The effects of laying cycle upon the blood pH, blood gases and other

The effects of laying cycle upon the blood pH,
blood gases and other related parameters in
geese
B. KARADEMIR1*, I. KAYA2, O. UCAR3 and G. KARADEMIR4
1
Department of Internal Medicine, Faculty of Veterinary Medicine, Kafkas University, Kars-Turkey
Department of Animal Nutrition and Nutritional Diseases, Faculty of Veterinary Medicine, Kafkas University, Kars-Turkey
Department of Reproduction and Artificial Insemination, Faculty of Veterinary Medicine, Kafkas University, Kars-Turkey
4
Department of Animal Nutrition and Nutritional Diseases, Institute of Health Sciences, Kafkas University, Kars-Turkey
2
3
* Corresponding author : E-mail: <[email protected]> or <[email protected]>
SUMMARY
RÉSUMÉ
This study was carried out to determine the changes in venous blood pH,
HCO3- concentration, BE-ecf, BE-b, pCO2, ct-CO2, pO2 and O2sat every 6
h during the laying cycle of the goose. Seven geese (2 year-old, weighing
4.26 kg at average) with a laying cycle of 42 h were used. Diets were formulated to cover their nutrient requirements. After 15 days of adaptation
period, blood samples were collected every 6 h during the laying cycle. A
first decrease of HCO3- concentrations, base excess in extracellular fluid
(BE-ecf) or in blood (BE-b), pCO2 and ct-CO2 was observed at the 6th h,
following by a more marked reduction at the 30th h of the laying cycle.
Highly significant correlations were obtained between HCO3- concentrations, base excess, pCO2 and ct-CO2 (p < 0.001, correlation coefficients
were comprised between 0.946 and 1.000). Although blood pH values
remained within normal ranges, close to the inferior limit, multiple regression analyses evidenced links between blood pH, alkaline reserve and CO2
related parameters. By contrast, pO2 and the percentage of O2 saturation
(O2sat) fluctuated in an opposite way with the occurrence of 3 spikes at the
6th, 18th and the 30th h, and were highly positively correlated (p < 0.001, r
= 0.942). These results indicate that buffering systems (HCO3-, base excess)
and functional adaptive responses of lungs and probably kidneys are involved for blood pH regulation during the laying cycle in goose. Therefore, it
is suggested that decreased blood HCO3-, BE-ecf, BE-b, pCO2 and ct-CO2
should be corrected in geese, especially at the 30th h of laying cycle for animal’s health and productivity.
Effets du cycle de ponte sur le pH sanguin, les gaz du sang et les autres
paramètres associés chez l’oie. Par B. KARADEMIR, I. KAYA, O.
UCAR et G. KARADEMIR.
Keywords : Goose - laying cycle - blood pH - blood gas bicarbonate.
Les objectifs de cette étude sont d’analyser les variations dans le sang
veineux du pH, des concentrations de HCO3- et du CO2 total (ct-CO2), des
excès de bases dans le liquide extracellulaire (BE-ecf) et dans le sang (BEb), des pressions partielles de CO2 et de O2, et du pourcentage de saturation
de O2 (O2sat) durant le cycle de ponte chez l’oie. Sept oies âgées de 2 ans,
pesant 4.26 kg en moyenne et présentant un cycle de 42 heures ont été utilisées. Les rations alimentaires ont été adaptées pour que les besoins en
nutriments soient couverts. Après 15 jours d’adaptation, des échantillons
sanguins ont été prélevés toutes les 6 heures au cours du cycle de ponte. Une
première faible diminution des concentrations de HCO3-, des excès de
bases, de pCO2 et de ct-CO2 a été observée à la 6ème heure du cycle, suivie
d’une autre réduction, plus marquée à la 30ème heure. De très fortes corrélations positives ont été obtenues entre ces paramètres (p < 0.001, les coefficients de corrélations étant compris entre 0.946 et 1.000). Bien que les
valeurs du pH sanguin soient restées comprises dans les valeurs normales,
proches de la limite inférieure, l’analyse en régression multiple a mis en évidence des liens significatifs entre le pH sanguin, les réserves alcalines et les
paramètres associés au CO2. En revanche, pO2 et O2sat, très positivement
corrélés (p < 0.001, r = 0.942), ont montré des variations opposées caractérisées par 3 pics obtenus à la 6ème, 18ème et 30ème heures. Ces résultats indiquent que des systèmes tampons (HCO3-, excès de bases), et des réponses
fonctionnelles adaptatives des poumons et probablement des reins sont
impliqués dans la régulation du pH sanguin durant le cycle de ponte chez
l’oie. De ce fait, il est suggéré que les variations des concentrations de
HCO3-, du CO2 total, des pressions partielles de CO2 et des excès de base
dans le secteur extracellulaire et dans le sang devraient être corrigées afin
de préserver la santé et la productivité des animaux.
