Factors influencing Awassi lambs survivorship ... - Livestock Science

Livestock Science 199 (2017) 1–6

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Factors influencing Awassi lambs survivorship under fields conditions ⁎

Anas Abdelqader , Rabie Irshaid, Mohammad Jihad Tabbaa, Mohannad Abuajamieh, Hosam Titi, Abdur-Rahman Al-Fataftah

MARK

Department of Animal Production, School of Agriculture, The University of Jordan, Amman 11942, Jordan

A R T I C L E I N F O

A B S T R A C T

Keywords: Awassi Starvation Lamb mortality Sheep Survival analysis Infection

The objective of this study was to investigate the pre-weaning survival rates of Awassi lambs and identify the causes of death in extensive and semi-extensive production systems. The study was designed to collect data under field conditions. Data were recorded on 29,290 lambs born alive during lambing seasons from 2011 to 2015. Postmortem autopsy findings were collected from 5448 lambs died during the pre-weaning period. About 63.5% of losses occurred during the first 7 days of life. The overall pre-weaning mortality rates were 19.7% and 16.9% in the extensive and semi-extensive production systems, respectively. Lamb birth weight had a strong effect (P < 0.0001) on the pre-weaning mortality rate. The mean mortality rate in lambs weighed < 2 kg at birth was 45.1%. The proportion of autopsied lambs dying by category was starvation (28.6%), respiratory infections (19.2%), gastrointestinal infections (16.2%), birth injuries (10.2%), hypothermia (8.6%), enterotoxaemia (8.2%), dystocia (4.4%) and predation (2.1%). Explanatory variables best used by Weibull model to estimate the hazard ratio (HR) of lambs falling into a certain death category were production system, lamb sex, birth type, and lamb birth weight. Lambs born in extensive production system were more (P < 0.0001) likely to die from starvation (HR=4.6), gastrointestinal infections (HR=3.2), and hypothermia (HR=2.2), compared with semiextensive system. Lambs weighed < 2 kg at birth were more (P < 0.0001) likely to die from starvation (HR=5.5), hypothermia (HR=3.6), gastrointestinal infections (HR=2.4) and respiratory infections (HR=2.2), compared with lambs weighed 3–4 kg. Triplet lambs were 4.6 more (P < 0.0001) likely to die from hypothermia and 4.3 more (P < 0.0001) likely to die from starvation. Survival rates of Awassi lambs can be improved by applying appropriate management practices that target intermediate birth weights and minimize the infectious diseases, starvation and cold stress.

1. Introduction High mortality rate in lambs is a worldwide problem threats sustainable sheep farming. It can reach up to 40% of total lambs born (Binns et al., 2002) which represents a significant economic loss. Although many studies have been conducted to identify the key involved factors, results are heterogeneous and highly influenced by breed and production system (Sawalha et al., 2007; Dwyer et al., 2016). Awassi is a desert sheep breed that is well-adapted to poor range lands and arid environments. It is the most common breed in many Middle Eastern countries and the only local breed in Jordan (Galal et al., 2008). There are three systems for sheep production in Jordan; transhumant, sedentary and nomadic. The former two represent about 90% of sheep farming (Abu-Zanat et al., 2005). Transhumant is a sort of extensive systems where flocks are kept outdoor to exploit the native vegetation in the desert from late summer to winter. During late winter and spring flocks are moved to barley cultivated rangelands. The sedentary is a sort

⁎

of semi-extensive systems where flocks are housed in barns, fed the barley grains and wheat bran during the year. Animals graze the vegetation around the farm during the day and return to the barns at night. Lamb mortality is a great problem faces sheep farming in Jordan (Abdelqader, 2013). Nevertheless, the real causes of mortality in these systems under field conditions have not been investigated. Lamb mortality studies are usually conducted on-farm under controlled conditions or based on records analyses (Binns et al., 2002; Sawalha et al., 2007; Barazandeh et al., 2012; Binabaj et al., 2013). This study was designed to collect real data directly from the fields, where farmer do not keep records. Lamb mortality can be analyzed using binary or logistic regressions models (Fogarty, 1995; Southey et al., 2001) assuming that lambs die on day of birth or later are alike and contribute the same amount of information to the statistical model. However, sheep flocks are highly dynamic under filed conditions, i.e. animals can leave or enter the flock at any time. Consequently, modeling the

Corresponding author. E-mail address: [email protected] (A. Abdelqader).

http://dx.doi.org/10.1016/j.livsci.2017.03.007 Received 17 November 2016; Received in revised form 2 March 2017; Accepted 4 March 2017 1871-1413/ © 2017 Elsevier B.V. All rights reserved.


