Diversity, not uniformity: slaughter and electrical waterbath stunning procedures in Belgian slaughterhouses

Diversity, not uniformity: slaughter and electrical waterbath stunning procedures in Belgian slaughterhouses G. Devos,∗,† C. P. H. Moons,∗ and K. Houf†,1 ∗

Department of Animal Nutrition, Genetics, and Ethology, Faculty of Veterinary Medicine, Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium; and † Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium prised a constant voltage, multiple bird stunner. The minimum average electrical current that every chicken should receive at a certain frequency, as stated by the European Regulation No 1099/2009, was not achieved for each animal monitored due to the bird’s characteristics and the different applied stunning settings, with the exception of all ISA laying hens and broiler breeders in one particular slaughterhouse. The survival rate ranged from 96.0 to 100%, 97.0 to 100%, 68.0%, 72.0 to 85.1%, and 5.6 to 52.4% in 5-wk-old broilers, 6-wk-old broilers, LSL laying hens, ISA laying hens, and broiler breeders, respectively. Monitoring of unconsciousness after passing through the waterbath was not always performed and when it was, there was no uniformity in the applied criteria. It was concluded that a large variation in slaughter and stunning practices exists among slaughterhouses in Belgium. Further research should explore the effect of the different settings on inducing a successful stun and on carcass quality, and assess if the observed variation also exists in other EU member states.

ABSTRACT Data on slaughter and stunning protocols in Belgian poultry abattoirs were collected, and subsequently the survival rate after electrical waterbath stunning in 1,400 animals across 7 selected slaughterhouses was determined. The majority of the abattoirs applied electrical waterbath stunning (72%), whereas the other methods were gas stunning (13%), head-only stunning (6%), and dry stunning (3%). In 6% of the slaughterhouses, the birds were killed without previous stunning, according to religious rites (i.e., ritual or religious slaughter). Although religious slaughter occurred in a substantial number of abattoirs, the customers of the majority of them allowed stunning, provided the animals were not killed by the stunning procedure. Substantial variation both in electrical waterbath devices and technical settings (electrical current type, wave type, voltage, frequency) combinations was observed. These settings did not only differ between slaughterhouses, but also between subsequent visits to the same slaughterhouse. Despite this variation, all systems com-

Key words: poultry, electrical waterbath stunning, technical setting, survival rate 2018 Poultry Science 0:1–11 http://dx.doi.org/10.3382/ps/pey181

INTRODUCTION

slaughter, provided that the animals are not killed by this procedure (Velarde et al., 2014). Though several stunning methods are permitted (European Union, 2009), a report of the European Commission (2013) indicated that the majority of broilers (80%), laying hens (83%), parent flocks (61%), and turkeys (76%) slaughtered in the EU are stunned by electrical waterbaths, whereas controlled atmosphere stunning is applied for 20, 7, 37, and 24% of the abovementioned categories of animals, respectively. Other alternatives are head-only electrical stunning and low atmosphere pressure stunning, the latter currently being only allowed in the United States (European Commission, 2013). Most poultry slaughterhouses apply a multiple-bird waterbath for electrical stunning, in which the voltage is applied between 2 electrodes: one is located at the bottom of the waterbath, whereas the other one is the shackle line that is grounded for safety reasons. The electrical circuit is closed when the bird’s head

According to European Regulation No 1099/2009 (European Union, 2009) on the protection of animals at the time of killing, it is required that animals, including poultry, are stunned by an appropriate method before slaughter and that they remain unconscious and insensible to pain until death occurs. An exception to this regulation is represented by the slaughter prescribed for religious rites (European Union, 2009), where the animals need to be alive, healthy, and have suffered no injury at the time the neck’s blood vessels are severed according to the requirements of the Jewish (shechita), Muslim (halal), and Sikh (jatka) communities. However, some Muslim communities allow stunning before