Mots-clés : Oie - cycle de ponte - pH sanguin - gaz sanguin - bicarbonate.
Introduction
For optimum productivity, the animals have to be in healthy conditions. Particularly, the pH of body fluids is maintained within narrow limits (7.35-7.45) [6]. It is also needed for
the maintenance of protein structure and function, which
represent essential conditions for normal progression of
metabolic events [4]. These pH ranges have been also validated for geese, as with other animals [22].
The blood pH, HCO3- concentration (mmol/L), base
excess of extracellular fluid (BE-ecf, mmol/L), base excess
of blood (BE-b, mmol/L),CO2 pressure (pCO2, mmHg),
Revue Méd. Vét., 2005, 156, 5, 275-280
total CO2 (ct- CO2, mmol/L) O2 pressure (pO2, mmHg) and
O2 saturation (O2sat, %) are related parameters to each other
[6, 19]. Changes in one of them immediately affect others
and thus can impair all body functions. In healthy individuals, approximately 60% of CO2 is transported within the
blood stream in the form of bicarbonate. Carbonic acid
(H2CO3) is formed when dissolved CO2 combines with
water in the erythrocytes with the aid of Carbonic anhydrase
enzyme. H2CO3 spontaneously ionises to H+ and HCO3-.
The oxygen affinity of haemoglobin (Hb) is influenced by
H+ status so-called as to the Bohr effect [12]. Alveolar
macrophages have a crucial role in defence system of the
lungs [10], as they are capable of destroying microorganisms
276
(such as bacteria and viruses) by phagocytosis. For this,
these cells need a high content of pO2 and a correct pH.
Undoubtedly, a low pO2 and acidosis reduce pulmonary
macrophage functions [23].
CaCO3 was the mainly constituent of the eggshell. The
necessary Ca2+ is provided from either the bone or nutrients,
while CO32- is obtained from the blood HCO3-. HCO3concentrations and pH decline to their minimum values in
blood at the 22nd h during the laying cycle in hens [14]. At
this time, the pH was reported to be 7.34 in hens [11].
Additionally, the changes in CO2 contents in blood can affect
both the pH and eggshell quality [14]. It was also reported
that low blood pH and HCO3- concentrations impair the eggshell thickness [24]. Thus, several experimental protocols
have been proposed in laying hens to restore blood pH and
HCO3- concentrations and consequently to improve the eggshell quality [2, 5, 9].
The values of blood pH, pCO2 and pO2 in geese and in
chickens were reported to be numerically similar to each
other [21, 22]. Additionally, it was also reported that no
significant changes of these parameters were observed in different races, seasons or genders in geese [22].
Little information about the effects of laying cycle upon
blood pH, gases and other related parameters is available in
geese. Therefore, the aim of the present study was to determine the influence of laying cycle on venous blood pH,
HCO3- concentration, BE-ecf, BE-b, pCO2, ct-CO2, pO2 and
O2sat in geese.