A. Abdelqader et al.

dium and then the perirenal area and its color is changed from creamypink to dark brown (Everett-Hincks and Duncan, 2008). Stomach and small intestine were opened and examined, absence of milk clots in the stomach or white substances in the intestine were the signs that indicated starvation. Lambs to be classified as dying from hypothermia (cold exposure), the following 3 conditions were required: the presence of an extreme cold weather (air temperature < 0.0 °C with wind-chill), evidence that the lamb was not starved and there were signs of cold injuries. The later included obvious yellow subcutaneous edema in extremities (distal limbs), ear and tail (Haughey, 1973; Holst, 2004; Radostits et al., 2006). These lambs must have breathed, catabolized fat and walked as indicators of viability (Refshauge et al., 2016). There may be a line of demarcation between normal and affected area (Radostits et al., 2006). Edema usually accompanied by varying degrees of fat catabolism. Some lambs showed cold injury signs and catabolized all of their brown fat while remaining of milk clots were detected in their stomach. These were considered as typical cases of insufficient milk intake (Everett-Hincks and Duncan, 2008). Therefore these lambs were assigned starvation as the primary cause of death. Clinical signs of dystocia were the presence of subcutaneous edema around the head, neck and shoulders, hypoxia and sub-cranial hemorrhage (EverettHincks and Duncan, 2008; Refshauge et al., 2016). Liver was examined for tears. In most cases, lambs had not catabolized perirenal and pericardial fats. For a lamb to be classified as dying from birth injury, the presence of abdominal hemorrhage accompanied with significant lesions was required. Lambs also had breathed and had catabolized perirenal and pericardial fats (Refshauge et al., 2016). Lambs were examined for congenital defects by checking for defects of the spine or legs and other congenital abnormalities such as cleft palate, imperforate anus, joint problems and skeletal defects (Everett-Hincks and Duncan, 2008). Predation was difficult to diagnose because it may be a secondary and another factor was a primary cause of death. Primary predation was assigned when the lamb was born normal and survived for some time but had signs of injury from a predator (Refshauge et al., 2016). Lambs bled heavily with acute wounds or loss of organs were assigned as predation. Diagnosis was confirmed by locating claws punctures on skin, skull or neck (Holst, 2004). If a lamb had no signs of starvation or injuries then it was examined for infections. No pathology test was done to identify causative microbes. Lambs died from respiratory infections, as with Sharp and Nettleton (2007) and Sargison (2008), were found to have a complex of the following clinical signs: lungs sinks in fluids, lesions in the upper respiratory tract, pleural hemorrhage, enlarged or solid lung, grey or purple lung color with many lesions. Lobular consolidation which indicated incomplete lungs expansion. Anterior lobe consolidation and fluid in bronchioles which indicates inhalation Pneumonia. Lung tissue showed a degree of reddening due to autolysis. Congestion which indicated possible acute pasteurellosis or viral infection. At this age, pasteurellosis is usually septicemic therefore miliary abscess formation were detected also. Lambs died from gastrointestinal infections were found to have many of the following clinical signs: diarrhea, blood-tinged fluid in the abdominal cavity, high collection of watery blood and fibrinous clots in the intestine, destruction of the intestinal epithelia, ulcerative intestinal mucosa, hemorrhagic enteritis, necrotic enteritis, localized area of necrosis and the intestinal mucosa is congested with dark red ulcers penetrating deeply into the serosa (Lewis, 2007; Sargison, 2008). Soft pulpy kidney accompanied with hemorrhagic or necrotic enteritis and attendant excess of sanguineous serous fluid in the abdominal cavity were the major findings required for positive diagnosis of enterotoxaemia caused by Clostridium perfringens type D (Lewis, 2007). To confirm the diagnosis, the “sea anemone” test was conducted as described by McFarlane (1965) and Lewis (2007). The kidney was incised transversely, extruded from its capsule and examined for autolysis. The kidney was held under a gentle stream of water by projecting onto the subcapsular cortex. A positive diagnosis of pulpy kidney was indicated when the parenchyma was washed away leaving a

