Journal of Thermal Biology 98 (2021) 102916 Available online 25 March 2021
0306-4565/© 2021 Elsevier Ltd. All rights reserved.
Effect of thermal conditioning on growth performance and thermotolerance in broilers: A systematic review and meta-analysis
Chris Major Ncho a, Vaishali Gupta b, Akshat Goel a,* a Department of Animal Science, Gyeongsang National University, Jinju, 52828, Republic of Korea b Department of Applied Life Science, Gyeongsang National University, Jinju, 52828, Republic of Korea
A R T I C L E I N F O Keywords:
Thermal conditioning Broilers Heat stress Meta-analysis
A B S T R A C T Thermal conditioning has been introduced as a cost-effective way to improve performance and thermotolerance in broilers. However, since all the trials were performed under various experimental conditions, it appears difficult to draw general conclusions. Therefore, the objective of this study was to quantify the response of broilers to thermal conditioning through a meta-analysis approach. A literature search was conducted on Scopus,
PubMed, Scielo, Web of Science, and Google scholar in December 2020. A restricted maximum likelihood random effect model was used to pool the effect sizes from the body weight gain (BWG), feed intake (FI), feed conversion ratio (FCR), and body temperature (Tb). BWG, FI, and Tb were computed using the standardized mean difference (SMD) while FCR was computed using mean differences (MD) with a 95% confidence interval (IC). Growth performances were evaluated during the thermoneutral conditions while Tb was evaluated after either acute or chronic heat stress after early age thermal conditioning. A total of 17 studies were included in the dataset. Thermal conditioning significantly increased BWG (SMD = 0.139, IC = 0.0372–0.2407, P = 0.0074) and
FI (SMD = 0.292, IC = 0.108–0.476, P = 0.0019) compared with the control. Additionally, subgroup analysis revealed that overall Tb was significantly reduced under acute heat stress (SMD = -0.455, IC = -0.718 to −0.192,
P < 0.001) but not affected during chronic heat stress (SMD = -0.115, IC = -0.651 to −0.420, P = 0.6729). In conclusion, thermal conditioning significantly increased the broiler’s BWG and FI under thermoneutral condi tions and can help in reducing Tb under acute heat stress.
1. Introduction As the global climate changes, environmental variation becomes a challenge for animal production (Nawab et al., 2018). Particularly in poultry cultivation, modern broiler breeds have been extensively sub mitted to selection for increasing their growth performances under mild climates (Sandercock et al., 2006). Additionally, the absence of sweat glands, as well as the presence of feathers, implies that chickens cannot regulate body temperature in high-temperature environments (Xie et al.,
2015).
Several studies demonstrated that early age thermal conditioning can be considered as a technique for mitigating the adverse impact of high ambient temperature in broiler production (De Basilio et al., 2001;
Oke et al., 2020; Yahav, 1999). Although different temperatures and time-period have been tried by the researchers, the method for thermal conditioning is similar and the temperature is kept slightly higher than the recommended one for few hours or even days for this purpose (Fig. 1). The improvement of broiler’s thermotolerance via thermal conditioning was made possible due to the immaturity of the mechanism of temperature regulation during the first week of their life (Modrey and
Nichelmann, 1992) which is firmly linked to sympathetic neural activity and the integration of thermal information in the hypothalamus (Kin ney, 1992). In addition, evidence shows that submitting broilers to thermal conditioning can bring about better development in growth performances as well as higher carcass yield (Bengharbi et al., 2016b;
Uni et al., 2001).
However, despite the fact that extensive research has been conducted to explore the role of thermal conditioning, there are numerous di vergences among the outcomes acquired from the literature. Therefore, it is critical to evaluate the previously published data to discover the potential effectiveness of thermal conditioning in broiler production.
The current study aimed to quantify the reaction of broilers to thermal conditioning through a meta-analysis approach. Growth parameters such as body weight, feed intake, and feed conversion ratio were
* Corresponding author.
E-mail address: genesakshat@gmail.com (A. Goel).
Contents lists available at ScienceDirect Journal of Thermal Biology journal homepage: http://www.elsevier.com/locate/jtherbio https://doi.org/10.1016/j.jtherbio.2021.102916
Received 3 February 2021; Received in revised form 19 March 2021; Accepted 19 March 2021
Journal of Thermal Biology 98 (2021) 102916 2 evaluated during thermoneutral conditions and body temperature was evaluated during high ambient temperature conditions.