 C 2018 Poultry Science Association Inc. Received September 13, 2017. Accepted April 18, 2018. 1 Corresponding author: [email protected]

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DEVOS ET AL.

enters the water resulting in an electrical current flowing through the bird, causing unconsciousness (Kettlewell and Hallworth, 1990). Consciousness is defined as the ability to feel emotions and to control voluntary mobility, whereas sensibility is defined as the ability to feel pain (European Union, 2009). In conscious animals, the neurons in the brain are in a depolarized state, but when electrical stunning is applied, this depolarized state is being disrupted by electrical current flowing through the brain, thereby causing unconsciousness and insensibility (Raj and Tserveni-Gousi, 2000). European Regulation No 1099/2009 has imposed requirements concerning the minimum electrical current that each bird submitted to waterbath stunning should receive in relation to a particular frequency range. Each chicken has to receive a minimum electrical current of 100, 150, or 200 mA when frequencies of less than 200 Hz, from 200 to 400 Hz, or from 400 to 1,500 Hz are used, respectively (European Union, 2009). Birds submerged simultaneously in the waterbath can be considered as a series of resistors connected in parallel. This implies that the electrical current flowing through each animal varies according to multiple factors, i.e., the applied voltage, the electrical impedances of the birds (which is determined by its characteristics such as gender, weight, age, etc.), the electrical contacts in the circuit, the depth of immersion (depending on the size of the birds and the height of the waterbath), and the degree of contact between the birds’ wings (Kettlewell and Hallworth, 1990; Gregory, 1995). For example, Sch¨ utt-Abraham et al. (1987) have shown that the resistance of laying hens can vary from 1,900 to 7,000 Ω. It is difficult to measure the electrical current passing through each bird during the stunning procedure in slaughterhouse conditions. In such a context, the minimum electrical current is estimated as being the total electrical current flowing through the waterbath, divided by the number of birds that are simultaneously submerged in the waterbath (EFSA, 2012). The minimum electrical current stipulated in the European Regulation No 1099/2009 is in fact expressed as a minimum average electrical current per each bird. Other factors having an influence on the outcome of the stun are the duration of contact, the frequency, the electrical current type (alternating current [AC] or direct current [DC]), and the waveform (e.g., sine wave) (Kettlewell and Hallworth, 1990). An epileptic seizure, and hence loss of consciousness, is being induced when a sufficient electrical current reaches the brain of the animals. When insufficiently stunned (i.e., the electrical current reaching the brain is too low), such animals could be immobilized, but still sensitive to pain and stress (Barbut, 2002). On the other hand, it is also possible that ventricular fibrillation is induced by the electrical current, which means that the birds are killed by the stunning procedure (Gregory and Wotton, 1987; Gregory et al., 1991). Some birds may pass the electrical waterbath without ever making contact with the water, as they are too small and their heads do not reach the water level or

when wing flapping occurs. The latter can also lead to birds experiencing pre-stun electric shocks, which do not induce unconsciousness, and occur when the birds’ wings make contact with the waterbath before the head, or by contact with water overflowing at the entrance of the waterbath (Heath et al., 1981; Gregory, 1989). In Belgium, between 2014 and 2016, almost 302 million poultry were slaughtered on average each year, of which 99.67% chickens (Gallus gallus), 0.27% turkeys (Meleagris gallopavo), 0.02% ducks (Anas platyrhynchos), and 0.04% other poultry. This amounts to a total slaughtered weight (cold weight) of 449 million kilograms, or 24.63% of the total weight of all animals slaughtered in Belgium (beSTAT-FOD economie, 2017). Belgium is one of the most important EU exporting member states and, together with the Netherlands, France, Poland, the United Kingdom, and Germany, covers 79% of the total EU poultry meat export (European Commission, 2015). To date, there is limited information available about current Belgian slaughter practices and, consequently, the implementation of the requirements stated in the European Regulation No 1099/2009. The aims of this study were to make an inventory of all the Belgian poultry slaughterhouses, to perform an observational study about the use of the electrical waterbath stunning by visiting several poultry slaughterhouses, and to determine the effect of the applied technical settings on the post-stunning survival rate.