Materials and methods
KARADEMIR (B.) AND COLLABORATORS
TABLE I. — Ingredients and chemical composition of geese diet.
a For per kg : vitamin A 4 800 000 IU, vitamin D 96 000 IU, vitamin E
3
12 000 mg, vitamin K3 1 000 mg, vitamin B1 1 200 mg, vitamin B2 2 800
mg, vitamin B6 1 600 mg, vitamin B12 6 mg, nicotinamide 16 000 mg,
calcium-D-pantothenate 3200 mg, folic acid 400 mg, D-biotin 18 mg,
vitamin C 20 000 mg, chlorine 50 000 mg, manganese 32 000 mg, iron
16 000 mg, zinc 24 000 mg, copper 2 000 mg, iodine 160 mg, cobalt 40
mg, selenium 60 mg, antioxidant 4 000 mg.
b Calculated from the tabular values [18].
ANIMALS
Seven out of 98 native (local, cross-bred), 2 year-old geese
(from Kars district) were used in their second laying period
for this study. Selection of these animals was made as follows : It was observed that the laying cycles of these 98
geese lasted from 38 h to 52 h and each goose laid an average
of 10 to 15 eggs within the laying period. Then, observations
during a couple of laying cycle of individuals also showed
that most animals with regular cycle had about 42 h laying
interval and the total number of them was only seven. The
average weight of these animals was 4.26 kg and they were
kept in individual cages with a self-feeder and water ad libitum. Since the room where the animals were kept had presented irregular light supply, a continuous (24 h) lighting
scheme were applied for standardisation of this condition
during the study, as also routinely used in laying hens.
The animals were fed by a basal diet formulated to cover
their nutrient requirements [18] (the composition is given in
table I).
BLOOD COLLECTIONS
After 15 days of adaptation period, a total of one ml of
blood samples was collected from the vein, V. cutanea ulnaris (in plastic syringes containing 500 IU/ml heparin) within
the first hour of laying. Then, the collections were continued
at every 6 h during the whole laying cycle until the 36th h.
Since all the 7 geese used have not laid promptly at the 42nd
h (some laid just before, while others just after), it was considered that blood samples to be collected at that time would
lead inconsistency in the results. Therefore, sample collections at the 42nd h were neglected. Following the collections,
the anaerobic condition of blood samples was obtained by
closing the syringes with glass putty and blood samples were
then kept at 0-5°C until the analyses made within 30 minutes
after collections [3].
LABORATORY ANALYSES
Chemical Analysis : The parameters of dry matter (DM),
organic matter (OM), crude protein (CP), ether extract (EE),
crude fibre (CF), nitrogen-free extract (NFE) of diet were
determined by AOAC [1]. The values of metabolisable
energy (ME), calcium (Ca) and phosphorus (P) were also
calculated from the tabular values [18].
Biochemical Analyses : For analyses of the blood pH,
HCO3- concentration (mmol/L), base excess of extracellular
fluid (BE-ecf) (mmol/L), base excess of blood (BE-b)
(mmol/L), pCO2 (mmHg), total CO2 (ct-CO2) (mmol/L),
pO2 (mmHg) and O2 saturation (O2sat) (%) a Rapid Lab 248
pH/Blood Gas Analyzer (Chiron Diagnostics, USA) was
used. Control of accuracy was performed using a commercial quality control solution (Complete®, Bayer, East
Walpole, USA). Control values were within the normal
ranges as described by the manufacturer. To determine techRevue Méd. Vét., 2005, 156, 5, 275-280
BLOOD PH, BLOOD GASES AND LAYING CYCLE IN GEESE
nical precision of all the parameters, blood samples collected
from 7 geese were analysed five times each. Coefficients of
intra-assay and inter-assay variations of these parameters
were as follows : pH : 0.02 - 0.52% ; HCO3- : 0.04 - 3.78% ;
BE-ecf : 0.26 - 20.46% ; BE-b : 0.30 - 27.02% ; pCO2 : 1.58
- 3.61% ; ct-CO2 : 0.21 - 3.67% ; pO2 : 0.24 - 5.91% and
O2sat : 0.02 - 5.37% , respectively.