mortality as a time-dependent variable would be better described by survival data analysis because it can use censored and uncensored records and retain information from animals that were culled before completing the study period (Abdelqader et al., 2012; van Pelt et al., 2016). In this study, we used survival analysis techniques that can account for the continuity of an event (e.g. mortality in this case) and allow estimating the hazard ratio of each death cause. The key concept was to provide field-relevant solutions to increase lamb survival rates. Therefore, the main goal of this study was to investigate survival rates and causes of mortality in Awassi lambs under filed conditions with the participation of farmers. 2. Materials and methods 2.1. Animals and study area A total of 140 flocks of Awassi sheep were selected through a stratified sampling method, and then enrolled in the study. The sample was balanced equally to cover the two major sheep production systems in Jordan; the extensive and the semi-extensive. Flocks were distributed over 7 governorates of Jordan (Namely: Amman, Zarqa, Mfraq, Madaba, Kark, Ajloun and Irbid). The geographical coordinates of the study area were between latitudes: 32°37ʹ N, longitudes: 35°46ʹ E and 30°48ʹ N, 36°46ʹ E. The study area is dominated by arid to semi-arid climate with hot summer (mean maximum air temperature: 35–41 °C) and cold winter (mean minimum air temperature: 2–12 °C). Most of lambs birth took place in December, January and February which are the coldest months of the year where ambient temperatures might drop several times below 0 °C. Before selecting the flocks, many visits were conducted to the governmental agriculture extensions to contact farmers. Farmers were included in the study upon their willingness. 2.2. Data collection Data were collected on 29,290 Awassi lambs born alive during the lambing seasons of years 2011–2015. Lambs and their mothers were ear-tagged and followed until weaning. Farmers used to wean their lambs on 60-day age. Data were collected on each lamb during the preweaning period. Eight trained enumerators were hired to collect information efficiently at field conditions. For the accurate precision of data recording under field conditions, an electronic identification and monitoring system (Agrident GmbH, Barsinghausen, Germany) was used in all selected flocks. The component of this system included electronic ear-tags for ewes and lambs identification, electronic handheld reader and recorder to collect and save information in short time with high accuracy, and software program to import data collected from fields. While enumerators were visiting the flocks on a daily basis during the lambing season to collect data on all lambs, the dead lambs were taken for autopsy. Lamb birth weight, birth type, sex of lamb, lambing date, mother number and any other information required for analysis were recorded. Data were sent frequently to the software for entry and routine validation. 2.3. Post-mortem examination protocol Farmers were asked to keep dead lambs to be autopsied by trained veterinarians. Postmortem examinations were conducted on a daily basis. Autopsy methods used for the diagnosis of deaths causes were according to the protocols described by many authors in lambs (Holst, 2004; Radostits et al., 2006; Everett-Hincks and Duncan, 2008; Sargison, 2008; Refshauge et al., 2016). A lambs death was categorized as “starvation” when the following 3 signs were observed: pericardial and perirenal brown fat has been completely catabolized, there were no milk clots in the stomach and there was no evidence of milk absorption in the lacteals of the small intestine. Fat surrounding the heart and kidneys were examined. Usually, fat is depleted first from the pericar2



frond-like cortical stroma. If no symptoms were detected or symptoms cannot be found using the post-mortem examination protocol, lambs were recorded as undiagnosed.

Table 1 Different factors affecting lambs pre-weaning mortality rate (Mean percentage for all flocks ± Standard Error). Effect

Number of lambs borne alive

Total number of lambs died

From birth to 7 days of age

From 8 to 60 days of age


Overall Production system Extensive Semiextensive Sex of lamb Male Female Type of birth Single Twins Triples Lamb birth weight (kg) 1– < 2 2– < 3 3– < 4 4–5

29,290

5448

11.8 ± 0.15

6.8 ± 0.32

18.6 ± 0.44

17,590 11,700

3465 1983

12.7 ± 0.25 10.4 ± 0.18

7.0 ± 0.26 6.5 ± 0.14

19.7 ± 0.53 16.9 ± 0.25

15,817 13,473

3070 2378

12.4 ± 0.16 11.7 ± 0.29

7.0 ± 0.16 5.9 ± 0.39

19.4 ± 0.36 17.7 ± 0.44

18,052 10,686 552

2870 2291 287

9.8 ± 0.31 13.8 ± 0.29 29.9 ± 0.33

6.1 ± 0.37 7.7 ± 0.52 22.1 ± 0.35

15.9 ± 0.34 21.4 ± 0.41 52.0 ± 0.37

5756 11,716 9932 1886

2594 1400 1012 442

34.5 ± 0.36 7.5 ± 0.43 8.0 ± 0.51 21.0 ± 0.18

10.5 ± 0.32 4.4 ± 0.34 2.2 ± 0.28 10.2 ± 0.38

45.1 ± 0.37 11.9 ± 0.42 10.2 ± 0.42 23.4 ± 0.34

2.4. Data analysis Data were analyzed with the SAS Version 9.1.3 (SAS, 2010). Mortality percentage was calculated by considering the flock as the experimental unit. Mean mortality rates within flocks under different categories were analyzed with one-way ANOVA implemented in the proc GLM procedure of SAS. Lamb mortality is a binary trait; meaning that the lambs are either coded 1 (alive) or 0 (dead). To investigate the influence of a specific reason on survival rate at a certain time lamb survival rate was analyzed by survival analyses model of SAS (SAS, 2010). The risk of death occurrence due to a certain reason at any time was estimated by the hazard ratios (HR) which assumed to follow a Weibull distribution. Weibull distribution does not assume a constant hazard rate and therefore has broader applications, hence, Weibull survival distribution was estimated for the probability of survival. The explanatory variables considered with fixed effects and influencing the lambs' mortality were classified as production system, lamb sex, birth type, and weight. To find out the best model, the importance of the explanatory variables was tested by using a likelihood ratio test for large samples. This test revealed effects that reached statistical significance. Under the proportional hazards model, the hazard function λ(t; xi zi) is the instantaneous death rate at time t of a particular animal i characterized by the set of explanatory variables, and can be written as the baseline hazard function multiplied by the exponential effect of the explanatory variables. The final proportional hazards model for death of a particular lamb at time (t) takes the form:

considered period due to reasons not related to mortality. To control the dynamic change in data, we considered the time interval from lambing to death or censoring as a dependent variable. 3. Results