MATERIALS AND METHODS Inventory of Poultry Slaughterhouses In 2014, all Belgian poultry slaughterhouses were localized based on a (yearly updated) list published on January 1, 2014 by the Federal Agency for the Safety of the Food Chain (FASFC) (FASFC, 2014). The applied stunning method (gas/electrical/no stunning) in these slaughterhouses was determined via phone or e-mail contact. After this initial screening, slaughterhouses applying electrical or no stunning were contacted again by phone or e-mail and more information was collected about the way of stunning, slaughtered poultry type, slaughter capacity, the market, and ritual slaughter. Four categories of slaughter capacity were arbitrarily defined: very small (<1,000 animals/wk), small (1,000 to 10,000 animals/wk), average (10,000 to 100,000 animals/wk), or large (>100,000 animals/wk).

Survey of Current Practices in Belgian Slaughterhouses (Electrical Stunning/no Stunning) Based on the results from the inventory, all slaughterhouses using electrical stunning or no stunning were then contacted for an onsite visit. These visits occurred from June 2014 to February 2015 and comprised 18

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ELECTRICAL WATERBATH STUNNING OF POULTRY

abattoirs. Per slaughterhouse, a standardized set of questions was used, which were administered to the contact person of the abattoir using a semistructured interview, or were completed through direct observation. The questions covered 7 main aspects of the stunning and slaughtering process: shackling, slaughter line and shackles, stunning device, adjustment and registration of the settings, neck cut, ritual slaughter, and monitoring of unconsciousness. For companies willing to cooperate but unable to allow an onsite visit, information was collected by phone, e-mail, or both.

Survival Rate after Electrical Waterbath Stunning Following completion and analysis of the survey, 7 slaughterhouses, representing at least 80% of the overall Belgian slaughter capacity, were visited again, from 2016 January to October, to verify the number of animals surviving the stunning procedure. Some abattoirs slaughtered multiple poultry types, some only one. In each slaughterhouse, 100 animals were tested per poultry type. For some slaughterhouses, multiple visits (with a maximum of 7) were necessary to achieve the intended number of animals. In addition, in 2 slaughterhouses, those who used technical settings approaching the requirements of the European Regulation No 1099/2009, an additional 400 animals were examined to confirm the findings from the first batch. To evaluate the effects of stunning on survival, each tested animal was taken from the line after passing through the waterbath and was placed on a table. It was registered whether the animal regained consciousness or, instead, died. As a reference for regained consciousness, the return of tension in the neck muscles was used, because absence of the neck tension can occur at the same time as suppression of brain activity (Gerritzen et al., 2004). Assessment of the neck tension was performed by placing the fingers of one hand under the neck and raising it. The neck tension was considered to have returned when the chicken could hold its head up independently. For each tested animal, the applied voltage, frequency, and estimated average electrical current flowing through the chicken were registered. Cameras (Hero 3+ black edition, GoPro, San Mateo, CA), placed at the beginning and end of the waterbath, registered when the chickens entered and left the waterbath. At the same time, another camera registered the technical settings (voltage, frequency, and total electrical current), which were shown on a display of the waterbath stunning equipment. Possible fluctuations in the voltage could not be registered as the waterbaths’ displays (either analog or digital) only showed a constant value. The waterbaths’ displays showed the total electrical current. However, European Regulation No 1099/2009 prescribes average electrical currents per animal (European Union, 2009). Therefore, an estimate of the

