature stress during transportation of chicks may increase the incidence of some leg problems. The optimal temperatures and ventilation conditions for transportation of chicks are not well established [10–13]. Therefore, we conclude that a need exists for further research in this area and that more attention is needed on maintaining adequate environmental conditions during the early life of chickens to improve leg health.

CONCLUSIONS AND APPLICATIONS

  1. 1

    The L early and H late incubation temperatures of broiler chickens can affect the early development of long bones and increase the incidence of some leg problems and locomotion issues at 40 d of age.

  2. 2

    Incubation profiles should be revised and monitored, possibly to improve bone development and reduce leg problems in broilers without affecting hatchability.

  3. 3

    Transportation conditions from the hatchery to the farm can affect the leg health of broilers, especially the incidence of twisted legs.

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