Calving Management: A Questionnaire Survey of Veterinary Subject Matter Experts and Non-Experts

Simple Summary We designed a questionnaire and asked two groups of veterinarians: (1) subject matter experts, who had published on calving management and (2) veterinary practitioners) for their opinion about aspects of calving management. Participants recommended to differentiate between the two stages of parturition and emphasized signs of imminent parturition, such as “restlessness” and “visibility of fetal parts”. There was no consensus on the right time to move the cow to the maternity pen. Almost half of the respondents recommended a 6-h observation interval for prepartum cows in the maternity pen. The two veterinary groups differed little in their knowledge of calving management. Abstract Accurate detection of the onset of parturition is a key factor in the prevention of dystocia. In order to establish current best practice recommendations for calving management, we asked subject matter experts (SME) who had published on calving management (by online survey, n = 80) and non-SMEs, veterinary practitioners (by workshop survey, n = 24) for their opinions. For this, we designed a questionnaire on the significance of signs of imminent parturition (SIP), the frequency of calving observation, and influencing factors for the timing of cow movement to a maternity pen. The response rate was 67.5% in the online survey and 100% in the workshop survey. The majority (89.7%) of all respondents agreed that it is beneficial for successful calving management to differentiate between stage I and II of parturition. Of 12 signs of imminent parturition (for stage I and II), “restlessness” and “visibility of fetal parts in vulva” were cited by 56.5% and 73.3% of SME and non-SME respondents, respectively. There was no consensus on the right time to move the cow to the maternity pen; recommendations varied from one to over 21 days. Almost half of the respondents (45.7%) recommended a 6-h observation interval for prepartum cows in the maternity pen. This study identified a strong consensus on the SIP and how and when to observe cows prior to parturition. SMEs and non-SMEs provided broadly similar recommendations, while the SMEs and the non-SMEs differed significantly in the number of publications on calving they authored, they differed little in their knowledge of calving management.


Introduction
Between 2 and 10% of all calves are born dead or die in the next 48 h after birth [1]. To prevent stillbirth and consequences of dystocia and related diseases, experienced personnel is required to detect the onset of parturition [2,3]. Management of periparturient cows is a skill learned through education and experience. However, diverse recommendations are made both in the scientific literature and by veterinary practitioners, for example, for the   (Figure 2)) was conducted. Basically, the same criteria were applied for the Pubmed search, but additionally, publications that had already been shortlisted for the Pubmed search (n = 29) were excluded. Publications with a title that was off-topic (n = 215), published before 1998 (n = 15), published in a journal with an IF ≤ 1 (n = 1) and not peer-reviewed (n = 1) were excluded. In addition, corresponding authors who were cited multiple times in the reference list of the 5 selected publications (n = 36) and corresponding authors who are members of our working group (n = 3) were excluded. This supplementary search resulted in 19 additional corresponding authors that were included in the final survey. In total, 80 corresponding authors were invited to participate as subject matter experts (SMEs) in the field of calving management in the survey.
For the non-SMEs, 24 participants in a workshop on bovine perinatology organized by the Ontario Association of Bovine Practitioners (OABP) delivered by J.F. Mee and held in Guelph, Canada on 2nd May 2019 were surveyed as a convenience sample of large animal practitioners.

Administration of The Questionnaire
The same questionnaire was administered to the two veterinary groups; corresponding authors of peer-review papers on calving management [using the online survey software Unipark (https://www.unipark.com/), (online survey) (accessed on 10 July-26 September 2018)] and veterinary participants in a workshop on bovine perinatology [using a paper copy of the questionnaire (workshop survey)].
For the online survey, a cover letter outlining the objective of the research and assuring the participants that all registered data would remain anonymous along with a hyperlink to the questionnaire was sent via personal email addresses to the 80 corresponding authors. The survey was online from 10th July until 26th September 2018 (79 days). The average duration to survey completion time was 20 min. Participation in the survey was voluntary, but participants of the online survey were reminded three times via email. The first reminder was sent out after one week, the second after another week, and the last In total, 80 corresponding authors were invited to participate as subject matter experts (SMEs) in the field of calving management in the survey.
For the non-SMEs, 24 participants in a workshop on bovine perinatology organized by the Ontario Association of Bovine Practitioners (OABP) delivered by J.F. Mee and held in Guelph, Canada on 2nd May 2019 were surveyed as a convenience sample of large animal practitioners.

