You are on page 1of 19

2006 Poultry Science Association, Inc.

Effects of Early Feed Restriction on Performance and 


Ascites Development in Broiler Chickens Subsequently 
Raised at Low Ambient Temperature 
S. O 
̈ 
zkan,*,1 I. Plavnik,† and S. Yahav† 
*Ege University, Faculty of Agriculture, Department of Animal Science, ̇ I 
zmir 35100, Turkey; and †ARO The Volcani Center, Institute of Animal Science, PO Box 6, Bet Dagan 
50250, Israel 
Primary Audience: Researchers, Broiler Managers, Extension Personnel 
SUMMARY 
The  objective  of  this  study  was  to  examine  the  effectiveness  of  early-age  growth  limitation,  achieved  through  feed 
restriction  (FR),  as  a  means  of  reducing  ascites  mortality  in  broiler chickens exposed to low ambient temperatures. Feed 
restriction  was  applied  to  broilers  from  5  to  11  d  of  age  so  as to reduce their weight gain to about 40% of that of control 
broilers  that  were  fed  ad  libitum  (AL).  At  the  age  of  21  d  the  chickens  were  exposed  to  a  temperature  of  15°C,  which 
induced  ascites.  By  46  d  of  age,  ascites  incidence  and  mortality  in  the  feed-restricted  birds  were  reduced  to  15.79  vs. 
36.84%  and  7.89  vs.  26.32%,  respectively,  compared  with  those  in  the  controls  (P  <  0.05).  After  feed  restriction  was 
stopped,  the  FR  chickens  had  accelerated  weight  gain  and  improved  feed  conversion  ratio  from  11  to  18  d  of  age  (P  < 
0.05),  and  by  46  d  they  had  achieved  the  same  body  weight  as  the  AL  birds.  Ascitic  broilers  had  smaller relative breast 
muscle  and  spleen  weights  than  those  of  the  healthy  broilers  at  46  d  (P  <  0.05).  However,  the  relative  weights  of  lung, 
heart,  and  liver  and  the right ventricle weight per total ventricle weight (RV:TV) ratios were greater in ascitic broilers (P 
<  0.05).  At  age  37  d,  when  ascites  had  developed  but  not  yet  caused  mortality,  the  ascitic  broilers  had  lower  plasma 
concentrations  of  the  thyroid  hormones  thyroxine  and  triiodothyronine,  and  higher  hematocrit  values  (P  <  0.05)  in 
comparison  with  the  healthy  ones.  Ascitic  birds also had lower oxygen consumption at 6 wk (P < 0.05), which agrees with 
information  that  the  terminal  stage  of  the  ascites  syndrome  can  be  characterized  by  low  oxygen  consumption.  We 
concluded  that  the  early-age  feed  restriction  reduced  ascites  incidence  and  mortality  and  prevented  reduction  of  the 
thyroid hormone concentrations in male broilers reared at low ambient temperature from the age of 3 wk onward. 
Key words: ascites, early feed restriction, thyroid hormone, oxygen consumption 
2006 J. Appl. Poult. Res. 15:9–19 

DESCRIPTION OF PROBLEM 
Ascites  in  broilers  is  associated  with  factors  such  as  fast  growth  rate and environmental pa- rameters, including 
low ambient temperatures 
1 Corresponding author: sezen.ozkan@ege.edu.tr 
(T 

)  and  high  altitude  [1].  The  syndrome  is  de-  fined  as  a  circuit  of  events  between  the  cardio-  vascular  and 
pulmonary  systems  responsible  for  metabolic  demands  [2].  The  association  of  asci-  tes  with  cardiopulmonary 
capacity and its ge- 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
JAPR: 10 Research Report netic background have been clearly demon- strated [3, 4], and Decuypere et al. [5] 
concluded that the hypothyroid state associated with the decreased metabolism for maintenance that is caused by 
continuous selection for fast growth and improved feed efficiency might be involved in ascites. The high metabolic 
rate in fast-grow- ing chickens, which increases dramatically in response to environmental conditions, leads to the 
development of the ascites syndrome, which may be characterized by enhancement of the erythropoiesis process [6]. 
This enhancement leads to a dramatic increase in the number of immature erythrocytes in the circulation and to a 
decline in the heart rate during early periods of growth [7]. These events lead to the develop- ment of hypoxemia 
[1], which can be confronted effectively by reducing oxygen demands, a mea- sure that can be achieved by early-age 
feed re- striction. 
Early  growth  restriction  induced  by  feed  re-  striction  has  resulted  in  improved  feed  effi-  ciency, because of the 
decrease  in  energy  re-  quirements  for  maintenance,  and  improved  car-  cass  quality  resulted  from  the  decline  in fat 
deposition  [8,  9].  Despite  this, conflicting find- ings have resulted from variations in the duration and severity of the 
restriction,  but,  nevertheless,  restriction  of  feed  either  as  nutritional  quality  or  quantity  of  feed or time accessing to 
feeders  is  one  of  the  primary  management  tools  currently  used  to  reduce  the  incidence  of  ascites  in  broiler 
production  [1,  10, 11, 12, 13, 14, 15, 16]. Feed restriction mainly reduces growth rate and, con- sequently, metabolic 
demands,  during  the  criti-  cal  periods  of  the  life  span  of  a  bird  [11,  12,  13,  14,  15,  16,  17,  18], and it is associated 
with  improvement  in  arterial  oxygenation  [10].  How-  ever,  feed  restriction  can  exert  negative  effects  on  the  body 
weight  at  marketing  age  [13]  and  on  the  relative  weight  of  breast  muscle  [12].  There  have  also  been  reports  of 
negative effects on thyroid gland activity [19] and on the plasma triiodothyronine (T 

