1. Introduction
Perinatal mortality may be defined as death of the fetus or calf before, during or within 48 h after calving at full-term (>260 days) [
1]. Perinatal mortality is a major problem in successful management of dairy young stock [
2] and adversely affects milk production [
3], reproduction and maternal survival [
4].
Concerns have been raised both about high [
5] and increasing rates of perinatal mortality particularly in Holstein heifers [
6] and about ‘normalisation’ of these rates in modern dairy herds [
7]. Maternal, fetal, environmental and management factors influence perinatal mortality. Some of these risk factors are well documented; dystocia [
8,
9], primiparity [
10], age at first calving [
11], twinning [
12], foetal gender [
13] and gestation length [
14].
However, the reasons why some herds have more calf losses than others has received little attention in the literature; few studies have been conducted comparing herds with high and low loss rates, specifically in perinates. An investigation of risk factors for young calf mortality (1–90 days) between 60 Swedish herds with high and low loss rates found that inadequate calf serum alpha-tocopherol and beta-carotene concentrations, number of faecal pathogens and cases of diarrhoea were significantly more likely in high loss herds [
15]. A Danish study comparing 28 herds with high and low young calf mortality (2–55 days) found that sociological factors such as the farm manager’s belief in whether they could influence loss rates was critical to calf health outcomes [
16]. An Icelandic study of 70 farms found few differences in management practices (use of AI in heifers, better housing, concentrate feeding) between herds with high and low stillbirth rates [
17].
In American beef herds it has been reported that calving in confinement and high dystocia rates were significantly associated with high, compared to, low calf morbidity (birth to weaning) herds [
18]. In an earlier study on dairy farms in the UK comparing high and low calf mortality (0–24 h) in heifers’ calves, no differences were found in heifer measurements, body condition score, age at calving or calf size [
19]. However, on high loss farms calving management differed and more heifers were assisted at calving and had dystocia indicating a significant farmer effect.
These limited observations indicate a paucity of information on why perinatal bovine mortality differs between high and low loss herds. Hence, the objective of this study was to investigate the management factors associated with a low risk (LR) and a high risk (HR) of perinatal bovine mortality on commercial dairy farms using an observational study design.
4. Discussion
The overall results are discussed first followed by the comparison between the case and control herds. As expected almost all herds had Holstein-Friesian heifers but a surprisingly high proportion of herds also had other dairy or crossbreed heifers, mainly Jerseys. This reflects a recent change within some herds in the Irish dairy industry (
www.icbf.com) and internationally [
21] towards crossbreeding. This is primarily in response to the recent decline in dairy herd fertility [
22] as crossbred animals have superior reproductive performance. This change was also evident from the fact that in only 77% of the herds in 2012 were the heifers bred to Holstein-Friesian sires: the remainder were predominantly bred to either Aberdeen Angus (for calving ease) or Jersey sires (for calving ease, better milk solids and fertility). This trend was also apparent for the cows. It might be expected that with increased use of non-Holstein-Friesian genotypes bovine perinatal mortality may decline as dairy crossbred animals have been shown to have lower bovine perinatal mortality rates than Holstein-Friesians [
23,
24].
While heifers were fed grass silage pre-calving in all herds a relatively small proportion were offered supplementary feeds or straw. This may be because of the generally high BCS of the heifers pre-calving. Because of the association between trace element deficiencies, bovine perinatal mortality and calving problems, heifers were supplemented with trace elements (mainly by mineral powder) in the majority (90%) of herds. As with the heifers, all herds of cows were fed grass silage with only a relatively small proportion offered ration or straw. In all herds cows were supplemented with trace elements pre-calving, most commonly by mineral powder. Previous studies at this research centre have shown the benefits of this practice [
25] and it has been recommended to Irish farmers. Thus the majority of farmers were implementing best practice.
