Ultrasonographic foetometry and maternal serum progesterone concentrations during pregnancy in Turkish Saanen goats

Accepted Manuscript Title: Ultrasonographic foetometry and maternal serum progesterone concentrations during pregnancy in Turkish Saanen goats Authors: Ebubekir Yazici, Erhan Ozenc, Haci Ahmet Celik, Mehmet Ucar PII: DOI: Reference:

S0378-4320(18)30075-7 https://doi.org/10.1016/j.anireprosci.2018.08.017 ANIREP 5919

To appear in:

Animal Reproduction Science

Received date: Revised date: Accepted date:

24-1-2018 8-7-2018 15-8-2018

Please cite this article as: Yazici E, Ozenc E, Celik HA, Ucar M, Ultrasonographic foetometry and maternal serum progesterone concentrations during pregnancy in Turkish Saanen goats, Animal Reproduction Science (2018), https://doi.org/10.1016/j.anireprosci.2018.08.017 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Ultrasonographic foetometry and maternal serum progesterone concentrations during pregnancy in Turkish Saanen goats Ebubekir Yazici, Erhan Ozenc, Haci Ahmet Celik, Mehmet Ucar Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Afyon Kocatepe

E-mail address of the Ebubekir YAZICI ,PhD, E-mail: [email protected] Erhan OZENC, PhD, E-mail: [email protected]

Mehmet UCAR, Professor, E-mail: [email protected]

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Haci Ahmet CELIK, Professor, E-mail: [email protected]

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University, 03200 Afyonkarahisar, Turkey

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Address for correspondence: Dr. Ebubekir Yazici, Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Afyon Kocatepe University, 03200, Afyonkarahisar, Turkey; Phone: +90 272 2281312; Mobile phone: +90 553 3969629; E-mail: [email protected]

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Gestational age can be estimated using ultrasonography in Turkish Saanen goats. Litter size can be determined in pregnancy based on progesterone concentrations. Progesterone levels are negatively correlated with the birth weights of the kids.

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Highlights

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ABSTRACT The objectives of the present study were (1) to generate reliable equations to estimate the gestational age of Saanen goats by measuring embryonic and foetal structures via B-mode ultrasonography (USG), (2) determine the maternal serum progesterone (P4) concentrations during pregnancy, and (3) compare the relationship between P4 concentrations and gestational

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age, litter size, and birth weight of kids. Seven pregnant goats were used in this study. Ultrasonographic examinations were performed transrectally from Days 15 to 27 of pregnancy

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at 3-day intervals and transabdominally from Days 30 to 128 at 7-day intervals. Blood samples were collected daily between Day 15 and 24 of gestation, and weekly from Day 27 to 128 to determine the serum P4 concentrations. Outer placentome diameter, biparietal diameter,

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occipito-nasal length, chest diameter, foetal heart rate, transversal heart diameter, orbit

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diameter, umbilical cord diameter, and kidney diameter were highly correlated with gestational

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age (P < 0.0001). Goats with twins had greater progesterone concentrations than those with a

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single foetus (P < 0.001). Furthermore, maternal serum progesterone concentrations detected

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on Days 51, 107, 114, and 128 of gestation were greater in goats carrying twins than those with a single foetus (P < 0.05). A negative correlation was evident between serum progesterone

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concentrations and birth weights of the kids (r = -0.78; P = 0.007). In conclusion, gestational age can be estimated using ultrasonographic foetometry, and litter size at specific times during

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pregnancy can be determined based on maternal serum progesterone concentration in Turkish Saanen goats.

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Keywords: Goat; Ultrasonography; Foetometry; Progesterone; Pregnancy; Foetus 1. Introduction Ultrasonography is an important technology to assist in increasing the reproductive efficiency of goats by determining the pregnancy status and litter size (Karadaev, 2015; Samir et al., 2016). Furthermore, gestational age (GA) may be estimated by measuring foetal

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structures on ultrasonography images (Kandiel et al., 2015; Jones et al., 2016). Previous studies reported that in goats, foetal age is highly correlated with embryonic vesicle diameter (EVD) (González de Bulnes et al., 1998), crown-rump length (CRL) (Abdelghafar et al., 2011; Abubakar et al., 2016), outer placentome diameter (OPD), biparietal diameter (BPD), and occipito-nasal length (ONL) (Karen et al., 2009; Nwaogu et al., 2010). Correlations of GA with