λ(t; xi zi)=λ0(t) exp [Sh+Wi+Gk+TLm+Fn]

3.1. Mortality rates and patterns

where:

Average weaning age in the selected flocks was 60 ± 5 days. The overall pre-weaning mortality rate was 18.6% (Table 1). The mortality rate in lambs was considered high at early ages and declined as the lambs grew up. The total number of lambs died during the pre-weaning period was 5448; about 63.5% of them were lost during the first 7 days of life. The production system had a significant effect on mortality rate at early ages (Table 1), being higher (P < 0.0001) in extensive compared with semi-extensive. Awassi lambs were 1.22 more (P < 0.0001) likely to die in extensive system compared with semi-extensive system (Table 2). The death risk was higher during the first 7 days of life (HR=1.28, P < 0.0001). Male lambs showed higher (P < 0.0001) mortality rate and risks than female lambs, particularly during the first 7 days of life. Mortality rates attributable to the sex of lamb were not significant during the rest of the period (Table 2). Litter size affected mortality rate throughout the study period, being higher (P < 0.0001) in twins and triplets than in singles. Triplets lambs exhibited high (P < 0.0001) death risk compared with twins and singles (Table 2). Preweaning survival rate had a strong (P < 0.0001) relationship with lambs' birth weight. The results showed that small size lambs (1– < 2 kg birth weight) were more susceptible (HR=4.82, P < 0.0001) to die than lambs born with greater birth weights (3–4 kg). Lambs born with intermediate birth weights (3–4 kg) had the lowest (P < 0.0001) mean mortality rate and death risk compared with other weight categories throughout the study. Heavy birth weight (4–5 kg) was associated with high death risks (HR=3.052, P < 0.0001) at early ages (1–7 days of life), with no significant effect during the rest of the period (Table 2).

λ(t)=hazard function for the probability of death at time t. λ0(t)=Weibull baseline hazard function at time t. Sh=the effects of production system (fixed time-independent with 2 classes; h=extensive, semi-extensive). Wi=lamb birth weight (fixed time-independent with 4 classes of kg interval; i=1– < 2, 2– < 3, 3– < 4, 4–5). Gk=the effects of lamb sex (fixed time-independent with 2 classes; k=male, female). TLm=type of lambing (fixed time-independent with 3 classes; m=single, twin, triplet). Fn=flock effect (fixed time-independent with 140 classes; n=1, 2,.., 140). In order to determine the adequate temporal scale of survival data for a Weibull survival analysis, the Weibull hypothesis for baseline (h0) was tested for the age at failure (death or censoring) measured with days. The validity of applying a Weibull proportional hazard model was assessed from the plot of the Kaplan-Meier as a nonparametric estimation of the survival curve, with shape parameter ρ and scale parameter λ of the Weibull distribution. The result of this plot combination showed a straight line which confirms that the data followed the Weibull distribution. Considering that, a value of HR=1 indicates that the risk of death is equal in comparable groups, while HR > 1 indicates an increasing hazard of death and HR < 1 indicates a decreasing hazard. Strength of association-hazard ratios were calculated for lambs likely to die from the different causes like hypothermia, starvation, trauma (birth injury), dystocia, predation, congenital defects, respiratory infections, gastrointestinal infections, enterotoxaemia and others. During the pre-weaning period, lambs could enter or exit the flock at any time and could be removed from the flock within the

3.2. Causes of lamb mortality The different causes of lambs' death are presented in Table 3. The 3



Table 2 Hazard ratios (95% Wald confidence limits) for the explanatory variables of lambs pre-weaning survival rate under the Weibull model. Effect Production system Extensive vs. Semi-extensive Sex of lamb Male vs. female Type of birth Single vs. Twins Triples vs. Twins Lamb birth weight (kg) 1– < 2 vs. 3– < 4 2– < 3 vs. 3– < 4 4–5 vs. 3– < 4




1.28 (1.13–1.35)**

1.14 (0.98–1.18)**

1.22 (1.13–1.28)**

1.20 (1.18–1.31)**

1.05 (1.00–1.15)ns

1.12 (1.10–1.19)*

0.48 (0.33–0.73)** 3.97 (3.34–4.72)**

0.58 (0.41–0.86)** 2.67 (2.21–3.23)**

0.49 (0.35–0.74)** 3.42 (2.76–4.24)**

4.82 (3.55–6.56)** 1.09 (1.04–2.57)* 3.05 (2.67–3.48)**

2.26 (2.00–2.54)** 0.96 (0.45–0.98)ns 0.97 (0.65–1.25)ns

3.27 (2.87–3.72)** 1.00 (0.33–1.04)ns 2.70 (2.38–3.06)**

ns

Not significant. * Significant at P < 0.05. ** Significant at P < 0.0001.