Administration of the Questionnaire
The same questionnaire was administered to the two veterinary groups; corresponding authors of peer-review papers on calving management [using the online survey software Unipark (https://www.unipark.com/), (online survey) (accessed on 10 July-26 September 2018)] and veterinary participants in a workshop on bovine perinatology [using a paper copy of the questionnaire (workshop survey)].
For the online survey, a cover letter outlining the objective of the research and assuring the participants that all registered data would remain anonymous along with a hyperlink to the questionnaire was sent via personal email addresses to the 80 corresponding authors. The survey was online from 10th July until 26th September 2018 (79 days). The average duration to survey completion time was 20 min. Participation in the survey was voluntary, but participants of the online survey were reminded three times via email. The first reminder was sent out after one week, the second after another week, and the last reminder with the hyperlink for participation after 3 weeks. For the workshop survey, the purpose of Animals 2021, 11, 3129 5 of 20 the questionnaire was explained to the participants of a workshop on bovine perinatology then it was distributed and collected before the workshop started.

Data Analysis
Data were entered into Microsoft Excel 2004 (Microsoft Corporation, Redmond, WA USA) and analyzed with descriptive statistics. The Likert scales were analyzed using the Mann-Whitney U-test to consider the strength of agreement and disagreement. Difference between responses of SME and non-SMEs were calculated using Fisher's exact test. The significance level was set at p < 0.05. Analyses were conducted using IBM SPSS Statistics for Windows (V. 26.0, IBM Deutschland GmbH, Ehningen, Germany).
In the following, only content with a statistical difference in the responses of SME and non-SMEs is mentioned. The responses that did not differ are not mentioned separately.

Response Rates
Of the 104 participants (80 SMEs and 24 non-SMEs) invited to fill in the questionnaire, 54 questionnaires of the online survey and 24 of the workshop survey were returned, with a response rate of 67.5% and 100%, respectively.
Of the 54 respondents in the online survey, 14 (25.9%) viewed the first page with the introduction of the survey; another 17 (31.5%) canceled the questionnaire early in the process, thus 23 SMEs completed all of the questions. While all workshop participants (non-SMEs = 24) finished the questionnaire, nine did not answer every question. In total, 38 out of 104 (36.5%) complete questionnaires were returned (28.8%-23/80 of the online survey; 62.5%-15/24 of the workshop survey). Incomplete questionnaires were included in the analysis; the data were adjusted to the respective number of participants per question.
Recommendations on the daily frequency of observations for signs of impending parturition were dependent on the proximity to parturition (Question 9, semi-open question, Figure 4). This question was answered by 24 SMEs and 24 non-SMEs. For cows that are not yet in the maternity pen, most respondents recommended observation intervals of twice a day (35.4%-8/24 SMEs; 9/24 non-SMEs) and every 6 h (31.3%-6/24 SMEs; 9/24 non-SMEs). Seven participants (14.6%-6/24 SMEs; 1/24 non-SMEs) commented that the observation interval strongly depends on the individual cow and its previous calving performance. The more SIP (signs of imminent parturition) observed the more frequent the number of recommended. As soon as the cow is in the maternity pen (Question 16, semiopen question), the recommended observation intervals were 6 h (45.7%-14/23 SMEs; 7/23 non-SMEs) and 2 h (26.1%-4/23 SMEs; 8/23 non-SMEs). Two participants (4.3%-2/23 SMEs; 0/23 non-SMEs) chose none of the options and stated that the observation interval depends on the individually observable signs of parturition. Answers of SMEs and non-SMEs did not differ significantly.

Observation Routine (Question 8-10, 16 and 17)
Recommendation by 24 SMEs and 24 non-SMEs on when [days pre expected calving date, (ECD)] to observe cows for signs of parturition and potential movement to the maternity pen ranged from more than 21 days to one day before ECD (Question 8, open question, Figure 3). Respondents recommended close observation at least 7 or 10 days (33.3%-7/24 SMEs; 9/24 non-SMEs) before ECD. SMEs and non-SMEs did not differ significantly in this regard. Recommendations on the daily frequency of observations for signs of impending parturition were dependent on the proximity to parturition (Question 9, semi-open question, Figure 4). This question was answered by 24 SMEs and 24 non-SMEs. For cows that are not yet in the maternity pen, most respondents recommended observation intervals of twice a day (35.4%-8/24 SMEs; 9/24 non-SMEs) and every 6 h (31.3%-6/24 SMEs; 9/24 non-SMEs). Seven participants (14.6%-6/24 SMEs; 1/24 non-SMEs) commented that the observation interval strongly depends on the individual cow and its previous calving performance. The more SIP (signs of imminent parturition) observed the more frequent the number of recommended. As soon as the cow is in the maternity pen (Question 16, semi-  A majority of study participants recommended moving cows to a maternity pen (81.3%-20/24 SMEs; 19/24 non-SMEs); the other 9 participants (18.8%-4/24 SMEs; 5/24 non-SMEs) disagreed with this practice (Question 10, closed question). The recommendations of SMEs and non-SMEs did not differ significantly.