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other foetal measurements such as chest diameter (CD), orbit diameter (OD), and umbilical cord diameter (UCD) has also been reported in different goat breeds (Kailash et al., 2015;

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Kandiel et al., 2015). Estimation of foetal age would be useful to dry off lactating females in an adequate period and help protect them from pregnancy toxaemia during late gestation (Karen

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et al., 2001; Jones and Reed, 2017). Furthermore, it is important to feed the goats according to

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the period of gestation for more economical and accurate breeding (Sahlu et al., 1995; Rastogi

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et al., 2008; McGregor, 2016; Pillai et al., 2017). Thus, the determination of GA is important

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especially when the mating time is uncertain. Despite several studies on GA in diverse goat breeds, different equations may be needed for varying breeds (Kandiel et al., 2015). To the best

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of our knowledge, there is no study determining the GA in Turkish Saanen goats. Determination of maternal serum progesterone (P4) concentrations can be used for

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pregnancy diagnosis in goats (Zamfirescu et al., 2011). Additionally, there was a positive

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correlation between P4 concentrations and litter size (Manalu and Sumaryadi, 1998; Haldar et al., 2013), whereas a negative correlation was reported between P4 concentrations and the birth weights of kids (Basset and Thorburn, 1973). Although in a study of Turkish Saanen goats it

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was determined the serum P4 concentrations until Day 30 of pregnancy (Cengiz et al., 2014), there is no report on P4 concentrations at later pregnancy periods and the relationship between P4 concentrations and gestational age, litter size, and the birth weights of kids. Turkish Saanen goats, which emerged as the result of the cross-breeding of hairy goats and Saanen goats, successfully adapted to the breeding environment of hairy goats (Kaymakçı

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et al., 2005). Furthermore, Saanen goats have a greater performance than local breeds such as Malta, Gökçeada, and hairy goats with respect to daily weight gain, carcass quality, and milk yields (Tölü et al, 2010; Yalçıntan et al, 2010; Çelik and Oflaz, 2015). Due to these characteristics, there is an emphasis on increasing the numbers of Turkish Saanen goats (Erten and Yılmaz, 2013).

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This study is the first to generate reliable equations to estimate the gestational age (GA) by measuring the EVD, CRL, amnion vesicle diameter (AVD), OPD, BPD, ONL, chest

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diameter (CD), foetal heart rate (FHR), transversal heart diameter (THD), OD, UC, and kidney

diameter (KD) using ultrasonic images to determine the maternal serum P4 concentrations

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during pregnancy and to investigate the relationship between P4 concentrations and GA, litter

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size, and the birth weights of kids at parturition in Turkish Saanen goats.

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2. Materials and methods

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2.1. Experimental animals

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Pregnant Turkish Saanen goats (n = 14), ages ranging from 20 to 29 months of age and with weights between 46 and 55 kg, were used in this study. The data from these goats were

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used to measure the daily P4 concentrations between Days 15 and 24 of gestation. In the subsequent periods, however, abortions occurred in seven animals. The data used in the present

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study to measure and calculate the value for the other variables were from seven goats that gave birth to healthy kids. The animals were fed ad libitum with a basal diet that was formulated

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according to NRC (1981). Diet included 2032 metabolisable energy (Kcal/kg), 9.2% crude protein, and 1.44 dry matter intake (DMI) kg/animal (calculated) in the early periods and 2160 metabolisable energy (Kcal/kg), 11% crude protein, and 1.74 DMI (calculated) in the last 2 months of pregnancy. Ad libitum water was supplied and the goats were taken to forage in suitable weather conditions.

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2.2. Experimental design The Committee for Research and Animal Experiments of Afyon Kocatepe University approved the experimental protocol (registration number B.302.AKÜ.09Z.00.00173). The oestrous synchronisation was conducted using vaginal sponges containing 20 mg flurogestone

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acetate (Chronogest CR, Intervet, Turkey) for 6 days. Two days before the removal of the sponges, 400 IU PMSG (Chronogest/PMSG, 6000 IU/flk, Intervet, Turkey) and 0.075 mg dcloprostenol (Gestavet Prost, 0.075 mg/ml, Hipra, Turkey) were injected intramuscularly.

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Twelve hours after the removal of the vaginal sponges, fertile Turkish Saanen bucks were placed with the female goats for natural breeding (Özer and Doğruer, 2011). The does were

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separated from the bucks following an observed mating and the day of mating was recorded as

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day 0 of pregnancy (Karen et al., 2009).

