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Introduction
Goat milk is an important food source worldwide due to its high nutritional value, as it provides high quality protein, fat, carbohydrates and vitamins. Goat milk production is a growing industry in many countries, therefore there is a need to assess the factors that affect milk production. It is known that milk yield and composition is affected by numerous non-infectious and infectious factors (e.g. genetic, physiological, nutritional, environmental, and animal management conditions, and goat health status during lactation or even during the previous pregnancy; Goetsch et al., 2011; Mellado and Garcia, 2014; Ibnelbachyr et al., 2015). Nevertheless, the effects of these factors are not well understood in some goat breeds.
Serrana goats are the most representative goat breed reared for dual purposes (i.e., milk and meat), with the prevailing ecotype Transmontano raised in Portuguese mountains. According to the pedigree book, adult Serrana females weigh 25 to 40 Kg, and measure, in average, 64 cm at the withers. An average body condition score of 3.2 for lactating females was reported by Lima et al. (2012). These authors also observed that body condition score in Serrana goats is negatively affected (p<0.05) by milk yield and parasitism, suggesting that metabolic energy balance and general health status of this rustic breed are important factors in these well-adapted goats to local environmental conditions.
Abortions, as well as assisted or non-assisted parturitions with stillbirths and fetal mummifications, are responsible for important reproductive and economic losses in goat herds. The etiology of abortion, when stillbirths at parturition are included and neonatal asphyxia is excluded, is wide-ranging and multifactorial, comprising single or multiple infectious and non-infectious (Menzies, 2011) causes, including toxic plants (Dantas et al., 2012; Santos dos Reis et al., 2016).
Normally, infectious causes of abortion, including stillbirths at parturition, are associated with specific enzootic or epizootic (outbreak) events. The major infectious agents reported in goats are Brucella melitensis, Chlamydia abortus, Campylobacter spp, Coxiella burnetii, Bluetongue, Neospora caninum, Toxoplasma gondii, Yersinia pseudotuberculosis, Listeria spp, and in some countries, Peste des petits ruminants virus and Border disease virus (Menzies, 2011; van den Brom et al., 2012; Ababneh et al., 2014; Lafi et al., 2014; Rosamilia et al., 2014; Rodolakis and Laroucau, 2015; Anastácio et al., 2013; Bauer et al., 2016; Gazzonisa et al., 2016; Kardjadj et al., 2016). Due to the potential multifactorial etiology, a definitive diagnosis can be difficult and expensive to obtain. Moreover, clinical signs of abortion may not be specific regarding etiology.
On other hand, dystocia may lead to fetal death due to neonatal asphyxia (Probo et al., 2011), which cannot be accurately differentiated from other abnormal conditions without veterinary assistance or further diagnostic testing. To our knowledge, no studies have been conducted to evaluate these reproductive problems and their effect on subsequent milk production in Portuguese Serrana goats.
The aims of the present study were to evaluate the incidence of abortions and parturitions with stillbirths (APS) in Portuguese Serrana goats breed ecotype Transmontano and their association with milk production in the following lactation.
Materials and methods
Animal records
Animal records from 1997 to 2014 were obtained from the pedigree book (Genpro, Ruralbit, Portugal) of Serrana goats ecotype Transmontano, located at Trás-os-Montes e Alto Douro region (latitude 41º29′0´´ N and longitude 7°11′0´´ W; Mirandela City). Serrana goats ecotype Transmontano were historically used to graze mainly in the mountain zones of northern Portugal. In 2013, each farm raised on average 70 adult animals according to the pedigree book. Reproductive management included natural mating, in some herds with bucks separated from females. Two annual parturation peaks occured in January and October (Simões, 2016). Depending on each farm, lactating goats were hand-milked once or twice per day. Prophylatic practices included periodical deworming and vaccination against common bacterial diseases (i.e. enterotoxemia and brucellosis) and, more recently, paratuberculosis.