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electrical current flowing through the tested animal was calculated by dividing the total electrical current by the number of birds having contact with the water. This calculation was done for every second the tested animal was submerged in the water, in order to calculate an average value per animal. Those data for individual animals were also combined to calculate an average and standard deviation for each poultry type slaughtered in a particular slaughterhouse. For the additional 400 chickens that were tested, the electrical current was not specifically linked to each of the tested birds. However, cameras registered the total electrical current in the waterbath while the tests were performed, and for every 5 s of images, the total electrical current was noted (approximately 500 data per poultry type in each of the 2 slaughterhouses). Then, an estimate of the electrical current flowing through individual animals was calculated by dividing the total electrical current by the number of birds in the waterbath. Those data for individual animals were also combined to calculate an average and standard deviation for each poultry type slaughtered in each of the 2 visited abattoirs. For this part of the study, approval to examine the animals at the abattoir was obtained from the Ethical Committee of the Faculty of Veterinary Medicine, Ghent University (EC 2015/32).

RESULTS Inventory of Poultry Slaughterhouses According to the list published by FASFC (FASFC, 2014), there were 39 poultry slaughterhouses operating in Belgium at the onset of the research. Seven abattoirs were excluded for further investigation for various reasons: slaughter of poultry types other than broilers, laying hens, turkeys, or breeders (n = 5); cessation of activities (n = 1), or no response to phone calls or e-mails (n = 1). Of the remaining 32 abattoirs, 26, 4, and 2 slaughterhouses applied electrical, gas, and no stunning, respectively. More information, as described below, was collected on 28 slaughterhouses that applied electrical or no stunning. Slaughter Capacity Eight of the 28 abattoirs slaughtered less than 1000 animals/wk (very small slaughterhouses that slaughter for private individuals or for their own poulterer shop, or both). The other slaughterhouses were small (n = 5/28), average (n = 7/28), and large (n = 8/28). In the largest slaughterhouse, almost one million animals were slaughtered every week. Type of Slaughtered Poultry Fourteen of the 28 abattoirs, mainly those with a (very) small slaughter capacity, slaughtered several types of poultry (broilers, laying hens, breeders, turkeys, quails, ducks, etc.). The remaining abattoirs slaughtered a single type of

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poultry, i.e., broilers (n = 12/28), laying hens (n = 1/28), or turkeys (n = 1/28). Market The majority of the abattoirs (n = 18/28) supplied, mainly or exclusively, the Belgian market. In addition, there were 3 slaughterhouses (with a large slaughter capacity) of which the products were mainly intended for export. The remaining 7 slaughterhouses (with a slaughter capacity ranging from small to large) delivered their products both in Belgium and abroad (mainly the Netherlands and France). Eighteen of the 28 abattoirs delivered fresh products, 9 others produced both fresh and frozen products, and in 1 abattoir each product was sold frozen. The majority of the slaughterhouses (n = 22/28) produced both whole carcasses and cut or processed products. In 3 of the 28 abattoirs, all carcasses were cut or further processed or both and 3 other slaughterhouses produced exclusively whole carcasses. Stunning Method In 26 slaughterhouses, different electrical stunning methods were applied: electrical waterbath (n = 23/26), dry stunning (n = 1/26), and head-only stunning (n = 2/26). The latter consisted of systems by which the head was manually held on the stunning system. With the dry stunning method, the animals were hung on the slaughter line, after which the head passed across an electrically charged metal grid. Both the dry stunning and head-only stunning methods were only used in (very) small abattoirs (<10,000 birds/wk). Two slaughterhouses did not apply stunning at all because of ritual slaughter. Ritual Slaughter Although more than 40% of slaughterhouses (n = 12/28) applied ritual slaughter, (mild) stunning was accepted by the customers in the majority of these abattoirs (n = 10/12). Mild stunning is the application of stunning settings that stun the birds with the certainty that they are not killed by the stunning procedure. In one slaughterhouse only Kosher slaughter was applied, whereas in the other slaughterhouse both Halal and Kosher slaughter were performed.