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Ultrasonography was performed via a B-mode real time ultrasonographic machine

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(Medelkom SLE 301 MF, Lithuania) with a slim tipped, self-handled linear rectal probe (4.0-

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6.5 MHz) (human prostate probe) for a transrectal approach and a linear rectal probe (4.0-6.5 MHz) for a transabdominal approach. Transrectal examination was initiated on Day 15 of

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gestation and performed at 3-day intervals until Day 30 of gestation. Transabdominal ultrasonography was conducted from Day 37 to 128 of gestation at 7-day intervals. Due to

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unusual weather conditions, however, the examination was delayed from Day 72 to 74 of gestation. Transrectal and transabdominal examinations were performed according to the

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methods described by Vural et al. (2008), Karen et al. (2009), Gündüz et al. (2010), and Meinecke-Tillmann (2017). Ultrasonographic videos were recorded by an MP4 player (Orite PMP500, Australia) that was connected to the ultrasonography device and the videos were transferred to a computer. Screen images were collected and stored at the most convenient scene while observations were being made with a GOM Player (Gretech Corporation, Seoul, South Korea), and the images were measured with ImageJ software (National Institutes of Health,

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Bethesda, MD, USA). ImageJ values were calibrated beforehand as described by Bracken et al. (2006). The following structures were measured on the ultrasonography image: EVD: The longest diameter of the anechoic area considered the first pregnancy detected in the uterus (Suguna et al., 2008). 1) CRL: Distance between the top of the skull and the end of the sacrum

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(Abdelghafar et al., 2011). AVD: Longest diameter of the area limited by the amniotic membrane encircling the developing foetus (Graham III, 2010). OPD: Calculated mean of the

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three largest placentomes; measured placentomes resembled button-shaped protrusions in the early stage (Kähn, 1994) and grey shades and “C” or “O” shapes in the uterus fluid in the

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subsequent period (Suguna et al., 2008) (Fig. 1). BPD: Calculated outer distance between the

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parietal bones. Measurements were made as described by González de Bulnes et al. (1998) and

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Abdelghafar et al. (2011) (Fig. 2). ONL: Distance between the back of the head and the tip of

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the nose (Gürler and Kaymaz, 2011) (Fig. 3). CD: Largest measured diameter of the rib cage (Suguna et al., 2008) (Fig. 4). FHR: Foetal heartbeat multiplied by four after counting the image

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on the screen for 15 seconds (Martinez et al., 1998). THD: Transversal diameter of the heart

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measured at the diastolic stage and the four chamber view when the foetal body was immobile (Lee et al., 2005) (Fig. 5), OD: Largest measured diameter when the line between the

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hyperechoic orbit and the hypoechoic eyeball was considered as the border of the eye (Kähn, 1989) (Fig. 6). UCD: Averages of two measurements taken from the area of the umbilical cord entering the body and 1 cm apart from the entrance when the foetus and the umbilical cord were

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visible at the same time on the ultrasonic screen (Lee et al., 2005) (Fig. 7). KD: Maximum measured diameter of the kidney that had an anechoic pelvis and was hypoechoically limited. The anatomical structure of the kidney was clearly evident (Gürler and Kaymaz, 2011; Fig. 8).

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For progesterone concentration evaluation, the blood samples were collected daily between Days 15 and 24 of gestation and weekly from Day 27 until the end of the study. The serum progesterone concentrations were measured using an ELISA kit (EIA-1561, DRG, Marburg, Germany; Salem et al., 2011).

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2.3. Statistical analysis The Shapiro-Wilk test was performed to assess the normal distribution of the data while

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comparing the embryonic and foetal developmental variables of the singleton and twin

pregnancies. Student’s t-test was used for the normally distributed data and the Mann-Whitney U test was used for the non-normally distributed data. The model that best represented the data

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was used for development of linear (y = a + bx) or quadratic (y = a + bx + cx2) regression

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models to estimate the relationship between the gestational age and the foetal measurements (y

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= dependent variable; a, b, and c = variables; x = gestational age, and x2 = the square of the

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gestational age).

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The Mann-Whitney U test was used to compare the mean serum P4 values between the singletons and twin pregnancies and to determine the days these values were different. The

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Friedman test was used to determine whether there was a difference between the days in terms

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of serum P4 concentrations, and the Nemenyi test was used to determine the days that contributed to the variation when a significant difference was detected by using the Friedman

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test.