(FCR) [23]. Recently, Luger et al. [24] reported that chickens that developed ascites could not produce T 

at  a  sufficient  rate  to  compensate  for  the  reduction  caused  by  exposure  to  cold,  which  coincided  with 
reduced T 

concentrations.  A  possible role of thyroid hormones in the develop- ment of the ascites 
syndrome has been sug- gested [6]. 
The  objective  of  the  present  study  was  to  elucidate  the  role  of  early-age  food  restriction on the development of 
the  ascites  syndrome  and  performance  related  parameters  in  broilers  reared under cold conditions from 3 wk of age 
onward. 
MATERIALS AND METHODS 
Experimental Design 
Male  broiler  chicks  (Cobb)  were  obtained  from  a  commercial  hatchery  and  housed  in  bat-  tery  brooders  under 
standard  management  con-  ditions  for  the  first  5  d  of  age.  At  5  d,  76  chicks  were  weighed,  wing-banded,  and 
randomly di- vided between 2 feeding groups with 7 replicates of 5 to 6 birds each. The chicks were exposed to T 

of  26.0  ±  1.0,  20.0  ±  1.0,  and  15.0  ±  1.0°C  at  7, 18, and 21 d of ages, respectively, to induce the development 
of  ascites  syndrome.  At  the  age  of 21 d, the birds were transferred to colony cages in a temperature-controlled room 
and kept at 15°C and 60% relative humidity until 46 d of age. 
Feeding 
Control  birds  were  fed  ad  libitum  (AL)  dur-  ing  the  experiment.  In  the  growth-restricted  group,  chicks  were 
exposed  to  feed restriction (FR) from 5 to 11 d of age; each chick was allowed a daily intake 18.7 g of feed that con- 
tained  sufficient  energy to support 50% of the normal growth rate. The energy allowance dur- ing FR was calculated 
according to the following equation modified from Plavnik and Hurwitz [9, 25]: 
EA = M × BW0.667 + G × GA 
where  EA  =  energy  allowance  (kcal),  M  =  main-  tenance  requirement  (1.5  kcal/g),  BW0.667  =  met-  abolic  body 
weight at the beginning of the feed restriction period (5 d), G = energy requirement 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
) concentration [20]. Alteration in thyroid hormone metabolism in ascites-susceptible broilers has 
been cited by several authors [21, 22, 23, 24], and low plasma triiodothyronine (T 

) concentration at low T 

has  been  reported  to  indicate  thyroid  insufficiency  associated  with 
ascites incidences in lines with a fast growth rate and low feed conversion ratio 
 
̈ O 
ZKAN ET AL.: EARLY FEED RESTRICTION AND ASCITES DEVELOPMENT 11 
for 1 g of growth (2 kcal/g), and GA = growth allowance (15 g/d). 
A  crumble  form  of  starter diet was supplied from d 0 to 21, and a pelleted grower diet was supplied from d 21 to 
46  of  the  experiment.  The  diets  were  designed  according to the National Research Council’s recommendations [26] 
and  contained  3,100  and  3,200  kcal/kg  of  metabolic  energy,  respectively,  and  22.6  and  19.6%  of  crude  protein, 
respectively.  Water  was  available AL, and continuous fluorescent illumination was applied to the broilers during the 
experimental period. 
Individual  body  weights  were  measured  at  5,  11,  18,  25,  and  46  d  of  age.  Feed  consumption  was  recorded 
weekly,  and  FCR  were  determined  for  each  replicate  (cage)  based  on  feed  consump-  tion  and  body  weight  gain 
including birds that died during the entire period. 
Blood  samples  were  taken  on  d  30  and  37  from  the  brachial  vein.  The  blood  samples  were  stored  at  4°C  for 
hematocrit  analyses,  and  an  aliquot  was  centrifuged  at  3,000  rpm  for  10  min  to obtain plasma, which was stored at 
−20°C pending further analyses. 
Ascites Diagnosis 
During  the  experiment,  all  dead  chickens  were  diagnosed  for  ascites  according  to  abdomi-  nal  and  pericardial 
fluid  accumulation  and  right  heart  enlargement.  At  the  end  of  the  experi-  ments,  all  chickens  were  euthanized  to 
detect  ascites  according  to  fluid  accumulation  in  the  body  cavities  and  to  right  heart  enlargement  [right  ventricle 
weight  per  total  ventricle  weight  (RV:TV)  ratio  >  0.28].  The  birds  that  showed  these  symptoms  were  considered 
ascitic  and  were  included  in  the  analysis  of  all  parameters  regarding  ascites.  Birds  not  showing  any  of  these 
symptoms were classified as healthy in all statis- tic analysis of each age. Birds having a slight hydropericardium but 
not showing right heart enlargement were also classified as healthy. 
Breast  muscle  (pectoralis  major  and  minor),  abdominal  fat pad, lung, heart, liver, and spleen were dissected and 
weighed. The RV:TV ratios were calculated. 
Hematocrit 
Blood in heparinized microcapillary tubes was centrifuged for 7 min for hematocrit (HCT) measurements. 
Thyroid Hormones 
Plasma samples were radioimmunoassayed for total T 