Discussion
The overall response rate was high. But it needs to be disaggregated into the online and the workshop survey, complete and incomplete questionnaires, and question type. As expected, the response rate (of complete questionnaires) was higher in the workshop (62.5%) than in the online survey (28.8%). However, the login rate (i.e., the number of participants that started the questionnaire) in the online survey (67.5%) is comparable with other online surveys (e.g., 85% in [30]; 67.3% in [31]; 58% in [32]); the number of participants in the workshop that started the questionnaire was 100%. With online surveys, subscriber loss can occur because individuals cannot distinguish between a legitimate survey and a spam message, even if the emails come from a trusted organization [33]. Reminders to participate and the use of QR (Quick Response) codes were found to significantly increase response rates [34]. In our study, reminders indeed significantly raised the number of participants from the initial 14 (of which only 7 completed the questionnaire) up to 54 (of which only 23 completed the questionnaire).
The distinction between stages I and II of parturition has been determined to be helpful in calving management and is found to be especially important for defining the right time to move cows to the maternity pen. The first stage of parturition is defined in veterinary textbooks [35,36], (i.e., cervix starts opening, myometrial contractions start and the fetus adopts the final position within the birth canal). The duration of this stage is highly variable [37] and has been described from as little as 2 h [38] to 24 h [22] or even has been reported to last up to days [35]. Survey participants recommended for determining this stage, observation of "Restlessness" and "Tail raising", also "Relaxation of the pelvic ligaments" and "Vaginal discharge". This is in agreement with Wehrend et al. [39] who recorded "Restlessness" as the most frequently observed behavioral change when parturition was imminent. Berglund et al. [4] included "Restlessness" in their definition of stage I of parturition (i.e., the interval from restlessness until the allantochorion appears). The same time of stage 1 is very flexible, the time when "Restlessness" is observed before parturition varies as well. Huzzey et al. [40] reported a rise in activity one day before calving, which can easily be triggered by other causes such as stress from a different environment [41]. Other authors found "Restlessness" on the day of calving [42] or 12 h [43], 6 h [44,45], 140 min [46], or 120 min before calving. "Restlessness" might be caused by discomfort from labor [47,48] and is expressed by increased standing/lying transitions and increased walking [40,43]. Study participants listed signs, such as "Frequent lying/standing transitions", "Isolation seeking behavior" and "Behavioral changes" separately, all these terms have been comprised under the term "Restlessness" [3,39]. "Tail raising" and "Relaxation of the pelvic ligaments" were also on the list of signs to identify stage I of parturition of the study participants. "Tail raising" [39,44], "Relaxation of the pelvic ligaments" [3,4,39] are described as visible signs of stage I of parturition. For "Tail raising" time of appearance is reported for 9 h before the onset of stage II, [49] or 6 h before parturition [43,45,48]. The measurement of the relaxation of the pelvic ligaments has been shown to be a useful and accurate tool in predicting parturition within 24 h [23] or no parturition within 12 h [50]. Clear "Vaginal discharge" alone was not considered to be a suitable predictor [49]. Other signs, like "Vulva edematization" [39] or "Olfactory ground checks" [3] were not mentioned by participants.
Signs to describe stage II of parturition named by study participants are consistent with signs reported in the literature [3,18,20,35,51,52]. "Visibility of fetal parts in the vulva" and "Lying lateral with abdominal contractions" were named most frequently as very important signs to check on a regular basis. Abdominal contractions can be increasingly observed about 3 h before parturition [49], so they are seen in stage 1 and stage 2 of parturition.
Recommendations on when best to first begin to observe cows for early signs of imminent parturition and potential movement to the maternity pen are rarely found in the literature. This may be the reason for the large range of suggestions given in our survey. These ranged from one to more than 21 d before ECD. Cook et al. [53] suggested observations of cows in the close-up pen even 14 to 21 d before ECD. The ECD is not a precise metric to move cows into the maternity pen, as the duration of pregnancy varies between 279.4 ± 5.7 [54]. Gestation length can be influenced by the sex of the calf [55], cattle breed [56], twinning [57], and parity of the cow [58]. If moving cows according to ECD, some cows will spend too long in the maternity pen with negative consequences for environmental hygiene [20]. Nevertheless, one SME and 5 of the non-SMEs recommended "gestation length" as the sole parameter to determine the time of moving cows. Possibly, SMEs were more likely to have read the literature providing information on the diverse factors influencing the duration of gestation length [54,58,59] and non-SMEs have experienced in daily routine, that days after insemination works well in practice.
Previous studies report diverse protocols of cow movements before parturition. Cows were moved when parturition was considered imminent, either with no time specification [60,61] or the timing of movement was calculated retrospectively, e.g., within 1-4 h prepartum [62], 4 h before calving [63], or 48 to 72 h [64] up to 7 to 5 d before calving [65].
Respondents prioritized "Relaxation of the pelvic ligaments" and "Behavioral changes" as key criteria when to move cows to the maternity pen. "Relaxation of pelvic ligament" has been described to start as early as 15 d before parturition up to only 7 h ante partum [4]. Measuring the increment in ligament relaxation has a high accuracy (93.9%) in predicting calving within 24 h with and can be easily applied in field conditions [23]. "Behavioral changes" though can be difficult to define. All behaviors such as "olfactory ground checks, nest-building behavior, vocalization, discharge of feces and urine, restlessness, tripping, turning the head towards the abdomen and tail raising" under the term "Behavioral change" [3,39]. The cow's behavior changes when parturition is approaching [12]; sometimes physiologically due to pain [42,48] and sometimes due to calving difficulties [43]. Sensors measuring behavioral changes for calving prediction, i.e., activity [41] or tail raising [66] are commercially available.