The Mann-Whitney U test was used to determine whether there were any differences in

birth weights between the singletons and twin kids. To determine the relationship between the P4 concentrations and birth weights, the average of the P4 values measured for each dam during pregnancy was calculated and the Spearman test was applied. The results were considered significant if P < 0.05.

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3. Results The embryonic vesicle that was considered to be the first pregnancy finding was observed in 2, 5, 12, and all 14 animals on Days 15, 18, 21, and 24 of gestation, respectively. Embryonic measurements were initiated on Day 21 of gestation. Abortions, however, occurred in four animals on Days 58, 65, 74, and 86 of pregnancy and in three animals on Day 79 of

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pregnancy. The measurements, therefore, were continued for the remaining seven goats that managed to give birth to healthy kids. Four singletons and three twin pregnancies were

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determined, and the embryonic and foetal structures of ten foetuses were measured. The first measurement was EVC on Day 21 of gestation, while the last measurements were THD, OD,

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KD, and FHR on Day 128 of gestation, the study’s final day.

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3.1. Embryonic and foetal measurements

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There were no significant differences between the singleton and twin pregnancies for

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any of the embryonic and foetal variables (P > 0.05), so the measurements of ten foetuses were

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used to form the regression curves and GA equations. The measurements of EVD, CRL, and AVD were taken three to four times. The

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correlation of these variables with GA, however, could not be established due to insufficient

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data. The values for OPD, BPD, ONL, CD, FHR, THD, OD, UCD, and KD were highly correlated with those for gestational age (P < 0.0001). The OPD was measured between Day 30 and Day 121 of gestation. The normal

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formation of the placentomes was distorted due to the pressure of the growing foetus during the later periods of gestation. The equation between the OPD and GA was developed based on a quadratic regression curve (Table 1, Fig. 9).

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The BPD, ONL, and CD were measured starting from Day 37 of gestation. The linear regression model was developed for the BPD and ONL measurement data, while the quadratic model was used for the CD measurement data (Table 1, Fig. 9). The heartbeat was first detected on Day 27 of gestation, but the FHR could only be detected on and subsequent to Day 37 of gestation. This might be due to the size (too small)

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and the speed of heart contractions that were too rapid to be measured on Day 27 and Day 30 of gestation. The THD was measured starting on Day 44 of gestation, which was after the

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boundaries of the heart were distinguishable. The equations that best fit both variables were the quadratic regression curves (Table 1, Fig. 9).

The diameters of the orbit, umbilical cord, and kidney were measured starting on Days

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44, 51, and 93 of gestation, respectively. The equations between these three variables and GA

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3.2. Serum progesterone concentrations

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were developed considering the linear regression curves (Table 1, Fig. 10).

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The maternal serum P4 concentrations of the 14 goats that were confirmed to be pregnant

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by ultrasonography changed from 13.39 ± 1.18 (SE) to 17.63 ± 1.88 ng/ml between Day 15 and 24 of gestation. The pregnant goats with twins had greater serum P4 concentrations than the

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goats with single foetuses (P < 0.001). There were differences at various times during the

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pregnancies in serum P4 concentrations between singleton and twin pregnancies on Days 51, 107, 114, and 128 of gestation (P < 0.05). The P4 concentrations were different with the singleton pregnancies between Day 44

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and Day 58, Day 51 and Day 58, Day 51 and Day 100, and Day 58 and Day 121 of gestation, whereas there were differences with the twin pregnancies between Day 44 and Day 107, Day 44 and Day 114, Day 58 and Day 74, and Day 58 and Day 121 of gestation (P < 0.05). The greatest mean and greatest median values for the P4 concentrations were observed on Day 100 of gestation with the singleton pregnancies, and these values were determined as

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17.94 ± 2.45 ng/ml and 18 ng/ml, respectively. The same variables for the twin births were observed on Day 114 of gestation as 24.87 ± 4.69 ng/ml and 23.33 ng/ml, respectively. The least mean and median values were 8.83 ± 0.61ng/ml and 8.82 ng/ml on Day 51 and Day 44 of gestation with the singleton pregnancies, respectively, and 12.88 ± 1.11 ng/ml and 11.84 ng/ml on Day 51 of gestation with the twin pregnancies, respectively (Fig. 11).

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The mean and median of the birth weights of the singletons were 4.09 ± 0.05 kg and 4.09 kg, respectively. The mean and median of the individual births weights of the twins were

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3.35 ± 0.09 kg and 3.34 kg, respectively. With the twin births, the mean and median values of the total birth weights of two kids were 6.7 ± 0.21 and 6.9 kg., respectively. The birth weights

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of the singleton kids were greater than the individual birth weights of the twins (P < 0.05).