Survey of Current Practices in Belgian Slaughterhouses (Electrical Stunning/no Stunning) Eighteen poultry slaughterhouses, representing 90% of the Belgian slaughter capacity, offered to cooperate. Fourteen of these slaughterhouses were visited. The remaining 4 slaughterhouses refused an onsite visit due to a lack of time, shortness of staff, or both, but provided information via phone or e-mail. Fifteen slaughterhouses used the electrical waterbath as stunning method, one applied head-only stunning, one other applied dry stunning, and the remaining one did not apply stunning (religious reasons). Shackling In the majority of slaughterhouses (n = 15/18), the animals were manually uncrated, whereas an automated system was used for this purpose in 3 abattoirs. In 16 of the 18 slaughterhouses, the ani-

mals were shackled prior to stunning. The place on the slaughter line where the birds were shackled was mostly rectilinear (n = 13/16), although there were a few slaughterhouses that used a carrousel system (n = 3/16). In the 2 remaining abattoirs, the animals were only shackled after neck cutting, as the animals were not stunned or the head of the animals was held manually on the stunning device (head-only stunning). Slaughter Line and Shackles The amount of bends that the shackle line showed between the place where the animals were shackled and the stunning device (the waterbath or the electrically charged metal grid) was 0 (n = 3/16), 1 (n = 4/16), 2 (n = 7/16), and 6 (n = 2/16). In more than 60% of the slaughterhouses (n = 10/16), the slaughter line inclined once or several times before the stunning device (waterbath or electrically charged metal grid) was reached. A limited number of slaughterhouses (n = 5/16) had equipped the slaughter line with a plate against which the breast of the animals could rest in order to reduce wing flapping between the place where the animals are shackled and the stunning device. All shackles were made from stainless steel. The distance between the shackles (measured near the point of attachment on the slaughter line) measured 15 cm (6 inch), 18 cm (7 inch), 20 cm (8 inch), or 23 cm (9 inch) and in case of turkeys 28 cm (11 inch). None of the shackles had the possibility to be adjusted to the size of the shanks in case multiple types of poultry were slaughtered. The distance between the place where the animals were shackled and the stunning device varied from 1.98 to 29.00 m. The time needed to bridge this distance measured 10 to 130 s, which resulted in a slaughter speed of 0.02 to 0.47 m/s (Table 1). Electrical Waterbath There were 15 slaughterhouses that applied electrical waterbath stunning. The waterbaths at the different abattoirs originated from 5 different manufacturers: LINCO Food Systems B.V. (Doesburg, the Netherlands), Foodmate B.V. (Oud-Beijerland, the Netherlands), Marel Stork Poultry Processing B.V. (Boxmeer, the Netherlands), Meyn Food Processing Technology B.V. (Oostzaan, the Netherlands), and Systemate Numafa B.V (now Meyn Food Processing Technology B.V.). These different types of waterbaths showed a large variation in length, age, number of animals simultaneously having contact with the water, and the duration of contact with the water (Table 2). With the exception of one abattoir, the height of the electrical waterbath could be adjusted as a function of the size of the animals that were about to be stunned. Although this possibility was available in all but one slaughterhouse, there were a number of abattoirs (n = 6/15) that never adjusted the height of the waterbath. Measures to prevent pre-stun electric shocks at the beginning of the waterbath were taken in 5 of the 15 slaughterhouses. These preventive measures included a steep entrance ramp, a plate under which the excessive water could flow away, or the slaughter

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ELECTRICAL WATERBATH STUNNING OF POULTRY Table 1. Distance from the location of shackling to that of stunning, time needed to bridge this distance, the resulting slaughter speed, and the time between leaving the stunning device and the neck cut. Slaughterhouse 1 2 3 4 5 6 7 81 9 10 11 122,3 132 142 152 16 174 185 Average ± SD6

Distance shackling to stunning (m) 16.00 6.90 17.10 9.70 3.40 3.10 11.40 1.98 29.00 (line 21.50 (line 2.50 5.20 2.00 2.00 2.00 2.00 19.44 (line 22.38 (line n/a7 n/a