STATISTICAL ANALYSIS
Data collected from the 7 geese whom the laying cycle has
lasted about 42 h were used for statistical analysis.
Firstly, data were analyzed by paired t test: comparisons
between each time points for each of the parameters were
made by considering paired individual data [15] and differences were considered to be statistically significant at
P<0.05.
Secondly, Pearson’s correlation test was used to have an
idea about the relationships between the blood parameters.
Then, simple regression analyses was used for the analyses
of parameters that have presented statistically significant
correlation (P<0.05) to give more detailed results, and parameters (blood pH, HCO3-, BE-ecf, BE-b, pCO2 and ct-CO2)
suspected to be related closely [6, 19] were finally analysed
by multiple regression analyses.
Minitab statistical software programme [17] was used for
all the analysis methods.
Results
The mean values of blood pH, HCO3- concentration, BEecf, BE-b, pCO2, ct-CO2, pO2 and O2sat according to time
intervals during the goose laying cycle are summarised in
table II.
During the laying cycle, pH values decreased at the 12th 18th h, slightly increased at the 24th h, then decreased again
at the 30th h, but not significantly, before roughly reaching
initial values at the 36th h (table II). Some positive significant correlations were obtained between blood pH values
and BE-ecf or BE-b or O2sat (table III). The correlation coefficients of simple regression were 0.306 (p < 0.05), 0.434 (p
< 0.01) and 0.424 (p < 0.01), respectively. Multiple regression analysis showed that pH, HCO3- concentrations, BE-
277
ecf, BE-b, pCO2 and ct-CO2 were closely related (p < 0.001,
table IV).
HCO3- concentrations, BE-ecf, or BE-b globally tended to
decrease during all the duration of laying cycle (1st h vs. 36th
h: p < 0.05). Moreover, the 3 parameters have presented
simultaneous variations with first slight drops at the 6th h (1
h vs. 6 h and 6 h vs. 12 h: p < 0.05) and more marked
declines at the 30th h (24 h vs. 30 h and 30 h vs. 36 h: p <
0.05) (table II). HCO3- concentration, BE-ecf and BE-b were
highly positively correlated together (p < 0.001) (figure 1).
The correlation coefficients were 0.982, 0.946 and 0.990 for
HCO3- concentrations and BE-ecf, HCO3- concentrations
and BE-b and for BE-ecf and BE-b, respectively. Similar
fluctuations of pCO2 and ct-CO2 were also noticed throughout the laying cycle : these 2 parameters showed a first
slight decline at the 6th h (1 h vs. 6 h and 6 h vs. 12 h: p <
0.05), then they markedly decreased again at the 30th h (24 h
vs. 30 h and 30 h vs. 36 h: p < 0.05) (table II). A strong positive correlation was obtained between pCO2 and ct-CO2 The
regression equation was pCO2 = 1.57 ct-CO2 , r = 1, p <
0.001. Furthermore, pCO2. was positively correlated with
HCO3- concentrations (r = 1, equation : pCO2 = 1.65 HCO3-,
p < 0.001), BE-ecf (r = 0.982, equation: pCO2 = 42.5 + 1.55
BE-ecf, p < 0.001) and BE-b (r = 0.946, equation: pCO2 =
43.8 + 1.80 BE-b, p < 0.001) (table III, figure 2a,b). In the
same way, ct-CO2, HCO3- concentrations, BE-ecf and BE-b
were significantly closely related (p < 0.001). The respective
correlation coefficients and regression equations were:
- for HCO3- concentrations and ct-CO2: r = 1, HCO3- =
0.952 ct-CO2
- for BE-ecf and ct-CO2: r = 0.982, BE-ecf = 0.974 ct-CO2
- 26.3
- for BE-b and ct-CO2: r = 0.946, BE-b = 0.784 ct-CO2 21.7.