When assessing the predictive value of a given SIP for determining the right time for cow movement, almost all participants chose the upper range between 41 and 100%, but only a very small proportion of participants (10.3%-2/24 SMEs; 2/15 non-SMEs) considered the predictive value of their selection to be very certain (i.e., 80-100%). However, this 10.3% of participants all selected different signs which they named to be very predictive. This suggests over-confidence in experts' ante judgment, failure to recognize objective ignorance, and perhaps lack of experts post evaluation. The favorite signs rated as important for imminent parturition were "Abdominal contractions" and "Vaginal discharge". Overall, signs selected were consistent with the literature [3,18,20,35,49,51,52].
Respondents recommended increased frequency of daily observations once the cows were in the maternity pen, most commonly every 2 or 6 h. These recommendations are similar to those published by Mee [37] who suggested observing cows in the first stage of parturition approximately every 3 to 6 h to detect the onset of the second stage or possible calving difficulties. After the onset of the second stage, an observation interval of every 30 min or continuous observation was recommended [37]. However, there are several protocols in scientific studies recommending an observation interval of every two [67] or every hour [3,41,49,65]. It has been shown that poor surveillance during calving leads to a significant increase in stillbirth frequency [68], but a constant presence of an observer can also lead to prolonged calving and dystocia [10]. A survey with farmers in Ireland revealed that only 33% of participants observed their prepartum cows at least every 6 h during the day or night and 24% reported not observing cows at all during the night [30]. Similar findings of poor nocturnal surveillance were reported in studies conducted in Canada [69,70] and in Brazil [71]. Since about half of calvings occur at night, these observation intervals may be inappropriate [72].
The benefits of technical devices for detecting calving and deciding when to move cows were not unanimously accepted by study participants. Various devices for calving surveillance have been developed and evaluated [41,63,73,74]. Study participants most frequently recommended vaginally inserted temperature loggers for calving detection. However, experiences and results of publications were diverse and such devices were not recommended by any author as a sole tool for calving prediction [6,63,73,75,76]. Tailfixed accelerometers were also recommended by study participants, although there is little published evidence to support their benefits. Studies [66,77] showed poor sensitivity of such a device and welfare issues retaining the sensor to the tail. Some respondents also recommended the use of cameras to monitor calving. Continuous calving monitoring with video cameras has been used in several (research) studies [43,45,48]. However, in practice 'calving cameras' are not widely used on commercial dairy farms internationally [30,69,70] and despite the various technological developments, visual observation of cow behavior is the most commonly used approach [6].
When asked about the importance of factors influencing the timing of cow movement to the maternity pen, study participants' assessments regarding the expertise of the personnel are consistent with the literature where comprehensive training on calving management practices has been identified as a top priority in order to reduce the incidence of calving difficulties [2,3,78]. The influence of the expertise of the personnel, like the influence of observation frequency, was fully agreed or agreed with by 84.4% of the study participants. Obviously the more often an animal is observed, the more likely it is that SIPs will be detected. A high proportion of study participants (80.0%) fully agreed or agreed on the influence of cow movement relative to the stage of parturition. Studies have been shown that there is a sensitive period near the end of stage I of parturition where moving a cow can disrupt calving progress [18,19]. Thus, the authors recommended moving cows during stage II of parturition [19,21] or having the facilities to move cows 2-3 wk earlier [22]. The timing of cow movement is predominantly seen to have an impact on the vitality of calves; 68.9% of study participants fully agreed or agreed. Research showed that the risk for prolonged second stage parturition increased for cows moved late in first stage parturition, resulting in a 2.5-fold increase in stillbirths [19,79]. In addition, studies showed that the duration of parturition significantly influenced the degree of calf vitality [80] and more precisely a study showed that 71% of calves had low vitality when stage II parturition lasted longer than 2 h [81].
Most participants agreed (26.66% fully agreed and 33.33% agreed) that the timing of moving cows to the maternity pen has an influence on the duration of parturition. Stress caused by moving the cow to the maternity pen during the first stage of parturition can stop or delay the calving process [22] and cause dystocia [37]. Undisturbed calving is essential because the duration of the second stage of parturition determines the course of calving [79]. Fourteen participants (31.1%) did not consider that, possibly due to the diversity of opinion in the literature [60][61][62][63][64][65] or based on their personal experience.
Most participants agreed (22.2% fully agreed and 42.2% agreed) that the timing of moving cows to the maternity pen also affects the ease of calving. Other studies reported that moving primiparous cows to the maternity pen in stage two of parturition resulted in lower average calving ease scores compared to stage one [21].
A vaginal examination can help to rule out dystocia. The majority (89.4%) of study participants recommended such an examination and only five (10.6%) did not recommend examining the cow or only in cases of no calving progress or if blood or the placenta came out. In some studies, cows were given a vaginal examination if no progress of parturition was observed two hours after AS burst [39] or feet were visible [82]. A Canadian study found that 61.3% of farmers do a vaginal examination if the AS already burst but calving is not progressing [69]. In North America, 94.6% of dairy farmers surveyed examined or assisted heifers and cows within 3 h of AS appearance, and 48.4% of those farmers would intervene within 1 h [52]. A high percentage of respondents (77.8%) in the present study recommended an examination within 1 h after observing the AS or feet outside the vulva. Bloody vaginal discharge was considered an immediate indicator for a vaginal examination for 37% of respondents, but others recommended waiting up to 24 h after seeing bloody vaginal discharge. Some of this variation may be due to the imprecise description of bloody vaginal discharge in the question, i.e., neither the volume nor the nature of the discharge was specified.