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There was a negative correlation between the P4 concentration and the birth weights of

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kids when the birth weights of the twins were calculated individually (r =-0.78; P = 0.007), and

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the correlation was not significant when the birth weights of the twins were calculated together (r = 0.393; P = 0.383).

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4. Discussion

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According to the results of this study, the gestational age can be estimated in Turkish Saanen goats using ultrasonographic measurements of the OPD, BPD, ONL, CD, FHR, THR,

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OD, UCD, and KD variables. To the best of our knowledge, this study is the first to provide information on the relationship between the gestational age and these foetal variables in Turkish

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Saanen goats.

The first detection days of the embryonic vesicle (EV) were reported to be on Day 14

of gestation in Egyptian native goats using a 7 MHz intra-rectal human prostate vector probe (Karen et al., 2009); Dwarf goats using a 3.5 MHz abdominal probe (Sayuti et al., 2016); Days 17-22 of gestation in Boer goats using a 7.5 MHz linear-array probe (Padilla-Rivas et al., 2005); Days 17-34 in Jamunapari goats using a 5 MHz linear array probe (Singh et al., 2004); Day 18

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in Anglo-Nubian goats using a 5 MHz linear-array probe (Martinez et al., 1998); and Day 20 in Beetal goats using a 7.5 MHz linear-array probe (Kailash et al., 2015a). In the present study, the embryonic vesicles were detected in two animals on Day 15 of gestation with a 6.5 MHz human prostate probe. This finding is consistent with those of the aforementioned researchers except for Martinez et al. (1998) and Kailash et al. (2015). Thus, the difference may be due to

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the type of probe used and breed differences.

There were no significant differences in any of the embryonic and foetal measurements

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between the singleton and twin pregnancies in the present study. The finding in present study is consistent with those in previous studies with ewes (González de Bulnes et al., 1998; Jones

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et al., 2017) and goats (Martinez et al., 1998). In addition, studies of pregnancies in abattoirs

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indicated that there were few differences between the measurements of singleton and twin

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foetuses and these differences can only be detected in the latter stages of pregnancy (Robinson

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et al., 1977; McDonald et al., 1978).

With previous studies, there were reports that in goats, foetal age is highly correlated

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with the EVD (González de Bulnes et al., 1998) and CRL (Martinez et al., 1998; Abdelghafar et al., 2007; Amer, 2008, 2010; Abdelghafar et al., 2011; Abubakar et al., 2016). Furthermore,

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from studies in abattoirs, there have been reports of a high correlation between gestational age

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and CRL (Chudasama et al. 2017). There has been no research examining the relationship between AVD and pregnancy age in small ruminants. In the present study, the correlation between foetal age and these three variables could not be evaluated due to insufficient data. In

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addition to the probe and breed differences, the examination frequency may have affected the amount of the obtained data and different results may have been obtained between the studies as a consequence. The outer diameter of the placentome was first measured on Day 30 of gestation. Similar findings in goats were reported by Doize et al. (1997) and Karen et al. (2009). In addition, the

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OPD was correlated with foetal age and this finding was consistent with those of other studies (Doize et al., 1997; Lee et al., 2005; Suguna et al., 2008; Karen et al., 2009; Nwaogu et al., 2010). In the present study, the BPD was first measured on Day 37 of gestation. Accordingly, the BPD could be measured starting at Days 36 to 42 of gestation in different studies (Reichle

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and Haibel, 1991; Amer, 2008; Abubakar, 2016; Karadaev et al., 2016). The BPD was highly correlated with the foetal age in the present study, similar to the findings in other studies

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(Reichle and Haibel, 1991; Lee et al., 2005; Amer, 2008; Karen et al., 2009; Nwaogu et al., 2010; Abdelghafar et al., 2011; Abubakar, 2016).

Previous studies indicated that the ONL could be measured starting from Days 36 to 38

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of gestation in ewes (González de Bulneset al., 1998; Gürler and Kaymaz, 2011) and from the

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sixth week in goats (Kandiel et al., 2015). In the present study, the ONL could be measured

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starting on Day 37 of gestation. This finding was similar to those in studies with ewes but detection was earlier in goats. The correlations between the ONL and gestational age were high,

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which was consistent with previous studies of sheep (González de Bulneset al., 1998; Gürler and Kaymaz, 2011) and goats (Nwaogu et al., 2010; Kandiel et al. 2015).