Although pO2 and the percentage of O2sat were also diminished during all the laying cycle like pCO2, HCO3- concentrations, BE-ecf and BE-b, opposite variations (spikes whom
the magnitude gradually decreased) were noticed at the 6th,
18th and 30th h (1 h vs. 6 h and 6 h vs. 12 h: p < 0.05; 12 h vs.
18 h and 18 h vs. 24 h: p < 0.05; 24 h vs. 30 h and 30 h vs. 36
h: p < 0.05) (table II). A highly significant correlation was
obtained between pO2 and O2sat (r = 0.942, equation: pO2 =
0.921 O2sat - 15.5, p < 0.001) (table III, figure 3).
TABLE II. — Variations of blood pH, gases and other releated parameters during the goose laying cycle (Mean ± SEM)
The values with different superscripts within the same column are statistically significant (P<0.05).
Revue Méd. Vét., 2005, 156, 5, 275-280
278
KARADEMIR (B.) AND COLLABORATORS
TABLE III. — Correlation coefficients (r) of simple regression between blood pH, gases (pCO2, pO2)
and other related parameters measured in laying geese. BE-ecf: base excess of extracellular fluid,
BE-b: base excess of blood, O2sat: percentage of O2 saturation, ct-CO2: total CO2. * P<0.05;
**P<0.01; ***P<0.001.
TABLE IV. — Multiple regression analyses between blood pH, gases (pCO2) and other related parameters in laying geese. BE-ecf: base
excess of extracellular fluid, BE-b: base excess of blood, ct-CO2: total CO2.
* The parameters are highly correlated with other X variables (predictors) and have been removed from the equation.
Discussion
In the present study, we describe the effect of laying cycle
in geese upon the parameters of venous blood: pH, HCO3-,
BE-ecf, BE-b, pCO2, ct-CO2, pO2 and O2sat.
Decreases of blood pH were observed in hens during eggshell formation [14]. In goose, blood pH values remained
close to the physiological inferior limits (7.33-7.36 vs. 7.257.33 for geese [22] and 7.20-7.60 for the chicken [21]) and
differences between time points were not statistically significant.
CO2 + H2O ⇔ H2CO2 ⇔ H+ + HCO3⇑
Carbonic Anhydrase
According to equation given, HCO3- used for the formation of eggshell leads to an increase of H+ concentration in
blood. Similarly, an additional free H+ will be available
while CO32- is provided from HCO3- [14]. These elevations
of H+ concentrations would decrease the blood pH.
However, blood pH may also be influenced by other buffering systems (haemoglobin, hydrogeno-phosphates, proteinates, etc.) and by the functional adaptive responses of lungs
and kidneys (not directly explored in this study). Indeed,
although blood pH value may vary, more or less, in parallel
to fluctuations of related parameters (HCO3- concentration,
BE-ecf, BE-b, pCO2 and ct-CO2) studied during the laying
cycle, it remained at around physiological limits in laying
geese.
In a first attempt, the tendency to acidosis will be compensated by the conversion of HCO3- into H2CO3. Base excess
in extracellular fluid (BE-ecf) and in blood (BE-b) are involved in the acid-base equilibrium and are highly correlated
together. The BE-ecf and BE-b have to be comprised between -4 and 4 mmol/L for compensations of acid-base fluctuations [13], otherwise blood pH and other relevant biochemical and physiological cellular functions would be inevitably impaired [4]. Consequently, blood HCO3- concentrations
and BE-ecf or BE-b decreased. These variations have been
observed firstly at the 6th h and finally at the 30th h during
the laying cycle. As pH values were only moderately correlated with HCO3- concentrations, BE-ecf and BE-b, other
buffer systems probably occurred for pH regulation or lungs
and kidneys would develop adaptive responses. Moreover,
the buffering capacity of blood HCO3- would be reduced
during laying cycle because CO32-, which are obtained from
HCO3- are required for eggshell formation. Consequently,
blood HCO3- concentrations gradually decline during egg
formation. It was previously reported that HCO3- concentrations were minimal at the 22nd h of the hen laying cycle [14].
In our study, this minimal value was obtained at the 30th h in
laying geese.