had a great (P < 0.0001) influence on lamb survival rate. Lambs born with low birth weight (< 2 kg) were 5.5 more (P < 0.0001) likely to die from starvation and 3.6 more (P < 0.0001) likely to die from hypothermia when compared with lambs born with an intermediate birth weight (3–4 kg). In the same manner, small size lambs were at greater (P < 0.0001) risk of death from infections such as enterotoxaemia, respiratory diseases and gastrointestinal diseases than lambs born with an average birth weight (Table 4). Heavy lambs were at greater (P < 0.0001) risk of death from dystocia, trauma (birth injuries) and gastrointestinal infections than lambs born with an average birth weight (Table 4).

Table 3 Distribution of dead lambs into each cause of death category (Mean percentage for all flocks ± Standard Error) during the pre-weaning period. Mortality causes

Non-infectious Starvation Trauma (birth injury) Hypothermia (cold exposure) Dystocia Predation Congenital defects Infectious Respiratory infections Gastrointestinal infections Enterotoxaemia Undiagnosed

Total number of lambs died




1558 553

32.7 ± 0.12 12.8 ± 0.21

21.5 ± 0.37 5.6 ± 0.08

28.6 ± 0.43 10.2 ± 0.28

469

11.5 ± 0.11

3.6 ± 0.14

8.6 ± 0.21

242 117 14

6.2 ± 0.11 1.6 ± 0.34 0.26 ± 0.45

1.4 ± 0.37 3.1 ± 0.17 0.25 ± 0.22

4.4 ± 0.32 2.1 ± 0.28 0.26 ± 0.46

1044

15.6 ± 0.14

25.3 ± 0.17

19.2 ± 0.19

883

13.8 ± 0.24

20.5 ± 0.35

16.2 ± 0.43

446 122

3.8 ± 0.24 1.8 ± 0.37

15.9 ± 0.16 2.9 ± 0.11

8.2 ± 0.14 2.2 ± 0.18

4. Discussion The overall rate of lamb mortality found in this study was higher than that reported in previous studies (Sawalha et al., 2007; Chniter et al., 2011; Barazandeh et al., 2012; Binabaj et al., 2013). This could be due to the breed differences and the nature of the study. This study was conducted under field conditions that located in arid to semi-arid areas where most of the flocks were kept in outdoors. Most lambs were under high mortality risk from birth up to 7 days of age. A lamb which dies during this period may not provide a return on the investment. This definitely will lead to great economic losses which affect the economic sustainability of sheep production. The high mortality rate during the first 7 days of life was in agreement with previous reports (Nowak et al., 2000; Barazandeh et al., 2012). In the present study, the production systems, lambs sex, birth type and weight were the factors validated by Weibull model to be used as major explanatory valuables. These variables were also reported in many previous data on lambs' mortality (Sawalha et al., 2007; Hinch and Brien, 2014; Refshauge et al., 2016). The direct role of health, management and environmental factors on lamb mortality was obvious in this study. This emphasizes the potential for substantial improvement in lamb survival by improving management and health practices. Lambs born in extensive production system were suffering the extreme exposure to cold stress, wind-chill and wet weather. Flocks of extensive system were almost kept in outdoors without bedding or shelters. The negative impact of extensive production system on lambs' mortality emphasizes the effectiveness of providing shelter for lambs and parturient ewes during lambing season when compared with semi-extensive system. In addition, Awassi breed characterized by a light fleece with limited surface area covered with wool fibers due to a low density of wool follicles per unit of area (Sharafeldin, 1965). This would increase the death risk of Awassi neonates when exposed to windy cold weather. This would emphasis on the necessity of providing shelter for parturient ewes. The causes of lambs' mortality in this study were not independent of each other. For example, hypothermia with starvation, small body size at birth with starvation, and large litters with small body size at birth

proportions of autopsied lambs dying by category were starvation (28.6%), respiratory infections (19.2%), gastrointestinal infections (16.2%), birth injuries (10.2%), hypothermia (8.6%), enterotoxaemia (8.2%), dystocia (4.4%) and predation (2.1%). These causes were significantly high during the first 7 days of life (Table 3). 3.3. Survival analysis for the causes of mortality The lambs which maintained under extensive production system were at a greater (P < 0.0001) risk of dying from most mortality causes, compared with those maintained under semi-extensive production system (Table 4). Lambs born in extensive system were 3.2 more (P < 0.0001) likely to die from gastrointestinal infections compared with lambs born in semi-extensive production system (Table 4). In the same manner, lambs born in extensive system were 4.6 and 2.2 more (P < 0.0001) likely to die from starvation and hypothermia, respectively, compared with lambs born in semi-extensive systems. Predation represented a high (P < 0.0001) risk in extensive system than in semi-extensive system. Males were at greater (P < 0.0001) risk of death from trauma, dystocia, starvation and respiratory infections than females (Table 4). Lambs born from twin or triplets litters were under very high (P < 0.0001) risk to die from hypothermia, starvation, gastrointestinal infections and respiratory infections. Triplets were 4.6 as likely to die from hypothermia and 4.3 as likely to die from starvation compared with singles (P < 0.0001). Lambs birth weight 4