2. Materials and methods 2.1. Search and data filtering
The studies’ research was conducted by consulting the following electronic databases: Scopus, PubMed, Scielo, Web of Science, and
Google scholar in December 2020. Performing the research in such a wide variety of repositories prevents from including articles found in only one database. The keywords considered for the research were:
“thermal acclimation”, “thermal conditioning”, “heat conditioning”,
“temperature conditioning”, “broilers” as well as their different combi nations. Two independent researchers conducted the research. Studies before inclusion in the database were critically analyzed subsequently by their title, abstract, and finally the full text. A study was selected only after the agreement of both researchers. No author has been contacted to ascertain further information or to obtain unpublished data.
The main criteria to select the published articles were: (i) articles should be published in the English language in peer-reviewed journals; (ii) broilers were used as experimental animals; (iii) articles should include at least one treatment of thermal post-hatch conditioning; (iv) all thermal conditioning parameters (temperature, duration, starting age) should be available in the material and method; (v) articles should evaluate heat conditioning (cold conditioning studies were not included in the database); (vi) for studies evaluating heat stress responses there should be a control treatment under heat stress conditions. After the filtering step, the final database included data collected from 17 papers.
2.2. Data recording and coding The response traits extracted from the studies were categorized as follows: growth parameters and body temperature. From each study, the mean, standard deviation, or standard error of the mean (SEM) and the number of animals in each treatment were extracted. When the standard deviation was not reported, it was calculated based on the standard error of the mean. Since there was a shortage of data from studies that reported growth performances under heat stress and to just consider the effect of the thermal conditioning, only the growth parameters reported under standard housing temperature were included in the dataset. The body weight gain (BWG), feed intake (FI), and feed conversion ratio (FCR) were the traits considered. The body temperature under heat challenge (Tb) was the last response trait extracted for analysis.
2.3. Statistical analysis The package “metafor” of the R software version 4.0.3 (R Core Team,
2020), was utilized to conduct all statistical analyses and generate fig ures. A restricted maximum likelihood random effect model was used to analyze the dataset. Due to the distinct nature of the response traits, they were computed using the standardized mean difference (SMD) except
FCR which was transformed in the mean difference (MD) as previously executed by De Toledo et al. (2020). Concerning the Tb, a subgroup analysis was carried out by splitting the different heat stress categories to evaluate heterogeneous results and making comparisons between these groups. The two subgroups considered were chronic and acute heat stress. Studies were included in one group or another depending on the category of heat stress they considered in their design. Heterogeneity was evaluated by the calculation of the Chi-square test (Q) and the I2 statistic. Substantial heterogeneity was noticed if P-value < 0.05 (Q) and/or I2 > 50%. Finally, publication bias was assessed via Egger’s test and the realization of funnel plots.
3. Result 3.1. Study selection process Details regarding the selection process of studies are showed in
Fig. 2. The literature searches in the electronic repositories for articles published from 1996 to 2020 retrieved a total of 8040 studies. After removing 1348 duplicates, the number of articles remained 6692. A thorough screening of the abstracts and the titles of these articles resulted in the exclusion of 6662 records that were not directly linked to our topic. Subsequently, from the 30 articles retained, 11 were excluded due to the lack of significant data helpful in the study after analysis of the full text. Moreover, 2 articles that were evaluating cold conditioning were not selected in light of the fact that the motivation behind this review was just to access the impacts of heat conditioning.
3.2. Dataset description Table 1 shows the characteristic of the articles selected for the meta- analysis. The frequency of strains used in the studies was the following:
Arbor Acres (n = 1); Ross (n = 3); Hubbard (n = 3); Cobb (n = 7) and 3 studies did not specify the strain of the broiler chicken. Fig. 3 presents the bubble chart of the studies selected in the meta-analysis. The tem perature of conditioning varied widely from 35 ◦C to 40.5 ◦C. Most of the studies applied a duration of conditioning of 1 day (n = 11). A total of 4 studies did not include a heat challenge in their design while 6 opted for chronic heat stress and 7 for acute heat stress. The overall heat stress temperature variation ranged from 30 ◦C to 43 ◦C. The most-reported response trait was BWG (14 studies) followed by FI (12 of studies),
FCR (9 studies), and Tb (9 studies). The summary statistics of the re sponses traits evaluated are presented in Table 2.