The farms were periodically visited by technicians of the agricultural association responsible for the pedigree book (Associação Nacional de Caprinicultores da Raça Serrana, ANCRAS) to record goat data. These records included adult individual identification, date and number of parturitions (parity), number of kids per parturition (prolificacy), and abnormal reproductive occurrences. Abnormal reproductive occurrences were defined as abortion, identified by farmers normally during the second half of pregnancy, and the presence of at least one stillborn or mummified fetus at the time of parturition. However, these anomalies were obtained from the pedigree records without distinction between them. The number of does and bucks were periodically reported by the farmer, and registered in the pedigree records.
Cumulative milk production (L) for each lactation was recorded by the technicians. The estimated 150-d normalized milk production (i.e. cumulative L produced in each lactation until 150 d), was also recorded in the pedigree records, and this estimation was determined from periodical measurement of milk at milking time according to ANCRAS guidelines.
The parturition dependent variable was classified as normal in the presence of parturitions without stillborn(s) or abortions, with a subsequent new lactation, or abnormal when parturition had at least one stillbirth, including mummified fetus and dystocia.
Parity was classified as primiparous or multiparous in females with a single parturition and two or more parturitions, respectively. Prolificacy of females in each parturition or abortion was classified as single (one fetus) and multiple (more than one fetus) according to the number of fetuses and denominated gemelarity.
Statistical analysis
Associations between the presence or absence of APS and the effect of year, month, parity and gemelarity variables, including all two-way interactions, were evaluated using a multivariable logistic regression analysis.
A Van der Waerden test was used for comparison of APS between parturitions of primiparous and multiparous goats or parturitions of goats with a single fetus and with multiple fetuses. This test was also used for comparison of 150-d normalized milk production between primiparous and multiparous groups with or without the above-described reproductive abnormalities.
Differences were considered significant at a p-value level of 0.05. All statistical analyses were performed with the JMP® statistical software of SAS, version 10 (SAS, Institute Inc. 2012; Cary, NC, USA).
Results
The overall incidence of APS between 1997 and 2014 was 8.7% (19,351/223,798; 95% confidence interval from 8.6 to 8.8%) for all parturitions. A higher incidence of APS was observed in parturitions of primiparous (12.9%; 6,919/53,838) compared with multiparous (7.3%; 12,432/169,960; p<0.001) goats. The incidence of APS was also higher in parturitions of a single fetus (14.0%; 18,414/131,222) than multiple fetuses (1.0%; 937/92,576; p<0.001).
According to the multiple logistic regression analysis, the incidence of APS was associated with year, month, parity and gemelarity (p<0.001), and their interactions (p<0.01), except for the interaction between gemelarity and parity (p = 0.08). Results are presented in Figures 1 and 2.
The 150-d normalized milk production was also lower in goats experiencing abnormal parturition with stillbirths or abortion compared to goats with normal parturition (Table 1).
Table 1 Comparison of the mean (± SEM) 150-d normalized milk production between primiparous and multiparous goats with or without abortion and/or stillbirth(s).
| Goat parturitions | Abortions and/or stillbirth(s) | At 150 d (L) | p-value |
|---|---|---|---|
| Primiparous | Yes (n = 4,797) No (n = 29,450) | 79.4 ± 0.5 90.8 ± 0.2 | p<0.001 |
| Multiparous | Yes (n = 8,715) No (n = 101,959) | 92.9 ± 0.4 98.8 ± 0.1 | p<0.001 |
Moreover, when only APS were considered with regards to offspring that did not make it to term, a lower 150-d normalized milk production was observed in females with multiple offspring (85.2 ± 1.5 L ± SEM; n = 604) compared to females with single offspring (93.4 ± 0.5 L; n = 8111; p<0.001). These differences were not significant for primiparous goats (multiple offspring: 77.5 ± 2.5 L; n = 120 vs single offspring: 79.5 ± 0.5 L; n = 4677; p>0.05).
Figure 1 Annual incidence of abortions and/or parturitions with stillbirths according to parturition type (single vs. multiple) and parity (primiparous vs multiparous goats; p<0.001).