The most commonly used vaccines (leptospirosis and salmonellosis: 86% of herds) in heifers reflect the perceived importance of these pathogens in causing abortions and weak calves in Irish dairy herds. However, while salmonella spp. are one of the most commonly diagnosed causes of abortion in Irish cattle herds [
26], leptospira are detected much less frequently [
27]. In recent years, with widespread publicity in the Irish farming media about BVD [
28], the use of BVD vaccines has increased substantially from a low base [
29]. Similar trends were found in cow vaccinations. Thus the majority of farmers were implementing best practice. The majority (70%) of farms had at least one farm dog and foxes were present on the majority (90%) of farms. Both of these species are intermediate hosts for
Neospora caninum, a cause of perinatal calf mortality [
30,
31]. A small number of herds had a recent clinical history of neosporosis. However, the most common recent clinical problems relevant to bovine perinatal mortality in these herds were BVD (23% of herds) and salmonellosis (33%).
Traditionally tie-up stalls in the 1960s and individual calving pens from the 1970s to the 1990s were the norm on Irish dairy farms, in the latter case due to their dual use as isolation pens for suspected cases of brucellosis. However, in this study only half of all herds had individual calving pens with a large proportion using group pens, outdoor pads or combinations of both. This apparent move away from individual pens may reflect the large herd sizes in this study (on average approximately 160 cows compared to the national average of 40 dairy cows/herd) [
32], the eradication of brucellosis and attempts to save labour at a busy time of the year in these seasonally calving herds. In all study herds dedicated calving facilities were used. This contrasts with a recent Canadian study where such facilities were used in less than half of the herds surveyed [
33].
A surprisingly small proportion of farmers (33%) moved their pregnant animals to the calving unit at least 24 h pre-calving. This may have been due to limited calving accommodation following gradual herd expansion over years. This early move allows animals to adapt to their new environment, social group and diet. On a large proportion (43%) of farms pregnant animals were moved to the calving unit between 6 h and 24 h pre-calving reflecting the detection of impending signs of calving such as relaxation of the sacrosciatic ligaments and/or colostrum dripping from the teats. A smaller proportion (20%) of farmers moved pregnant animals to the calving unit on the point of calving which may reflect limited observation of animals pre-calving or limited calving facilities. This ‘just in time’ calving movement protocol has become popular in North America and has recently been shown to have no detrimental effects on calving performance and is preferable to moving animals during stage one of calving [
34].
The majority (73%) of farmers observed pregnant animals once they were in the calving unit for signs of impending calving every 4 h to 6 h. This is similar to the findings of a recent Canadian survey in dairy herds [
33]. Given that stage one of calving may last this long this is adequate to detect the onset of this stage of calving but as stage two of calving may be on average, 45–90 minutes, this interval may miss this stage of calving completely. However, once the foetal hooves were observed the majority (63%) of farmers assisted heifers between 1 and 2 hours later. Similarly, cows were generally (73% of herds) assisted between 1 and 2 hours after the onset of stage two. This indicates that farmers were cognisant of avoiding prolonged calving. These findings are in agreement with an earlier Irish survey which found that the majority of farmers intervened within 2 hours of the onset of calving [
35]. All farmers used a calving aid (‘calving jack’) and some used additional calving aids. Whilst such aids are common on Irish dairy farms [
35], their use is regulated in some dairy industries, e.g., in Scandinavia and in the Netherlands.
Resuscitation techniques were used on the majority (86%) of farms, a figure comparable with that on US dairies (81%) [
36]. The most common first-aid resuscitation techniques used (hypothermal stimulation, nasal stimulation and calf suspension) have been shown to induce a gasp reflex, improve blood acid-base balance and improve rectal temperature in newborn calves [
37,
38]. Control of milk fever was based on either providing mineral powder (composed of many macro and micro-nutrients including calcium, phosphorous and magnesium at concentrations designed to prevent hypocalcaemia) pre-calving or therapy of clinical cases reflecting the widespread use of mineral powder for prevention of other periparturient problems.