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In the present study, the first measurement day of the CD was on Day 37 of gestation.

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In goats, the earliest detection days of CD were on Day 23 of gestation by González de Bulnes et al. (1998), Day 42 of gestation by Kandiel et al. (2015), and Day 63 of gestation by Suguna et al. (2008). There was also a high correlation between the CD and the gestational age which

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is consistent with findings in these previous studies. Although the foetal heartbeat was first detected on Day 27 of gestation for the first time

in the present study, the rate of heart contractions could not be determined until Day 37 of gestation. Similarly, in many studies the heart is too small and the heart rate is too rapid for determining the rate of heart contractions during the early periods of gestation (Martinez et al.,

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1998; Suguna et al., 2008; Karen et al., 2009; Raja Ili Airina et al., 2011). In previous findings, the earliest days for determination of FHR varied from Day 21 to 50 of pregnancy (Suguna et al., 2008; Raja Ili Airina et al., 2011). Using different methods to determine the procedures for FHR (M-mode, B-M mode, and Doppler ultrasonography) may have contributed to these differences in findings. In the present study, the number of heart contractions decreased as the

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gestational age progressed. Similar results were reported by Suguna at al. (2008) and Karen et

al. (2009). In the present study, there was a high correlation (r = 0.98P < 0.0001) between the

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FHR and gestational age while Karen et al. (2009) reported a low correlation between values for these variables.

The boundary of the heart could be clearly observed beginning on Day 44 of gestation

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and the FHD could be measured on this day in the present study. The finding in the present

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study is similar to that of Kandiel et al. (2015) but earlier than that of Raja Ili Airina et al. (2011)

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who measured the FHD on Day 42 and 50 of gestation, respectively. In addition, there was a

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high correlation between values for the THD and gestational age and this is consistent with the

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findings in previous studies (Lee et al., 2005; Kandiel et al., 2015). The diameter of the orbit could be measured starting on Day 44 of gestation and could

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be determined until the end of the study. Similarly, Kandiel et al. (2015) and Karadaev et al. (2016) were able to measure the OD on Day 42 and 49 of gestation, respectively. Furthermore,

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Lee et al. (2005), Nwaogu et al. (2010), and Kandiel et al. (2015) reported a high correlation between the values for OD and gestational age. The results of the current study were consistent

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with the findings of these previous studies. The UCD was measured starting on Day 51 of gestation. This finding was similar to the

finding of Abdelghafar et al. (2011). Karen et al. (2009) measured the UCD on Day 30 of gestation using a 7 MHz human prostate vector probe. The values for UCD were highly correlated with gestational age in the present study, which was consistent with the results of

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Karen et al. (2009), Abdelghafar et al. (2011), and Kailash et al. (2015). Lee et al. (2005) and Nwaogu et al. (2010), however, reported a lesser correlation between the UCD and gestational age than that determined in the present study. Differences in animal breeds might be the reason for the variations in findings among the studies. In the present study, the KD was measured beginning on Day 93 of gestation. The first

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KD measurement day was reported on Day 60 (Léga et al., 2007) and 76 of gestation (Kailash

et al., 2015b) in goats and on Day 50 (González de Bulnes et al., 1998) and 70 (Da Silva et al.,

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2018) of gestation in ewes. These findings on the KD were earlier than those in the present study. The correlation between the KD and gestational age was high, which was similar to the

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findings of González de Bulnes et al. (1998), Léga et al. (2007), and Kailash et al. (2015).

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The serum P4 concentrations varied from 13.39 ± 4.42 ng/ml to 17.63 ± 7.06 ng/ml

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between Day 15 and 24 of gestation in the present study. Zamfirescu et al. (2011) reported that

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the maternal serum P4 concentrations varied between 12.18 and 13.33 ng/ml between Day 14 and Day 25 of gestation in goats. The determination method of P4 (ELISA-RIA), breed

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differences, suckling-milking, and physiological factors might be the reason for the variations (Thorburn and Schneider, 1972; Gaafar et al., 2005).