Discussion
One of the major limitations of this study was the inability to differentiate goats with dystocia due to neonatal asphyxia (Sobiraj, 1994) or mummified fetuses at parturition from goats experiencing abortion. Moreover, misclassification of dystocia might have occurred if unobserved stillborn or mummified fetuses were classified as normal parturition. The second major limitation is the potential lack of agreement on APS classification used by the different technicians between 1997 and 2014. On the other hand, the fact that a new lactation occurred after an abortion was indicative of a late pregnancy phase, that was concomitant with the dry period in goats with at least one parturition in primiparous or multiparous goats.
Overall, the incidence of APS (8.7%) was higher than the normal values reported in the literature. The critical level of abortion incidence in small farms range from 2 to 5% (Menzies, 2011), and incidence of dystocia from 3 to 5% is considered normal in goats (Braun, 2007). However, because no distintion between the two occurrences was possible in our study, comparision with other reports should be interpreted with caution.
Interestingly, after 2009 the incidence of abortion increased in pregnancies with multiple fetuses as opposed to singletons for both primiparous and multiparous goats. Probably this increment was due to different criteria used by technicians throughout the years considered in the present study (1997-2014). However, abortion incidence was higher in nulliparous than in multiparous goats. In cows, the incidence of neonatal mortality was reported as approximately 4%, with a higher incidence in nulliparous than in multiparous cows (Mee et al., 2011). In the present study, it was not possible to address the etiology of APS (i.e. the distinction between infectious disease causes). This should be investigated in future studies. For example, the impact of caprine Chlamydiosis and Q fever, two diseases reported as important causes of APS in other countries (Menzies, 2011) should be further investigated. In order to control brucellosis in goats, the Trás-os-Montes e Alto Douro region has implemented a vaccination program using conjunctival vaccination with live B. melitensis Rev.1 strain (Olsen, 2013) for those counties with a herd- level prevalence greater than 2.5%. This prevention program may have changed the abortion rate due to the expected effect in the epidemiology of this bacterium among vaccinated flocks.
The Q fever has been reported in goats raised in Portugal (Anastácio et al., 2013), but a large herd screening of small ruminants is required in the northeast region, as has been conducted in dairy cattle (Pimenta et al., 2015). It is agreed that prophylactic measures, including active immunization against several infectious agents with reproductive impact other than B. melitensis (Lacasta et al., 2015) are needed in this region. Without significant epidemiological studies regarding the incidence and etiology of reproductive diseases and dystocia occurrence, it is difficult to advance a consistent explanation for the findings observed in the present study.
One other important question concerning the annual variation can be tentatively connected to climate change. In fact, the effect of climate change on reproductive events has been reported in sheep (Sejian et al., 2013). Marino et al. (2016) conducted an extensive literature review on climate change impact on the epidemiology of several diseases affecting the reproductive system of small ruminants. Climate has also been associated with decreased rates of fertility after artificial insemination in goats (Arrébola et al., 2016).
In our study, APS prevalence was higher in parturitions with singletons than parturitions with twins or more fetuses. This finding should be interpreted with caution. Firstly, the data were obtained over several years by different technicians, and recording of observations may have varied among technicians. Secondly, the recording of stillbirth and live fetuses may have been more easily noticed in the presence of singletons than multiple fetuses. In fact, a stillbirth can be omitted or undetected by farmers. Moreover, when abortion occurs in the dry period, a new lactation can be promoted by milking. Finally, there is seasonality to parturition in goats, and recording errors may be more common during the kidding season due to more intensive labor required by farmers or technicians. In fact, in October, during one of the main peaks of parturition (Simões, 2016), a low incidence of singleton abortion or stillbirth was observed in the present study. Moreover, a significant number of farmers also engage in other agricultural activities that require more intensity during this same season of the year and consequently less attention may be given to goats.
The 150-days normalized milk production observed in subsequent lactations was lower in the presence of APS than after normal parturitions (Table 1), and these findings are in agreement with those reported by Neves and Almendra (1996). This result emphasizes the adverse effect of APS occurrence upon subsequent lactation. Consequentely, APS should be reduced in order to minimize these situations.
In conclusion, the APS incidence reported in the present study seems to be higher for this species and was affected by year, month, parity, and gemelarity. These occurrences induced lower milk production. A more detailed study recording dystocia and abortion separately is warranted to distinguish the cause and factors affecting these two reproductive problems.