Most of the management factors investigated here did not differ between case and control herds. This finding is congruent with the results of recent surveys on perinatal calf mortality in German [
39] and in Icelandic herds [
17]. Herdowners of high risk herds were more likely to use Je or JexHF sires on cows. This may be due to an attempt to reduce difficult calvings and bovine perinatal mortality in HF animals by crossbreeding with an easy calving breed such as the Jersey [
40]. The lower BCS of heifers in the high risk herds may be a response to previous losses in heifers where over-conditioning was a contributory problem. Obesity in heifers is a risk factor for dystocia and calf loss [
41,
42]. However, the large ORs and wide CL95 for some of the BCS variables indicate that these outcomes could not be determined with confidence.
Both heifers and cows in HR herds tended to be more likely to be vaccinated against leptospirosis, reflecting the importance attributed to this pathogen in causing abortions and bovine perinatal mortality [
43] and probably also the results from laboratory confirmation of this pathogen causing abortions and perinatal mortality.
Pregnant animals were moved to the calving accommodation earlier on LR compared to HR farms. This may facilitate adaption to the new environment, diet and social hierarchy, particularly in heifers, where such stresses can negatively impact calving performance [
44]. The later transfer of pregnant animals to the calving unit in HR herds, during stage one of calving, is likely to lead to delay in the onset of stage two of calving, longer duration of stage two, more calving assistance, dystocia and stillbirths [
34]. The greater use of a combination of different calving unit types in HR herds compared to LR herds may suggest attempts over time to provide better calving accommodation by adding to the existing maternity units with different designs. The greater use of group calving units in the LR herds may allow pregnant animals to express their natural pre-calving behaviours more easily as such units simulate the natural environment of the cow at pasture. Group calving accommodation was more common on LR farms which may reflect less stress of isolation in individual calving pens and more normal social interaction pre-calving [
1]. There were no apparent differences between HR and LR farms in how calvings were supervised (observation intervals) or assisted (time to assist or use of calving aids). This is in contrast to an earlier study finding that the difference between a high and a low bovine perinatal mortality farm was the ability of the farm personnel to calve heifers successfully [
19]. HR herds were more likely to have two people managing calvings but some LR herds had up to four people managing calvings. No information was gathered on the experience of the staff who managed calvings, a factor which may have a more important bearing on the quality of calving management than the number of personnel. Poor calving and calving pen management was identified in a survey of 28 Canadian dairy farms as a possible contributory factor in poor calf welfare [
45].
Calves were more likely to be resuscitated using intranasal or hypothermal stimulation than no resuscitation in the HR herds. This may be due to ongoing calf losses in the HR herds. Both of the techniques listed, prodding a straw up the calf’s nostrils and pouring cold water in the ear or over the calf’s head, are commonly used revival practices on Irish farms [
46] known to stimulate the gasp reflex and ultimately to improve gas exchange in the immediate postparturient period [
37,
38].
No apparent changes in the genotypes present on these farms over time were detectable which is not surprising given the short time frame of the study. No changes were apparent either in the feeding management of the heifers or cows pre-calving over this period. This may reflect the generally optimal feeding management adopted by these farmers and the previous changes they had made to prevent problems at calving. For both heifers and cows there was an increase in the number of herds vaccinated against salmonellosis and IBR over the three years. In the former case the incidence of clinical disease tends to have annual cycles [
47] a peak of which may have occurred during these years which stimulated vaccination. In the case of IBR very few herds were vaccinated at the start of the study. However, in the intervening years greater publicity has been focused on this disease in the Irish farming media by both the pharmaceutical industry [
48] and by Animal Health Ireland, a national body which provides advice on animal health management (
http://www.animalhealthireland.ie/index.php). This probably influenced farmers to commence vaccination as no increase in clinical IBR was reported in these herds.
No changes in calving supervision, calving assistance, newborn calf care or milk fever control, were apparent over the three years. As these farmers appeared to generally implement best practice and these tended to be practices of habit and routine, changes were possibly unlikely to occur in this relatively short time frame.