1) 2)

1) 2)

9.87 ± 8.83

Time shackling to stunning (s)

Slaughter speed (m/s)

Time stunning to neck cutting (s)

45.00 18.00 41.00 130.00 10.00 12.50 120.00 48.00 62.00 46.00 58.00 61.00 110.00 85.00 90.00 80.00 90.00 103.00 n/a n/a

0.36 0.38 0.42 0.08 0.34 0.25 0.10 0.04 0.47 0.47 0.04 0.09 0.02 0.02 0.02 0.03 0.22 0.22 n/a n/a

7 9 7 28 20 20 26 40 7 7 17 32 10 15 10 20 13 17 2 n/a

67.19 ± 36.14

0.20 ± 0.17

16.16 ± 9.93

1

Presented data refer to male turkeys with a body weight ranging from 13 to 17 kg. Data collected by phone or e-mail or both. 3 Stunning by electrically charged metal grid. 4 Stunning by manually holding the head on the stunning system. 5 Slaughterhouse 18 did not apply stunning for religious reasons. 6 Standard deviation. 7 Not applicable. 2

line that descended steeply right above the entrance of the waterbath. In one slaughterhouse, an arbitrary amount of salt was added to the water in order to improve the conductivity. This was added once at the beginning of slaughter and was not repeated during the rest of day. The water level was maintained by means of a float (n = 5/15) or by a continuously running tap (n = 10/15). The applied electrical current type was pulsed DC (n = 5/15) or AC (n = 3/15). In approximately half of the abattoirs, the applied electrical current type was unknown to the people working with the electrical waterbath. When AC was used, a square or sine waveform was applied. Details about the used settings are shown in Table 2. Head-only Stunning In the slaughterhouse where the animals were stunned by holding their heads on the electrical stunning device, the contact time with this device measured 4 s. The set voltage was 85 V, but the resulting electrical current could not be verified due to the absence of a display on the stunning device. After the animals were stunned, it took 2 s until the neck was cut. The neck cut was performed manually and bilaterally. Dry Stunning In the slaughterhouse where the animals were stunned by passing with their heads across an electrically charged metal grid, the contact time with

this device measured 15 s. The set voltage was 80 V, but information about the resulting electrical current was not available. After the animals were stunned, it took 10 s until its neck was cut. Like the head-only stunning method, the neck cut was performed manually and bilaterally. Neck Cutting after Electrical Waterbath Stunning After leaving the waterbath, it took 7 to 40 s until the neck was cut (Table 1). In 5 of the 15 slaughterhouses that applied electrical waterbath stunning, the neck cut was performed mechanically, whereas in more than half of the abattoirs (n = 8/15) this was done manually. In 2 of the 15 slaughterhouses, the neck was cut manually or mechanically, depending on whether the slaughter was performed ritually or not. In case of a mechanical neck cut, there was always a minimum of 1 person present in order to check the cut and, if necessary, to repeat it. In general, the neck cut was performed bilaterally (n = 11/15). Adjustment and Registration of the Settings A total of 17 slaughterhouses applied electrical stunning (electrical waterbath, head-only, or dry stunning). In more than half of these slaughterhouses (n = 9/17), the settings were occasionally changed. Reasons for adjustments were, for example, the slaughter of different poultry types or the fact that a difference was made between heavy and light animals. In turkeys, separate settings were used for males and females and the weight

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Table 2. Length and age of the waterbath, duration of contact with the water, number of animals that were simultaneously in the waterbath, slaughtered poultry type, and the applied technical settings in the different slaughterhouses.