3.3. The effect of thermal conditioning on growth performances in broilers
The forest plot (Fig. 4) indicates that there was an overall positive effect on the BWG of birds that were thermally conditioned compared to the control birds (SMD = 0.139, IC = 0.0372–0.2407, P = 0.0074).
Heterogeneity was present in this effect since I2 = 57.7% with P-value
<0.001. Similarly, in Fig. 5 the diamond position reflects the positive effect of thermal conditioning on the FI in broilers. The overall effect
Fig. 1. Diagram explaining thermal conditioning process. Thermal condition ing consists of exposing birds in their first week of life to acute heat spells in order to enhance their thermal resistance in their later life. Temperature can range from 35 ◦C up to 40.5 ◦C and the duration of exposure is usually 24 h.
C.M. Ncho et al.
Journal of Thermal Biology 98 (2021) 102916 3 was estimated at SMD = 0.292, IC = 0.108–0.476, P = 0.0019 with significant heterogeneity (I2 = 85.7% with P-value <0.001). Fig. 6 shows that there was no significant effect of thermal conditioning on the
FCR of broilers (MD = -0.013, IC = -0.0307–0.0041, P = 0.1346).
Moreover, significant heterogeneity was observed (I2 = 89.7%; P value
< 0.001).
3.4. The effect of thermal conditioning on body temperature in broilers
During the heat challenges, the difference in body temperature be tween the thermally conditioned birds and the control was wider at the two extreme ambient temperatures (30 and 43 ◦C) while between 36 and
39 ◦C, body temperatures of both groups were similar (Fig. 7A). During acute heat stress, the birds recorded an overall higher body temperature compared to the data collected from studies that evaluated chronic heat stress (Fig. 7B). The diamond in the forest plot (Fig. 8) indicates an overall lower Tb in thermally conditioned birds compared to the control group (SMD = -0.315, IC = -0.584 to −0.046, P = 0.0219) under heat stress. This effect was significantly heterogeneous (I2 = 73.9% with P- value <0.001). The subgroup analysis showed a significant reduction in the body temperature of thermally conditioned birds during acute heat stress (SMD = -0.455, IC = -0.718 to −0.192, P < 0.001). However, under chronic heat stress, thermal conditioning did not show any statistically significant difference in Tb compared to the control group (SMD = -0.115, IC = -0.651 to −0.420, P = 0.6729). Publication bias.
Fig. 9 shows funnel plots of the parameters studied in this meta- analysis. The symmetry of all funnel plots was confirmed by Egger’s linear regression test. Results were not significant for BWG (t = 0.06, df
= 31, P = 0.9524), FI (t = -0.40, df = 29, P = 0.6925), FCR (t = 0.65, df
= 24, P = 0.5245), and Tb (t = 0.84, df = 30, P = 0.4098). Thus, there was no risk of publication bias detected in this study.
4. Discussion The livestock industry is extremely competitive. Extensive selection and nutritional programming emphasize for identifications of new methods for improving growth performances and heat tolerance in broiler chickens. Several trials evaluating the impact of early thermal conditioning on growth performances and thermotolerance of broilers have been conducted over the last decade. Nonetheless, up-to-date in formation summarizing the result from the previous experiment on this topic remains scarce. Thus, this review was an attempt to evaluate the potential outcomes of thermal conditioning in broilers through a sta tistical meta-analysis approach. In this study, since moderate to high heterogeneity was detected in all the response traits evaluated, a random effect model was applied. Indeed, random-effect methods
Fig. 2. Process for studies selection. A total of 8040 studies were retrieved from the electronic repositories (PubMed, Web of Science, Scopus, Scielo, Google Scholar).
Finally, a total of 17 studies were included in the meta-analysis.
C.M. Ncho et al.
Journal of Thermal Biology 98 (2021) 102916 4 explicitly account for the heterogeneity which represents the across- study variation (DerSimonian and Kacker, 2007).