Table 4 Hazard ratios estimated from Weibull model for the different causes of lambs pre-weaning mortality under each explanatory variable†. Effect Production system Extensive Semi-extensive Sex of lamb Male Female Type of birth Single Twins Triplets Lamb birth weight (kg) 1– < 2 2– < 3 3– < 4 4–5

Starvation

Gastrointestinal infections

Respiratory infections

Enterotoxaemia

Trauma

Hypothermia

Dystocia

Predation

Congenital defects

4.6* 1.0

3.2* 1.0

1.2* 1.0

1.2* 1.0

1.0 1.0

2.2* 1.0

1.0 1.0

2.3* 1.0

1.0 1.0

2.4* 1.0

1.2* 1.0

1.7* 1.0

1.1 1.0

2.2* 1.0

1.4* 1.0

1.6* 1.0

1.0 1.0

1.0 1.0

1.0 3.1* 4.3*

1.0 1.2* 2.4*

1.0 1.3* 1.4*

1.0 1.1 1.3*

1.0 0.64 0.44*

1.0 2.2* 4.6*

1.0 1.0 0.68

1.0 1.4* 1.7*

1.0 1.0 1.0

5.5* 1.7 1.0 2.3

2.4* 1.0 1.0 1.6

2.2* 1.1 1.0 1.0

1.7 1.0 1.0 1.1

1.0 1.0 1.0 1.4

3.6* 1.7 1.0 0.82

1.0 1.0 1.1 2.1

1.0 1.0 1.0 1.0

1.0 1.0 1.0 1.0

† Hazard ratio was fixed to 1.0 as a reference level of the comparable group. * Significant at P < 0.0001 compared with the reference level of the comparable group

of gastrointestinal and respiratory infections. Along with the nutritional role of colostrum as a source of nutrient and energy, it provides immuneglobulins which improve the passive immunity. Sheep have epitheliochorial placenta where immunoglobulins do not cross the placental barrier. Consequently, improving survival rate is necessary to get the lambs' early access to the first meal of colostrum, which will provide the neonates with necessary immunoglobulin as well as energy. It is well recommended that the first meal to be taken from the udder which strengthen the mutual bonding between the mother and her young (Nowak et al., 2000). This would enhance the maternal behavior of the ewe to take care of her young (Dwyer et al., 2016). Therefore, the first hours postpartum are critical for both establishing the maternal bond and providing the first dose of immunoglobulin and energy. Lamb birth weight and mortality rate were associated in a curvilinear relationship. This was also confirmed in other studies (Sawalha et al., 2007; Barazandeh et al., 2012; Binabaj et al., 2013; Refshauge et al., 2016). Lambs with either extreme-low or extreme-high birth weight were under high death risks compared with intermediate birth weights. The small lambs (< 2 kg) were susceptible to starvation, weakness and cold exposure while the heavier (> 5 kg) were susceptible to dystocia, lambing difficulties and birth injuries (trauma). Dystocia was previously reported to cause mortality in lambs with the heaviest birth weights (Sawalha et al., 2007). Most of lambs suffered from dystocia were lost few days postpartum. Generally, the total lambs died from dystocia in this study were lower than that reported in the literature for other breeds of sheep (Sawalha et al., 2007; Refshauge et al., 2016). Lambs dying from dystocia were 2.1 more likely to be overweight at birth and 1.6 likely to be males than females. Males usually have higher birth weights than females. Therefore, the optimal birth weight, rather than maximum birth weight, should be the target for survival rate improvement. Type of birth had a significant effect on lambs' survival rate. Lambs born in large litters usually had low birth weights and these lambs were predisposed to starvation and lower energy reserves. These results were in agreement with other studies (Awemua et al., 1999; Sawalha et al., 2007). The triplets lambs were under very high death risk, mainly due to starvation and cold exposure. This might indicate that the primiparous ewes were more likely to exhibit poor mothering ability with insufficient milk production. Previous studies have confirmed that twins were often disadvantaged by lower birth weight, lower energy reserves and lower colostrum intake than singles (Hall et al., 1990; Nowak and Poindron, 2006). Along with the current findings, hormonal enhancement to increase twining rate should be avoided particularly in extensive system of Awassi sheep. The low survival rates of male lambs and the high hazard ratios of their death compared with the females