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In pregnant animals, although the number of corpora lutea (CL) is not always related to

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the litter size (Jarrel and Dziuk, 1991), it was reported that the P4 concentration was greater in twins generally due to the increase in the number of CL with the number of foetuses (Ranilla et al., 1997; Manalu and Sumaryadi, 1998; Haldar et al., 2013). Apart from this, with the increase

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in the number of foetuses, the placental mass increases and more placental P4 is secreted from the glands (Manalu et al., 1996). Cengiz et al. (2014) reported that there was not a correlation between the values for P4 concentrations and litter size until Day 30 of gestation in Turkish Saanen goats. There are also studies indicating that there is a low correlation between the litter size and serum P4 concentration, and there are large individual differences in the P4

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concentrations among goats (Mukasa-Mugerwa and Viviani, 1992; Salah, 1994; Khanum et al., 2001). In the present study, there was a difference between the singletons and twins in terms of the serum P4 values throughout pregnancy. The difference between the single and twin births was first observed on Day 51 of gestation. It was also determined that the concentration of P4 was greater in twins than in singletons, consistent with reports from earlier studies of goats and

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ewes (Buttler et al., 1981; Manalu et al., 1996; Manalu and Sumaryadi, 1998; Haldar et al.,

2013). The thought is as the number of kids increases, the concentration of P4, which is known

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to have a role in the development of the mammary glands, also increases so the kids have an

adequate nutrient intake from the milk of the dam after birth. The difference in the P4 concentrations among the single and twin births, therefore, is greater, especially in the last

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months of pregnancy when the development of the mammary gland increases (Buttler et al.,

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1981; Manalu et al., 1996). In the present study, although it was not observed in the last month,

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it was determined that the difference between the twin births and the single births in terms of

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the serum P4 concentrations increased, especially toward the last period of pregnancy (Days

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107, 114, and 128).

The P4 values that were measured during pregnancy in the present study were similar to

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those reported by Gaafar et al. (2005), lesser than those reported by Alwan et al. (2010), and greater than those reported by Kornalijnslijper et al. (1997) and Yahi et al. (2017). These

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differences may be due to breed and individual physiological variations, feeding, season, suckling-milking, and the P4 measurement methods (Thorburn and Schneider, 1972; Mukasa-

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Mugerwa and Viviani, 1992; Gaafar et al., 2005; Marai et al., 2006; Alwan et al., 2010; Pehlivan et al., 2017; Lemley et al., 2018). It was reported that litter size affects the birth weight in goats and ewes (Khanum et al., 2001; Juengel et al., 2018) and singletons have a greater birth weight than twins and triplets (Khanum et al., 2001). Likewise, there was a greater birth weight of singleton kids Savaş (2009)

16

in Turkish Saanen goats. In the present study, the birth weights of the singletons were greater than the twin births which was similar to reports in previous studies. There was a high correlation in a previous study between values for serum P4 concentrations and values for birth weights of the kids (Basset and Thorburn; 1973), while there was a low correlation reported by Mukasa-Mugerna and Vivani (1992). Manalu and Sumaryadi

IP T

(1998) concluded that as the mean birth weights of lambs decreased maternal serum P4 concentrations increased. Similar to Basset and Thorburn (1973) and Manalu and Sumaryadi

SC R

(1998), there was a negative correlation between the values for birth weights of the kids and the maternal serum P4 concentrations in the present study. 5. Conclusions

U

In the present study, gestational age could be estimated using transrectal and

N

transabdominal ultrasonography in Turkish Saanen goats by measuring the embryonic and

A

foetal structures. The results of the present study suggest that the use of the BPD, ONL, and PD

M

measurements are more suitable for the early stages of gestation, while the OD and KD

ED

measurements are preferable in the later stages of gestation. It is also recommended that measuring the maternal serum progesterone concentrations during pregnancy can be used to

PT

determine the litter size in Turkish Saanen goats. Conflicts of interest

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We confirm that the manuscript has been read and approved by all of the named authors

and that there are no others who satisfied the criteria for authorship but are not listed. We further

A

confirm that the order of the authors listed in the manuscript was approved by all. Acknowledgements This study was supported by the Afyon Kocatepe University Scientific Research Projects Coordination Unit (Project number 11.SAĞ.BİL.04) and summarised in the PhD thesis

17

“Monitoring of Embryonic and Foetal Development by Transrectal and Transabdominal Ultrasonography in Turkish Saanen Goats.”