and T 

with commercial kits [27] validated for domestic fowl [28]. The T 

assay  was  characterized  by  intraassay and interassay CV of 7.0 and 9.4%, 
respectively, and the T 
4  assay  by  intraassay  and  interassay  CV  of  5.0  and  7.5%, 
respectively. The T 

assay  was  carried  out  according  to  the  manufacturer’s  instructions  without 
modifications, whereas in the T 

analy- sis 100-μL samples were used. 
Oxygen Consumption 
On  3  consecutive  days  during  the  sixth  week  of  age the oxygen consumption of 14 (7 from each feeding group) 
broilers  was  measured  with  an  oxygen  analyzer  [29]  according  to  the  proce-  dures  of  Yahav  and  Buffenstein  [30]. 
Birds  were  chosen  for  measurement  according  to  their  pre-  viously  measured  HCT  levels.  For  this  purpose,  3  or 4 
birds  with  high  (>41%)  or  low  (<41%)  HCT  were  chosen  from each feeding group, but the final descriptions of the 
birds as either ascitic or healthy were confirmed by necropsy at slaughter or death. 
Statistical Analysis 
Data,  except  for  feed  consumption  and  FCR,  were  subjected  weekly  to  2-way  ANOVA  with  respect  to  the 
following  main  effects:  ascites  (ascitic  or  healthy  birds), feeding (FR or AL feeding), and their interaction using the 
JMP  statistics  software  package  [31].  Body  weight  on  d  5  was  included  in  the model as a covariance parameter for 
the  body  weight  and  weight  gain  data.  Only  feeding  effect  was  included  in  the  statistical  model  for  feed 
consumption  and  FCR data. Least square means were separated with Student’s t-test [32]. The distribution of ascites 
incidence  and  mortality  within  feeding  groups  were  analyzed  with  the  chi-squared  test.  Shapiro  Wilk’s  normality 
test was performed on all data and, if necessary, a common log transformation was applied to the T 

, T 

,  and  HCT  data  to  obtain  a  normal  distribution  [32].  Actual  values,  however,  are 
presented in the tables. 
RESULTS Ascites Incidence and Mortality 
The feed restriction treatment reduced the total mortality, mortality from ascites, and over- 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
JAPR: 12 Research Report Table 1. Distribution of total mortality, mortality from ascites, ascites defined at slaughter, and total 
ascites incidence within feeding groups 
Total Mortality from Ascites defined Total ascites mortality ascites at slaughter incidence Trait (%) (%) (%) (%) 
Feed restriction (FR) 18.42 7.89 7.89 15.79 
n = 7/38 n = 3/38 n = 3/38 n = 6/38 Ad libitum (AL) 39.47 26.32 10.53 36.84 
n = 15/38 n = 10/38 n = 4/38 n = 14/38 Overall (FR + AL) 28.94 17.10 9.21 26.32 
n = 22/76 n = 13/76 n = 7/76 n = 20/76 χ2 = 4.166* χ2 = 4.756* χ2 = 0.158 χ2 = 4.438* 
*P < 0.05. 
all ascites incidence (Table 1) significantly (P < 0.05). Ascites mortality was first observed 1 wk after cold exposure, 
and all mortality oc- curred during the fifth (6 birds) and sixth (7 birds) weeks (data not shown). 
Body Weight and Gain 
Feed  restriction  resulted  in  a  lower  body  weight  (P  <  0.05; Table 2). However, at the end of the experiment, FR 
broilers achieved body weights similar to those of the AL birds. During the feed restriction period (d 5 to 11), the FR 
group  gained  38.94%  of  the  weight  that  the  AL  gained.  During  the  first  week  posttreatment  (d  11  to  18)  the  FR 
broilers  gained  significantly  more  weight  than  the  AL  ones  (P < 0.05), which suggests that their growth accelerated 
during  this  stage  of  life.  On the other hand, the FR birds did not show any further compensatory growth even during 
the  later  stages  of  life.  There  was  no  interaction  between  ascites  and  feeding regi- men for body weight and weight 
gain  at  any  age (Table 2). The body weights of ascitic and healthy birds differed significantly only at the age of 46 d 
(P < 0.05). 
Feed Consumption and FCR 
The  cumulative  feed  consumption  and  FCR  (5  to  46  d)  did  not  differ  between  the  feeding  regimens  (Table  3). 
The FR group performed better than the AL group from d 11 to 25 (P < 0.05). 
Relative Weights of Organs 
Ascites affected all carcass parameters with the exception of the abdominal fat (Table 4). 
At  slaughter  age,  ascitic  broilers  had  smaller  relative  weights  of  breast  muscle  and  spleen than those of the healthy 
birds,  but  the  relative  weights  of  lung,  heart,  and  liver  and RV:TV ratios were greater in the ascitic ones (P < 0.05). 
The  feeding  regimen  did  not  affect  any  of  these  above  parameters  (Table  4).  No  interactions among the treatments 
were observed in their effects on any of these traits. 
Hematocrit 
A  significant  effect  of  ascites  on  HCT  was  observed  at  37  d  of  age  (P  <  0.05;  Table  5).  Ascitic  birds  had 
significantly  higher  hematocrit  values than the healthy birds. However, the feed- ing regimen did not affect the HCT 
measure- ments at 30 and 37 d. 