In this study, the values of pCO2 ranged from 35.27 to
52.27 mmHg that were similar to those reported previously
in geese (33 to 43.5 mmHg) [22] and in the chicken (17 to 56
mmHg) [21]. The H+ fixation by haemoglobin (Bohr effect)
would spare blood HCO3- concentrations and amplify H+
Revue Méd. Vét., 2005, 156, 5, 275-280
BLOOD PH, BLOOD GASES AND LAYING CYCLE IN GEESE
279
FIGURE 1. — Positive correlation between HCO3- concentrations and base excess in extracellular fluid (BE-ecf) (●) or in blood (BE-b)
(❍) obtained in geese during the laying cycle. The regression equations were HCO3- = 25.8 + 0.942 BE-ecf and HCO3- = 26.5 + 1.09
BE-b respectively. The regression equation between BE-ecf and BE-b was : BE-ecf = 0.761 + 1.19 BE-b.
FIGURE 2a. — Positive correlation between pCO2 and base excess in extracellular fluid (BE-ecf) (●) or in blood (BE-b) (❍) obtained
in geese during the laying cycle. The regression equations were pCO2 = 42.5 + 1.55 BE-ecf and pCO2 = 43.8 + 1.80 BE-b respectively.
FIGURE 2b. — Positive correlation between pCO2 and HCO3- concentrations (■) or ct-CO2 ( ) obtained in geese
during the laying cycle. The regression equations were pCO2 = 1.65 HCO3- and pCO2 = 1.57 ct-CO2 respectively.
pulmonary elimination via formation of H2CO3 into pneumocytes and dissociation into CO2 and H2O after Carbonic
Anhydrase action [8]. Indeed, pCO2 and ct-CO2 also decreased at the 6th and the 30th h and were strongly correlated with
HCO3- concentrations. Multiple regression were obtained
Revue Méd. Vét., 2005, 156, 5, 275-280
for pH, HCO3-, BE-ecf, BE-b, pCO2 and ct-CO2, indicating
that fluctuations of these parameters were linked to each
other [6, 19]. Simultaneously, pO2 and O2sat showed opposite variations with significant increases at the 6th, 18th and
30th h during the laying cycle. It is well known that the H+
280
KARADEMIR (B.) AND COLLABORATORS
FIGURE 3. — Positive correlation between pO2 and percentage of O2 saturation (O2sat) obtained in geese during the laying cycle. The
regression equations was pO2 = 0.921O2sat - 15.5.
fixation on haemoglobin decreases its affinity to O2 [12],
leading to increases of pO2 into blood. Nevertheless, pO2
and O2sat remained within normal ranges (pO2: 43.6- 62.7
vs. 41.5-56.6 mmHg for geese [22] and 25 to 68 mmHg for
the chicken [21]) throughout the laying cycle. Although no
precise O2sat values could not be found in literature for
geese, the present values observed (from 64.66 to 82.62%)
were very close to those (70%) reported to be ‘normal’ in
human [10]. These findings suggest that O2 equilibrium was
weakly affected by laying process. On the other hand, weak
increases of blood HCO3- concentrations, BE-ecf, BE-b,
pCO2 and ct-CO2 were noticed at the 12th and the 36th h, just
after each drops (at the 6th and the 30th h), suggesting the
occurrence of recovery mechanisms for alkaline reserve.
Although the urine acidity was not investigated during our
study, kidneys were probably involved for blood pH regulation by enhancing renal HCO3- reabsorption threshold and
urinary H+ excretion [7, 16, 19, 20].
In conclusion, HCO3- concentrations, BE-ecf, BE-b, pCO2
and ct-CO2, but also pO2 and O2sat at a lesser extend, exhibited marked fluctuations during the goose laying cycle, particularly at the 30th h, whereas blood pH remained relatively
constant. To overcome potentially debilitating effect of
laying process in geese, additives such as NaHCO3,
MgHCO3, KHCO3 and CaCO3 would be added to diets.
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