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Alwan, A.F., Amin, F.A.M., Ibrahim, N.S., 2010. Blood progesterone and estrogen hormones

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Fig. 1. Outer placentome diameter. 1: Placentomes. 2: Foetal fluid

Fig. 2. Biparietal diameter. 1: Parietal bones. 2: Falx cerebri. 3: Orbit

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27

Fig. 3. Occipito-nasal length. 1: Orbit. 2:

Fig. 4. Chest diameter. 1: Ribs. 2: Heart

M

A

N

U

SC R

Cerebral hemisphere. 3: Placentome

Fig. 6. Orbit diameter. 1: Orbit. 2: Cerebral hemispheres. 3: Parietal bones

CC E

PT

ED

Fig. 5. Transversal heart diameter. 1: Heart

A

Fig. 7. Umbilical cord diameter. 1: Umbilical Fig. 8. Kidney diameter. 1: Kidney. cord. 2: Foetus. 3: Placentome

Table 1

28

Regression equations and correlation coefficients (R) of the foetal measurements and gestational age of the Turkish Saanen goats Foetal measurements

Equation

Regression Equation

Interval

r

(days) Quadratic

y = -18.918+0.899x-0.004x2

Biparietal Diameter (BPD)

Linear

y = -9.68+0.463x

Occipito-Nasal Length

Linear

y = -30+1.07x

Chest Diameter (CD)

Quadratic

y = -26.337+1.125x-0.004x2

Foetal Heart Rate (FHR)

Quadratic

y = 223.409+0.452x-0.007x2

Transversal Heart Diameter

Quadratic

y = -4.47+0.127x+0.001x2

Outer Placentome Diameter

0.99

IP T

(OPD)

30-121

0.99

37-74

0.99

37-86

0.99

37-128

0.98

44-128

0.99

y = -5.488+0.218x

44-128

0.99

A

N

U

(ONL)

SC R

37-107

M

(THD) Linear

Umbilical Cord Diameter

Linear

y = -3.018+0.131x

51-121

0.98

Linear

y = -13.964+0.364x

93-128

0.98

(UCD)

PT

Kidney Diameter (KD)

ED

Orbit Diameter (OD)

A

CC E

Note: y = foetal measurement (mm), x = gestational age (day)

29

-12.218+0.525*X

45 40

35

35

BPD (mm)

40 30 25 20 15

30 25 20 15

121

37 44 51 58 65 74 79 86 93 100 107

Day

55

Day

-26.337+1.125*X-0.004X*X 50 45

45

40

35 30 25

35 30 25 20

U

CD (mm)

40

15

15

10

N

20

5

10

0

44

51

58

65

74

ED

223.409+0.452*X-0.007*X*X

250

100

CC E

50

PT

200 150

M

Day

300

37 44 51 58 65 74 79 86 93 100 107 114 121 128

0

Day

37

A

37

44

51

58

65

74

79

86

Day

35

-4.47+0.127X+0.001*X*X

30 25 20 15 10 5 0 44 51 58 65 74 79 86 93 100 107 114 121 128

5

THD (mm)

ONL (mm)

SC R

-30+1.07*X

50

FHR (pm)

IP T

114

107

93

100

86

79

74

65

58

0

51

5

0

44

10

5

37

10

30

OPD (mm)

50

-18.918+0.899*X -0.004X*X

45

Day

A

Fig. 9. Relationship between the outer placentome diameter (OPD), biparietal diameter (BPD), occipito-nasal length (ONL), chest diameter (CD), foetal heart rate (FHR), transversal heart diameter (THD), and gestational age. ---- = maximum values and ― — ― = minimum values

30

16 -5.488+0.218*X

25

12

20

6

Day

35

25 20

121

114

U

KD (mm)

30

15

107

SC R

-13.964+0.364*X

40

IP T

Day

93

0

100

0

51

2

86

4

5

79

10

8

74

15

65

UCD (mm)

10

44 51 58 65 74 79 86 93 100 107 114 121 128

OD (mm)

-3.018+0.131*X

14

58

30

5 0 100

107

114

A

93

N

10

121

128

M

Day

Fig. 10. Relationship between the orbit diameter (OD), umbilical cord diameter (UCD),

ED

kidney diameter (KD), and gestational age. ---- = maximum values, ― — ― = minimum

A

CC E

PT

values

Singletons Twins

24 22 20 18 16 14 12 10 8 6 4 2 0 16

23

30

37

44

51

58

65

74

79

86

93

Pregnancy Day

IP T

Progesteron (ng/ml)

31

100 107 114 121 128

SC R

Fig. 11. Median values of the serum progesterone concentrations in pregnant Turkish Saanen

A

CC E

PT

ED

M

A

N

U

goats