and T 

Hormones 
The plasma T 

concentration  was  signifi-  cantly  lower  in  ascitic  than  in  healthy  broilers  at  30 and 37 d of age 
(P < 0.05) but was not affected by FR at these ages (Table 5). 
The plasma T 

concentration  was  lower  in  ascitic  than  in  healthy  birds  only  at  37  d  of  age,  whereas  FR  birds 
exhibited a significantly higher plasma T 

concentrations  than  the AL birds at 30 d (P < 0.05; Table 5). The interaction of ascites × feeding regimen 
was not significant for either trait at any age. However, at 30 d of age in the FR group, T 

levels  of  ascitic  broilers  were  similar  to  those  of  healthy  birds  (2.51  and  2.62  ng/mL, 
respectively), whereas in the AL group T 

levels  differed  significantly  (P  <  0.05)  between  ascitic  and  healthy  broilers  (1.92  and  2.99  ng/mL, 
respectively; data not shown). 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
̈ O 
ZKAN ET AL.: EARLY FEED RESTRICTION AND ASCITES DEVELOPMENT 13 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
JAPR: 14 
Research Report Oxygen Consumption 
Oxygen  consumption  was  lower  in  ascitic  than  in  healthy  birds  (P  <  0.05;  Table  6).  Feeding  did  not  affect 
oxygen consumption and the asci- tes × feeding interaction was not significant. 
DISCUSSION 
The  results  obtained  emphasize  the  signifi-  cant  and  positive  effects  of  feed  restriction  in  preventing  the 
development of the ascites syn- drome in broiler chickens. 
Performance and Mortality 
Feed restriction from 5 to 11 d of age reduced weight gain (to 38.9% of that in the AL broilers) and reduced FCR 
during  the  restriction  period.  Following  the  restriction  period  (11  to  18  d  of  age),  compensatory  growth  was 
observed in the FR birds. It seems that the severity of the restric- tion period allowed full growth compensation up to 
the  marketing  age,  as  was  previously  reported  [8,  9,  11,  17,  20,  22,  33,  34,  35].  The  FR  resulted  in  a  marked 
reduction  of  ascites  incidence  and  mortality  compared  with  AL  feeding,  which  is  consistent with previous findings 
[11,  18,  13,  14].  In  general,  susceptibility  to  ascites has been asso- ciated with high growth rates [1, 36], and a posi- 
tive  correlation  between  potential  growth  rate  and  percentage  ascites  has  been  reported  by  Deeb  et  al.  [37].  In  the 
present  study,  the  retardation of growth rate during the FR period could have been the main reason for the decline in 
ascites  inci-  dences  and  mortality,  but  it  should  be  noted  that  other  studies  have  found  that  ascitic  broilers  are  not 
necessarily  the  fastest  growing  individuals  in the flock [4, 24, 38, 39]. Furthermore, detrimental effects of ascites on 
body  weight  have  been  re-  ported  previously  [1,  38],  and  those  findings are consistent with the lower body weights 
of  ascitic  broilers  at  marketing  age  that  was  found  in  the  present  study.  Acceleration  of  growth  in  FR  broiler 
accompanied  with  low  ambient  tempera-  ture  could  result  in  hypoxemia  and  trigger  the  ascites.  However, this was 
not  the  case  and  FR  resulted  in  late  maturity and lower incidence of ascites in this experiment, which that FR might 
affect the development of ascites in a critical stage prior to low T 

exposure. In general, the present findings on the relative weights of carcass parts and internal organs and 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
̈ O 
ZKAN ET AL.: EARLY FEED RESTRICTION AND ASCITES DEVELOPMENT 15 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
JAPR: 16 Research Report Table 5. Effect of ascites and feeding regimen on hematocrit (HCT), triiodothyronine (T 