One of the primary after-effects of the current examination is that thermal conditioning significantly increased the broiler’s BWG and FI while FCR was not affected. In general, the short-term exposure to heat during thermal conditioning results in subsequent growth retardation (Yahav and Hurwitz, 1996; Yahav et al., 1997). It is believed that the final increase in BWG and FI of thermally conditioned broilers is the result of a compensatory growth similar to that observed during feed restriction at an early age (Plavnik and Hurwitz, 1985). Indeed, it has been acknowledged that high housing temperature causes a deprivation in broiler’s FI leading to a reduction in body weight (Awad et al., 2020;
Farag and Alagawany, 2018). Therefore, growth is accelerated post-conditioning to totally compensate for the losses and sometimes result in higher body weight at marketable age (Yahav and McMurtry,
Table 1 Details of the studies included in the meta-analysis.
Author and year Strain Response variable extracted
Heat challenge Oke et al. (2020) Arbor acres BWG,FCR,FI
None Zaboli et al. (2017) Ross 308 BWG,FCR,FI,Tb Chronic
Uni et al. (2001) Cobb BWG,FCR,FI None De Basilio et al. (2001)
Cobb BWG,FI,Tb Acute Yahav and McMurtry (2001) Cobb
BWG,FCR,Tb Acute Taouis et al. (2002) Non- specified
BWG None Liew et al. (2003) Cobb BWG Chronic Yahav et al. (1997)
Non- specified BWG,FI Acute Abdelqader and Al-Fataftah (2014)
Hubbard BWG,FI,Tb Acute Kang et al. (2019) Ross BWG,FCR,FI
Chronic Marandure et al. (2011) Hubbard BWG,FCR,FI
Chronic Günal (2013) Ross 308 BWG,FCR,FI,Tb Chronic
Yahav and Hurwitz (1996) Cobb BWG,FCR,FI,Tb Acute Bengharbi et al. (2016a)
Hubbard 15 Tb Acute Zulkifli et al. (2003) Cobb Tb
Acute Yalçin et al. (2005) Non- specified Tb Chronic
Abdel-Fattah et al. (2018) Cobb 500 BWG,FCR,FI None
BWG: body weight gain; FI: feed intake; FCR: feed conversion ratio; Tb: body temperature.
Fig. 3. Bubble chart of the design of studies selected for the meta-analysis (n = 17 studies). The x-axis represents the studies included in the meta-analysis. The y-axis indicates the duration of the thermal condi tioning applied in each study (when treat ments evaluated a range of duration, the average value of all treatments was re ported). The diameter of the bubble specifies the temperature of conditioning applied in each study (when treatments evaluated a range of temperature, the average value of all treatments was reported). The color of the bubble designates the category of heat challenge broilers were submitted to in each study.
Table 2 Descriptive statistics of the response variables selected from studies used in the meta-analysis.
N Mean Median Min Max SE BWG (g) 50 1702.2 1890 94.7
2849.5 98 FI (g) 48 30005.8 3462.5 37.7 4940 219.3
FCR 40 1.92 1.82 1.38 2.7 0.05 Tb (◦C) 57 43.2 42.7
40.32 46.37 0.2 BWG: body weight gain; FI: feed intake; FCR: feed conversion ratio; Tb: body temperature.
C.M. Ncho et al.
Journal of Thermal Biology 98 (2021) 102916 5 2001). However, it is critical to make reference and there might be a correlation between the period of conditioning and the extent of sub sequent compensatory growth. Several studies (Yahav and Hurwitz,
1996; Yahav and McMurtry, 2001) reported no recovery in the growth performance parameters when the thermal conditioning period was extended above 24 h.
Interestingly, our results demonstrated that broiler’s Tb was signif icantly lower under heat stress when they were previously submitted to thermal conditioning. Tb has been generally utilized as a marker for heat stress resistance in broilers (Goel, 2021). Broilers due to the absence of sweat glands are more prone to heat stress which induces an increase in their Tb (Ensminger and Oldfield, 1990). Past examinations exhibited that lower Tb was frequently associated with a significant decline in triiodothyronine levels during exposure to heat stress (Yahav, 1999;
Yahav et al., 1997). Triiodothyronine, the major metabolic hormone plays a crucial role in thermoregulation in broilers and is positively correlated with heat production (Lin et al., 2006). In addition, the overall lower Tb observed in thermally conditioned birds may be an indicator of a lower metabolic rate proposing their ability to cope with high housing temperature (May et al., 1987). Furthermore, the subgroup analysis revealed that thermal conditioning was more effective in reducing broiler’s Tb under acute heat stress than chronic heat stress.