were closely associated. This agrees with previous studies (Hinch and Brien, 2014; Refshauge et al., 2016). However, survival analyses could estimate the hazard ratios of each factor. Starvation was among the principal causes of early lamb mortality. A lamb is born with a small reserve of energy, which in the course of its metabolism provides heat. When the lamb is losing heat to the environment at a rate faster than the body can produce it, hypothermia occurs. Directly after birth, young lamb is entirely dependent upon its mother for the provision of food. Therefore, lamb starvation is strictly related to management. As revealed by autopsy findings, about 28.6% of lambs died because they failed to get enough milk. In many cases, their stomachs were completely empty, particularly in neonates. Unless lambs receive colostrum within two or three hours of birth, body energy reserves become critically depleted. Colostrum is considered as the second major factor (after body energy reserve) that affect neonatal survival (Dwyer et al., 2016). Some of the farmers had a very good experience as they tipped each ewe at lambing, check her udder, and assist every lamb with its first meal. Starvation typically occurs during the first few days of life. Before death, it is easy to find that the stomach of starved lamb is empty upon palpation. Early recognition of starvation will reveal significant increase in survival rate. During periods of bad weather mortality occur due to hypoglycemia even body fat reserves still not totally depleted (Nowak and Poindron, 2006). Cold weather and small body size were strong predisposing factor for early mortality. Therefore, beside colostrum, lamb should be given glucose solution. Underweight lambs (< 2 kg) were under very high death risk because they were suffering from starvation. These lambs are usually too weak to stand and suck. As a result, small frequent feedings by a stomach tube may be necessary until the lamb gains enough strength. Heavier lambs (4–5 kg) were less exposed to hypothermia-starvation complex. This may be explained by the fact that large lambs have more body energy reserves. Large neonates have more brown fat per kilogram of body weight than smaller ones (Nowak and Poindron, 2006). Small lambs loss heat faster than larger lambs, as the former have higher body surface area to body mass ratio and therefore higher heat loss per unit of body weight (Dwyer et al., 2016). The small body size had a direct relation with the weakness of lamb and body energy reserves. The high death risk of lambs born with small body size (< 2 kg) can be explained by the fact that these lambs have limited energy reserve and need a quick supply of colostrum to maintain body temperature. About 20% of lambs in this study were born underweight (< 2 kg), and 45.1% of them were lost. This would shed lights on birth weight optimization through nutritional management of pregnant ewes. The effects of under-nourished ewes on lambs' birth weight were documented (Hinch and Brien, 2014). The underweight lambs were found in this study to suffer from the high risk