), and thyroxine (T 

) levels of broilers at 30 
and 37 d of age 
HCT (%) T 

(ng/mL) T 

(ng/mL) 
d 30 d 37 d 30 d 37 d 30 d 37 
Ascites1 
Ascitic 36.95 ± 1.03 40.24 ± 1.31a 2.21 ± 0.20b 1.94 ± 0.26b 3.29 ± 0.33 1.43 ± 0.32b 
(n = 18) (n = 13) (n = 12) (n = 10) (n = 12) (n = 10) Healthy 36.19 ± 0.59 36.59 ± 0.67b 2.80 ± 0.16a 2.73 
± 0.19a 3.03 ± 0.26 2.48 ± 0.23a 
(n = 40) (n = 48) (n = 18) (n = 19) (n = 18) (n = 19) Feeding 
FR2 35.89 ± 0.91 37.64 ± 1.12 2.56 ± 0.19 2.56 ± 0.23 3.78 ± 0.33a 2.12 ± 0.28 
(n = 32) (n = 33) (n = 13) (n = 15) (n = 13) (n = 15) AL 37.25 ± 0.76 39.19 ± 0.96 2.45 ± 0.16 2.11 ± 0.23 
2.54 ± 0.26b 1.79 ± 0.28 
(n = 26) (n = 28) (n = 17) (n = 14) (n = 17) (n = 14) P-values Source of variation 
Ascites  0.524  0.024  0.028  0.021  0.546  0.014  Feeding  0.256  0.364 0.650 0.171 0.007 0.415 Ascites × feeding 0.150 0.256 0.069 
0.375 0.224 0.289 
a,bValues with different superscripts for each main effect within age (column) differ (P < 0.05). 1Classification of birds as ascitic 
or healthy; ascitic data were derived from dead birds plus those inspected at the end of the experiment and having fluid 
accumulation in the abdomen, pericardium, or both and right heart enlargement (right ventricle weight per total ventricle weight 
> 0.28). 2FR = feed restriction; AL = ad libitum. 
on  the  RV:TV  ratios  of  ascitic  broilers  are  consis-  tent  with  previous  results  [1,  4,  5].  Increased  RV:TV  ratios and 
relative  weights  of  heart,  lung,  and  liver  reflected  the  enlargement  of  the  right  side  of  the  heart  and  edema  in  the 
supply organs. 
Table 6. The effects of ascites and feeding regimen on oxygen consumption of broilers at the age of 6 wk 
Oxygen consumption Ascites1 (mL/g per h; STP)2 
Ascitic 2.22 ± 0.43b Healthy 3.29 ± 0.37a Feeding3 
FR 3.00 ± 0.40 AL 2.51 ± 0.40 Source of variation P-values Ascites 0.043 Feeding 0.319 
a,bValues with different superscripts for each main effect within age (column) differ (P < 0.05). 1Classification of birds as ascitic 
or healthy; ascitic data were derived from dead birds plus those inspected at the end of the experiment and having fluid 
accumulation in the abdomen, pericardium, or both and right heart enlargement (right ventricle weight per total ventricle weight 
> 0.28). 2STP = standard temperature and pressure. 3FR = feed restriction; AL = ad libitum. 
The  significantly  lower  relative  weight  of  the  spleen  of  ascitic  broilers could be attributed to the stress responses of 
the  birds.  In  general,  re-  gression  of  lymphoid  organs  (e.g.,  the  spleen)  is  recognized  as  an  important  response  of 
chickens  to chronic stress [40, 41]. Significant reduction in abdominal fat pad size [8, 9, 34] and greater heart weight 
as  a  percentage  of  body  weight  [14,  20]  in  growth-restricted  birds  have  been  reported  before,  but  these  traits  were 
not affected by feed- ing in the present study. 
The  present  findings  showed  that  better  FCR  in  FR  than  in  AL  broilers  coincided  with  greater  weight  gain 
between  11  and  18  d  of  age,  but  the  FR  birds  did  not  perform  better  than  the  AL  ones  over  the  whole  production 
period.  This  finding  is  contrary  to  those  of  previous  studies,  which  reported  improvements  in  overall  feed 
conversion  ratio  as  the  most  consistent  result  of  early  feed  restriction  studies  [8,  9,  13,  25,  33,  35,  42].  This 
difference  may  be  attributed  to  the pronounced effect of cold stress on FR birds. Increased heat production rate with 
decreased  ambient  tempera-  ture  has  been  shown  in  broilers  [43].  In the present study the FR birds were smaller by 
the age of 46 d, probably because they had used a higher 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
̈ O 
ZKAN ET AL.: EARLY FEED RESTRICTION AND ASCITES DEVELOPMENT 17 
proportion of energy for maintenance than for growth. 
HCT, Thyroid Hormones, and Oxygen Consumption 
Ascites  had  a  significant  effect  on  HCT  levels  at  37  d  of age, and an increased HCT level is one of the defining 
characteristics of the ascitic broiler [15, 24, 44, 45]. 
The lowest levels of T 

to  hypoxemia  under  cold  and  low  oxygen  pressure  conditions (high altitude) have been suggested [1, 7, 15, 22, 46]. 
Our  findings  were  consistent  to  the  earlier  study  of  Scheele  at  al.  [47],  who  sug-  gested  that  low  oxygen 
consumption per meta- bolic body weight at low T 