Fig. 4. Forest plot of the standardized mean difference and 95% confidence interval of the effect of thermal conditioning on body weight gain of broilers. The dashed vertical line represents a standardized mean difference of zero, or no effect. Points to the left of the dashed vertical line represent a reduction in body weight gain, while points to the right of the line indicate an increase in body weight gain in broilers that were thermally conditioned.
Fig. 5. Forest plot of the standardized mean difference and 95% confidence interval of the effect of thermal conditioning on feed intake of broilers. The dashed vertical line represents a standardized mean difference of zero, or no effect. Points to the left of the dashed vertical line represent a reduction in feed intake, while points to the right of the line indicate an increase in feed intake in broilers that were thermally conditioned.
C.M. Ncho et al.
Journal of Thermal Biology 98 (2021) 102916 6 The thermotolerance improvement observed after thermal conditioning might be explained by the concept of reactive physiology suggesting a long-lasting memory mechanism (Yahav et al., 1997). Undoubtedly, a large portion of the studies included in this meta-analysis were applying thermal conditioning as short-term acute heat stress at an early age.
Therefore, submitting broilers to the same category of stress in their later life could activate their thermoregulatory memory acquired during their early life.
Through a meta-analysis approach, this study attempted to synthe size the literature and provide a quantitative analysis of the effects of thermal conditioning on growth performances and thermotolerance of broilers. However, some limitations exist within the present study.
Firstly, because of the shortage of records, BWG, FI, and FCR were recorded only under standard housing temperature. Indeed, studies that evaluated acute heat stress in their design could not provide the related growth parameters. Therefore, the effects of thermal conditioning on growth performances of broilers under heat stress could not be evalu ated. Secondly, significant heterogeneity was present in the response traits, thus it should be taken into consideration when using the result of this study.
5. Conclusion Growth performances are the important parameter for broiler chickens. The meta-analysis highlighted the positive effect of thermal conditioning on broiler growth performances, especially regarding BWG and FI irrespective of the heat stress conditions. Body temperature is a vital indicator of stress during high ambient temperature. Early age
Fig. 6. Forest plot of the mean difference and 95% confidence interval of the effect of thermal conditioning on feed conversion ratio of broilers. The dashed vertical line represents a mean difference of zero, or no effect. Points to the left of the dashed vertical line represent a reduction in feed conversion ratio, while points to the right of the line indicate an increase in feed conversion ratio in broilers that were thermally conditioned.
Fig. 7. Body temperature records extracted from the studies included in the meta-analysis (n = 17 studies). (A) Evolution of broiler’s body temperature based on the heat challenge temperature. (B) Distribution of broiler’s body temperature according to the heat challenge category. Abbreviations: CON: Control; TC: Thermal conditioned.
C.M. Ncho et al.
Journal of Thermal Biology 98 (2021) 102916 7 thermal conditioning effectively reduces the broiler’s Tb under acute heat stress. The effect of thermal conditioning on chronic heat stress broilers was limited in terms of Tb, therefore, other strategies should be considered for helping broilers to cope with chronic heat stress.
Author statement Akshat Goel and Chris Major Ncho: Conceptualization, Methodology.
Chris Major Ncho and Vaishali Gupta: Data curation, Writing- Original draft preparation.Akshat Goel: Supervision. Akshat Goel and Chris
Major Ncho:Writing- Reviewing and Editing.
Fig. 8. Forest plot of the standardized mean difference and 95% confidence interval of the effect of thermal conditioning on body temperature of broilers after heat stress. The dashed vertical line represents a standardized mean difference of zero, or no effect. Points to the left of the dashed vertical line represent a reduction in body temperature, while points to the right of the line indicate an increase in body temperature in broilers that were thermally conditioned.
Fig. 9. Publication bias analysis, funnel plot. Egger’s Linear regression test of funnel plot asymmetry: A) body weight gain (t = 0.06, df = 31, P = 0.9524); B) feed intake (t = -0.40, df = 29, P = 0.6925); C) feed conversion ratio (t = 0.65, df = 24, P = 0.5245); D) body temperature (t = 0.84, df = 30, P = 0.4098).
C.M. Ncho et al.
Journal of Thermal Biology 98 (2021) 102916 8 Declaration of competing interest
The authors declare no conflicts of interest.
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