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Binns, S.H., Cox, I.J., Rizvi, S., Green, L.E., 2002. Risk factors for lamb mortality on UK sheep farms. Prev. Vet. Med. 52, 287–303. Chniter, M., Hammadi, M., Khorchani, T., Krit, R., Lahsoumi, B., Ben Sassi, M., Nowak, R., Ben Hamouda, M., 2011. Phenotypic and seasonal factors influence birth weight, growth rate and lamb mortality in D’man sheep maintained under intensive management in Tunisian oases. Small Rumin. Res. 99, 166–170. Dwyer, C.M., Conington, J., Corbiere, F., Holmøy, I.H., Muri, K., Nowak, R., Rooke, J., Vipond, J., Gautier, J.-M., 2016. Invited review: improving neonatal survival in small ruminants: science into practice. Animal 10 (3), 449–459. Everett-Hincks, J.M., Duncan, S.J., 2008. Lamb post-mortem protocol for use on farm: to diagnose primary cause of lamb death from birth to 3 days of age. Open Vet. Sci. J. 2 (1), 55–62. Fogarty, N.M., 1995. Genetic parameters for live weight, fat and muscle measurements, wool production and reproduction in sheep: a review. Anim. Breed. Abstr. 63, 101–143. Galal, S., Gursoyb, O., Shaat, I., 2008. Awassi sheep as a genetic resource and efforts for their genetic improvement—a review. Small Rumin. Res. 79, 99–108. Hall, D.G., Egan, A.R., Foot, J.Z., Parr, R.A., 1990. The effect of litter size on colostrum production in crossbred ewes. In: Proceedings Aust. Soc. Anim. Prod., vol. 18, pp. 240–243. Haughey, K.G., 1973. Cold injury in newborn lambs. Aust. Vet. J. 49, 554–563. Hinch, G.N., Brien, F., 2014. Lamb survival in Australian flocks: a review. Anim. Prod. Sci. 54 (6), 656–666. Holst, P.J., 2004. Lamb Autopsy: Notes on a Procedure for Determining Cause of Death. State of New South Wales, NSW Agriculture, Australia. Lewis, C.J., 2007. Clostridial diseases. In: Aitken, I.D. (Ed.), Diseases of Sheep, fourth ed. Blackwell Publishing, Edinburgh, pp. 156–167. Mandal, A., Prasad, H., Kumar, A., Roy, R., Sharma, N., 2007. Factors associated with lamb mortalities in Muzaffarnagari sheep. Small Rumin. Res. 71 (1), 273–279. McFarlane, D., 1965. Perinatal lamb losses. 1. An autopsy method for the investigation of perinatal losses. N.Z. Vet. J. 13, 116–135. Nowak, R., Poindron, P., 2006. From birth to colostrum: early steps leading to lamb survival. Reprod. Nutr. Dev. 46 (4), 431–446. Nowak, R., Porter, R.H., Lévy, F., Orgeur, P., Schaal, B., 2000. Role of mother-young interactions in the survival of offspring in domestic mammals. Rev. Reprod. 5 (3), 153–163. Cold Injury. In: Radostits, O.M., Gay, C.C., Hinchcliff, K.W., Constable, P.D. (Eds.), Veterinary Medicine: A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs and Goats, 10th ed. Elsevier Health Sciences, London, UK, pp. 1794–1795. Refshauge, G., Brien, F.D., Hinch, G.N., van de Ven, R., 2016. Neonatal lamb mortality: factors associated with the death of Australian lambs. Anim. Prod. Sci. 56 (4), 726–735. Sargison, N., 2008. Sheep Flock Health: A Planned Approach, first ed. Blackwell Publishing, Oxford, UK. SAS, 2010. Institute, Inc., SAS OnlineDoc® Version 9.1.3. Cary, NC, USA. Sawalha, R.M., Conington, J., Brotherstone, S., Villanueva, B., 2007. Analyses of lamb survival of Scottish Blackface sheep. Animal 1, 151–157. Sharafeldin, M.A., 1965. Wool characteristics of Iraqi Awassi sheep. J. Agric. Sci. 65, 223–225. Sharp, J.M., Nettleton, P.F., 2007. Acute respiratory virus infections. In: Aitken, I.D. (Ed.), Diseases of Sheep, fourth ed. Blackwell Publishing, Edinburgh, pp. 207–211. Southey, B.R., Rodriguez-Zas, S.L., Leymaster, K.A., 2001. Survival analysis of lamb mortality in a terminal sire composite population. J. Anim. Sci. 79 (9), 2298–2306. van Pelt, M.L., Ducrocq, V., de Jong, G., Calus, M.P.L., Veerkamp, R.F., 2016. Genetic changes of survival traits over the past 25 yr in Dutch dairy cattle. J. Dairy Sci. 99 (12), 9810–9819.

were in agreements with previous reports (Mandal et al., 2007; Sawalha et al., 2007; Barazandeh et al., 2012; Binabaj et al., 2013). The higher survival rate of female lambs might be attributed to not clearly identified sex-linked factors (Mandal et al., 2007). Predation was considerably low contributor to lambs’ mortality compared with other studies. 5. Conclusion Rates of mortality in Awassi lambs were considerably high under field conditions, particularly in extensive production system. The first few days after birth were very critical for the survival of lambs. Starvation, respiratory infections, gastrointestinal infections, birth injuries, hypothermia and enterotoxaemia were the major causes of mortality. To improve lambs survival rate under field conditions, it is required to get lambs with intermediate birth weights, provide shelters, avoid twining enhancement and ensure early colostrum feeding. Special care should be given for small lambs, particularly in cold days. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgment This research was funded by the Scientific Research Support Fund (SRSF); Jordan, Project no. Agr/1/03/2011. References Abdelqader, A., 2013. Factors associated with Awassi lambs mortality in two production systems in Jordan. The 64th EAAP Annual Meeting, Book of Abstracts. Wageningen Academic Publishers, Nantes, France, No. 19, p. 265. Abdelqader, A., Al Yacoub, A., Gauly, M., 2012. Factors influencing productive longevity of Awassi and Najdi ewes in intensive production systems at arid regions. Small Rumin. Res. 104, 37–44. Abu-Zanat, M.M.W., Miqdady, H.A., Tabba'a, M.J., 2005. Production systems of small ruminants in the middle Badia of Jordan. Dirasat Agric. Sci. 32, 205–214. Awemua, E.M., Nwakalora, L.N., Abubakar, B.Y., 1999. Environmental influences on preweaning mortality and reproductive performance of Red Sokoto does. Small Rumin. Res. 34, 161–165. Barazandeh, A., Moghbeli, S.M., Vatankhah, M., Hossein-Zadeh, N.G., 2012. Lamb survival analysis from birth to weaning in Iranian Kermani sheep. Trop. Anim. Health Prod. 44 (4), 929–934. Binabaj, F.B., Tahmoorespur, M., Aslaminejad, A.A., Vatankhah, M., 2013. The investigation of non-genetic factors affecting survival of Karakul lambs from birth to one year of age using linear and nonlinear models. Small Rumin. Res. 113 (1), 34–39.

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