indicated inadequate metabolic action and could lead to pulmonary hypertension syndrome (PHS) and, finally, asci- 
tes in broilers. It coincided with higher HCT levels in a male line selected for improved FCR and growth rate as 
compared with a standard broiler stock. In a recent study, Malan et al. [48] con- firmed the association between 
ascites incidence and low heat production, thus oxygen consump- tion, per metabolic body weight. In the present 
study the reduction in oxygen consumption could have been related to the development of the syn- drome, which 
impaired the overall performance of the broilers (i.e., feed intake and weight gain). It can be concluded that FR 
significantly re- duced the development of ascites, as it can be induced by other methods (e.g., light restriction, 
dietary energy, or using mash vs. pellet diets) [11, 16, 49, 50, 51]. The FR induced better FCR in FR broilers, which 
consequently exhibited greater weight gain from d 11 to 18. However, the FR broilers did not retain this advantage 
over the AL birds for the whole of the production period, possibly because of the more pronounced effect of cold 
stress on the FR birds than on the AL ones in the present study. The lower oxygen con- sumption observed in the 
ascitic birds during their sixth week of age could be attributed to the overall deterioration of the birds’ conditions. 
However, further research is required to elucidate this question. 
3.  Wideman,  R.  F.,  Jr.,  Y.  K.  Kirby,  R.  L.  Owen,  and  H.  French.  1997.  Chronic  unilateral  occlusion  of  an  extrapulmonary 
primary bron- chus induces pulmonary hypertension syndrome (ascites) in male and female broilers. Poult. Sci. 76:400–404. 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
and T 

hormones  that  were  observed  at  the ages of 30 and 37 d in the present study are in 
accordance with the results of Luger et al. [24], who reported lower plasma T 

and T 

concentrations  in  ascitic  broilers  than  in healthy birds approximately 1 wk before the death of the former. 
Plasma T 

concentrations  in  the  FR  broilers  were  higher  than  those  in the AL birds at d 30, and 
increased thyroid hormone activities during the compensatory growth period was to be expected [13, 19]. 
The similarity of the T 

levels  in  the  ascitic  and  healthy  FR  broilers  at  30  d  of  age  (2.51  and  2.62  ng/mL, 
respectively; data not shown) may lead to the conclusion that FR birds were able to keep plasma levels of T 

high until they developed ascites. This, in turn, may indicate that growth restriction resulted in enhanced recovery of 
thy- roid gland functions. However, even if this recov- ery was better, it was not to a high enough level to prevent 
ascites development in all the FR broilers. The significantly lower oxygen consumption in the ascitic broilers was 
measured at the age of 6 wk, when the syndrome was already developing, as was to be expected under cold 
conditions that result in additional demands on the metabolic load on the birds. Increased incidence of ascites due 
CONCLUSIONS AND APPLICATIONS 1. The FR significantly reduced the development of ascites and could be 
used effectively as a 
management treatment to prevent the development of the syndrome. 2. The FR used from d 5 to 11 enabled the 
broilers to compensate for weight gain deficiency during 
the treatment and to reach the same BW as the AL birds by marketing age (d 46). 3. Terminal stages of ascites 
syndrome could be characterized by low oxygen consumption. 
REFERENCES AND NOTES 
1. Julian, R. J. 1993. Ascites in poultry. Avian Pathol. 22:419– 454. 
2. Currie, R. J. W. 1999. Ascites in poultry: Recent investigations. Review. Avian Pathol. 28:313–326. 
 