Conclusions
The objective of this survey was to elicit current recommendations on calving management from both SMEs and non-SMEs in order to provide farmers with best practice advice for managing the periparturient cow. There was good consensus between SMEs and non-SMEs apart from using ECD as a good sign for moving cows into maternity pens. It seems that some information found in the literature lacked high clinical utility due to the imprecision in either their definition, (e.g., restlessness), measurement (e.g., pelvic ligament relaxation), or timing (e.g., when to move the cow to the calving unit) or their poor evidential base (e.g., calving monitoring devices).
Thus, it can be concluded that it makes sense to differentiate between stages 1 and 2 of parturition. There is a broad agreement on how to identify imminent signs of parturition, but skilled and motivated personnel is needed to recognize those. However, more research is warranted to determine the best time for moving cows to the maternity pen. To rule out dystocia a vaginal examination of the calving cow was recommended. Technical devices are recommended to identify the onset of calving, without a clear recommendation of the best technique.
Author Contributions: C.F.-T. designed and supervised the study and had significant input into the survey instrument and all drafts; A.L.V. developed the questionnaire, conducted the online survey, and prepared all drafts of the paper; W.H. co-supervised the survey and had substantial contributions to drafts of the paper; J.F.M. interviewed practitioners at a congress and had substantial input into drafts of the paper. All authors have read and agreed to the published version of the manuscript. The timing of moving cows to the maternity pen has an influence on the duration of parturition.
The timing of moving cows to the maternity pen has an influence on calving ease.
The timing of moving cows to the maternity pen has an influence on the vitality of calves.
The expertise of the personnel has an influence on the right timing of moving cows to the maternity pen.
The frequency of observations has an influence on the right timing of moving cows to the maternity pen.

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There are technical device(s) that has/have an influence on the right timing of moving cows to the maternity pen.
The timing of moving cows to the maternity pen relative to the stage of parturition has an influence on the calving process.