JAPR: 18 
Research Report 4. Wideman, R. F. 2000. Cardio-pulmonary hemodynamics and ascites in broiler chickens. Avian Poult. 
Biol. Rev. 11:21–43. 
5.  Decuypere,  E.,  J.  Buyse,  and  N.  Buyse.  2000.  Ascites  in  broiler  chickens:  Exogenous  and  endogenous  structural  and 
functional causal factors. World’s Poult. Sci. J. 56:367–377. 
6.  Luger,  D.,  D.  Shinder,  D.  Wolfenson,  and  S.  Yahav.  2003.  Erythropoiesis  regulation  during  the  development  of  ascites 
syndrome in broiler chickens—a possible role of corticosterone. J. Anim. Sci. 81:784–790. 
7.  Olkowski,  A.  A.,  and H. L. Classen. 1998. Progressive brady- cardia, a possible factor in the pathogenesis of ascites in fast 
growing broiler chickens raised at low altitude. Br. Poult. Sci. 39:139–146. 
8.  Plavnik,  I.,  and  S.  Hurwitz.  1985.  The  performance  of  broiler chicks during and following feed restriction at an early age. 
Poult. Sci. 64:348–355. 
9. Plavnik, I., and S. Hurwitz. 1988. Early feed restriction in chicks: Effect of age, duration, and sex. Poult. Sci. 67:384–390. 
10.  Reeves,  J.  T.,  G.  Ballam,  S.  Hofmeister,  C.  Pickett, K. Morris, and A. Peacock. 1991. Improved arterial oxygenation with 
feed restric- tion in rapidly growing broiler chickens. Comp. Biochem. Physiol. 99A:481–485. 
11.  Shlosberg,  A.,  E.  Berman,  U.  Bendhaim,  and  I.  Plavnik.  1991.  Controlled  early  feed  restriction  as  a  potential  means  of 
reducing the incidence of ascites in broilers. Avian Dis. 35:681–684. 
12.  Acar,  N.,  F.  G.  Sizemore,  G.  R.  Leach,  R.  F.  Wideman,  Jr.,  R.  L.  Owen,  and  G.  Barbato.  1995.  Growth  of  broilers  in 
response to feed restriction regimens to reduce ascites. Poult. Sci. 74:833–843. 
13.  Gonzales,  E.,  J.  Buyse,  M. M. Loddi, T. S. Takita, N. Buys, and E. Decuypere. 1998. Performance, incidence of metabolic 
distur- bances and endocrine variables of food-restricted male broiler chickens. Br. Poult. Sci. 39:671–678. 
14.  McGovern,  R.  H.,  J.  J.  R.  Feddes,  F.  E.  Robinson,  and  J.  A.  Hanson.  1999.  Growth performance, carcass characteristics, 
and the incidence of ascites in broilers in response to feed restriction and litter oiling. Poult. Sci. 78:522–528. 
15.  Balog,  M.  J.,  N.  B.  Anthony,  M.  A.  Cooper,  B. D. Kidd, G. R. Huff, W. E. Huff, and N. C. Rath. 2000. Ascites syndrome 
and related pathologies in feed restricted broilers raised in a hypobaric chamber. Poult. Sci. 79:318–323. 
16.  Coello,  C.  L.,  M.  J.  Arce,  and  G.  E.  Avila.  2000.  Management  techniques  to  reduce  incidence  of  ascites  and SDS. Proc. 
XXI World’s Poult. Congr. WPSA, Montreal, Canada. 
17.  Yu,  M.  W.,  and  F.  E.  Robinson.  1992.  The  application  of  short-term  feed  restriction  to  broiler  chicken  production:  A 
review. J. Appl. Poult. Res. 1:147–153. 
18. Arce, J., M. Berger, and C. L. Coello. 1992. Control of ascites syndrome by feed restriction techniques. J. Appl. Poult. Res. 
1:1–5. 
19.  McMurtry,  J.  P.,  I.  Plavnik,  R.  W.  Rosebrough,  N.  C. Steele, and J. A. Proudman. 1988. Effect of early feed restriction in 
male  broiler  chicks  on  plasma  metabolic  hormones  during  feed  restriction  and  accelerated  growth.  Comp.  Biochem.  Physiol. 
91A:67–70. 
20.  Yahav,  S.,  and  I.  Plavnik.  1999.  Effect  of  early-age  thermal  conditioning  and  food  restriction  on  performance  and 
thermotolerance of male broiler chickens. Br. Poult. Sci. 40:120–126. 
21.  Decuypere,  E.,  C.  Vega,  T.  Bartha,  J.  Buyse,  J.  Zoons,  and  G.  A.  A.  Albers. 1994. Increased sensivity to triiodothyonine 
(T3) of broiler lines with a high susceptibility for ascites. Br. Poult. Sci. 35:287–297. 
22.  Buys,  N.,  C.  W.  Scheele,  C.  Kwakernaak,  J.  D.  Van  Der  Klis,  and  E.  Decuypere.  1999.  Performance  and  physiological 
variables  on  broiler  chicken  lines  differing  in  susceptibility  to  the  ascites  syndrome:  1.  Changes  in  blood  gases as a function of 
ambient temperature. Br. Poult. Sci. 40:135–139. 
23.  Buys,  N.,  C.  W.  Scheele,  C.  Kwakernaak,  and  E.  Decuypere.  1999.  Performance  and  physiological  variables  in  broiler 
chicken lines differing in susceptibility to the ascites syndrome: 2. Effect of ambient 
temperature on partial efficiencies of protein and fat retention and plasma hormone concentrations. Br. Poult. Sci. 40:140–144. 
24.  Luger,  D.,  D.  Shinder,  V.  Rzepakovsky,  M.  Rusal,  and  S.  Yahav.  2001.  Association  between  weight  gain,  blood 
parameters, and thyroid hormones and the development of ascites syndrome in broiler chickens. Poult. Sci. 80:965–971. 
25.  Plavnik,  I.,  and  S.  Hurwitz.  1991.  Response  of  broiler  chickens  and  turkey  poults  to  food  restriction  of  varied  severity 
during early life. Br. Poult. Sci. 32:343–352. 
26. NRC. 1994. Nutrient Requirements of Poultry. 9th ed. Natl. Acad. Sci., Washington, DC. 
27. Coat-A-Canine, T3 and T4 kits, Diagnostic Products Corpora- tion (DPC) Los Angeles, CA. 
28.  Yahav,  S.,  I.  Plavnik,  M.  Rusal,  and  S.  Hurwitz.  1998.  Re-  sponse  of  turkeys  to  relative  humidity  at  high  ambient 
temperature. Br. Poult. Sci. 39:340–345. 
29. Model S-3A/1 oxygen analyzer, Merom Instruments for Medi- cine and Research, Haifa, Israel. 
30. Yahav, S., and R. Buffenstein. 1991. Huddling behavior facili- tates homeothermy in Heterocephalus glaber. Physiol. Zool. 
64:871–884. 
31. SAS Institute. 2000. JMP: Statistics and Graphics Guide. Ver- sion 4. SAS Institute Inc., Cary, NC. 
32.  Steel,  R.  G.  D.,  and  J.  H.  Torrie.  1980.  Principles  and  Proce-  dures  of  Statistics:  A  Biometrical  Approach.  2nd  ed. 
McGraw-Hill Co., Columbus, OH. 
33.  Plavnik,  I.,  J.  P.  McMurtry,  and  R.  W.  Rosebrough.  1986.  Effects  of  early  feed  restriction  in  broilers.  1.  Growth 
performance and carcass composition. Growth 50:68–76. 
34.  Plavnik,  I.,  and  S.  Yahav.  1998.  Effect  of  environmental  tem- perature on broiler chickens subjected to growth restriction 
at an early age. Poult. Sci. 77:870–872. 
35.  Lee,  K.  H.,  and  S.  Leeson.  2001.  Performance  of  broilers  fed  limited  quantities  of  feed  or  nutrients  during  seven  to 
fourteen days of age. Poult. Sci. 80:446–454. 
36.  Peacock,  A.  J.,  C.  Pickett,  K.  Morris,  and  J.  T.  Reeves. 1990. Spontaneous hypoxaemia and right ventricular hypertrophy 
in fast growing broiler chickens reared at sea level. Comp. Biochem. Physiol. 97A:537–541. 
37.  Deeb,  N.,  A.  Shlosberg,  and  A.  Cahaner.  2002.  Genotype-by-  environment  interaction with broiler genotypes differing in 
growth rate. 4. Association between responses to heat stress and to cold- induced ascites. Poult. Sci. 81:1454–1462. 
38.  Wideman,  R.  F.,  and Y. K. Kirby. 1995. A pulmonary artery clamp model for inducing pulmonary hypertension syndrome 
(ascites) in broilers. Poult. Sci. 74:805–812. 
39.  Wideman,  R.  F.,  and  Y.  K.  Kirby.  1996.  Electrocardiographic  evaluation  of  broilers  during  the  onset  of  pulmonary 
hypertension initiated by unilateral pulmonary artery occlusion. Poult. Sci. 75:407–416. 
40. Siegel, H. S. 1995. Stress, strain and resistance. Br. Poult. Sci. 36:3–22. 
41. Puvadolpirod, S., and J. P. Thaxton. 2000. Model of physiolog- ical stress in chickens. 1. Response parameters. Poult. Sci. 
79:363–369. 
42.  Leeson,  S.,  and  A.  K. Zubair. 1997. Nutrition of the broiler chicken around the period of compensatory growth. Poult. Sci. 
76:992–999. 
43.  Koh,  K.,  and  M.  G.  Macleod.  1999.  Circadian  variation  in  heat  production  and  respiratory  quotient  in  growing  broilers 
maintained at different food intakes and ambient temperatures. Br. Poult. Sci. 40:353–356. 
44.  Maxwell,  M.  H.,  S.  Spence,  G.  W.  Robertson,  and M. A. Mitchell. 1990. Haematological and morphological responses of 
broiler chicks to hypoxia. Avian Pathol. 19:23–40. 
45. Shlosberg, A., M. Bellaiche, G. Zeitlin, M. Yaacobi, and A. Cahaner. 1996. Hematocrit values and mortality from ascites 
in cold- 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 
 
̈ O 
ZKAN ET AL.: EARLY FEED RESTRICTION AND ASCITES DEVELOPMENT 19 
stressed broilers from parents selected by hematocrit. Poult. Sci. 75:1–5. 
46.  Yersin,  A.  G.,  W.  E.  Huff,  L.  F.  Kubena,  M. H. Elissalde, R. B. Harvey, D. A. Witzel, and L. E. Giroir. 1992. Changes in 
hematolog-  ical,  blood  gas,  and  serum  biochemical  variables  in  broilers  during  exposure  to  stimulated high altitude. Avian Dis. 
36:189–196. 
47.  Scheele,  C.  W.,  W.  De  Wit,  M.  T.  Frankenhuis, and P. F. G. Vereijken. 1991. Ascites in broilers. 1. Experimental factors, 
evoking symptoms related to ascites. Poult. Sci. 70:1069–1083. 
48. Malan, D. D., C. W. Scheele, J. Buyse, C. Kwakernaak, F. K. Siebrits, J. D. van der Klis, and E. Decuypere. 2003. 
Metabolic rate 
and its relationship with ascites in chicken genotypes. Br. Poult. Sci. 44:309–315. 
49. Lott, B. D., S. L. Brabton, and J. D. May. 1996. The effect of photoperiod and nutrition on ascites in broilers. Avian Dis. 
40:788–791. 50. Buys, N., J. Buyse, M. Hassanzadeh-Ladmakhi, and E. De- cuypere. 1998. Intermittent lighting reduces the 
incidence of ascites in broilers: An interaction with protein content of feed on performance and the endocrine system. Poult. Sci. 
77:54–61. 
51.  Hassanzadeh,  M.,  M.  H.  Bozorgmerifard,  A.  R.  Akbari,  J.  Buyse,  and  E. Decuypere. 2000. Effect of intermittent lighting 
sched- ules during the natural scotoperiod on T3-induced ascites in broiler chickens. Avian Pathol. 29:433–439. 
Downloaded from https://academic.oup.com/japr/article-abstract/15/1/9/755180 by guest 
on 24 November 2017 

You might also like