Slaughterhouse

Length (m)

Age (yr) 2

Number of Duration of simultaneous contact (s) animals Poultry type

AC or DC

Voltage (V)

4

±600 550 to 1,100 960 to 1,120 2,10010 450 to 500 800 to 1,005

60 to 140

/ DC

50 to 90 95 to 107

50 1,000

/ / / / / DC DC

110 11010 90 to 110 70 to 100 27 to 100 26 to 27 100

/ 50 / / 67 110 to 111 1,100

100 to 300 2,200 to 2,700 / 500 to 700 / / / 500 to 620 /

2.00 2.70 3.40 1.02 1.60 2.44

/ 3 3 25 23 1

6 7 8.5 13 4.5 10

13 12 19 5 10 16

B5 B65 B6 B6 LSL6 ,ISA7 B5, B6

DC DC AC / AC AC

64 70 57 69 to 71 150 70 to 75

7

1.60

15

17

9

1.70 5.15 (line 1 and 2)

23 4

41 11

6 29

B5, B6, ISA, BB8 Turkeys B5,B6

DC

3

0.90 1.03 0.90 0.90 1.00 3.47 (line 1) 2.00 (line 2)

/ 20 / / / > 20 > 20

21 13 38 40 40 13 8

5 5 5 5 5 17 10

C9 B5, B6 C C C B5 B5

10 11 131 141 151 16

Total electrical current (mA)

1,007 190 500 167 50 1,200 to 1,300 199

1 2 3 4 5 6

8 9

Frequency (Hz)

500 to 820

1

Data collected by phone or e-mail or both. Data unknown. 3 Presented data refers to male turkeys with a body weight ranging from 13 to 17 kg. 4 Broiler 5 wk old. 5 Broiler 6 wk old. 6 LSL laying hen. 7 ISA laying hen. 8 Broiler breeder. 9 Combination of one or more of the mentioned types in the table with other poultry types. 10 Data that could not be read, but were communicated orally. 2

within each sex was also taken into account. Other reasons for adjusting one or more parameters were the observation of an increased incidence of carcass damage (e.g., haemorrhages) or too many animals being insufficiently stunned. However, when changes were made, almost exclusively the voltage was adjusted while the frequency was maintained. More than half of the abattoirs (n = 9/17) registered the data on the settings that were applied. In general, these data were written down at the beginning of slaughter and in about half of the slaughterhouses these data were also checked during the rest of the day, often when passing the equipment or when it was necessary to adjust the settings. The recorded data were stored for several years. Some slaughterhouses (n = 3/17) had recently started with this registration, whereas this was already a part of the routine for years in others (n = 6/17). Ritual Slaughter In about 55% of the abattoirs (n = 10/18), religious slaughter was applied, either exclusively or in combination with non-religious slaughter. A (mild) stun was accepted by most of the customers, with the exception of one slaughterhouse where the animals had to be slaughtered without prior stunning (religious reasons). A prerequisite for these customers was that the animals were not killed by the stunning procedure. It was therefore regularly checked, by personnel of the abattoir, whether the animals regained consciousness after the performed stun. To assess this, they reg-

ularly removed a bird from the slaughter line, placed it on the ground, and waited until the bird could stand on its feet again. With the exception of 2 slaughterhouses, neck cutting was performed manually when religious slaughter was applied. Monitoring of Unconsciousness In 7 of the 18 slaughterhouses, unconsciousness was not monitored. In abattoirs where this did happen, it appeared that the moment (after leaving the stunning device or after neck cutting) and frequency of controls varied. Monitoring was usually performed by the “animal welfare officer,” but sometimes other staff members also assessed the stunning result, although they had not received an official training for that. The following criteria were used most to assess unconsciousness: no movement, no breathing, no blinking, no corneal reflex, no response to comb pinching, no neck tension, and no wing flapping. None of the slaughterhouses used the same combination of parameters for the assessment. Absence of rhythmic breathing was the most important parameter for most of the abattoirs. However, this criterion was not maintained within each slaughterhouse.

Survival Rate after Electrical Waterbath Stunning A total of 1,400 birds was tested (in slaughterhouse 16, 2 different waterbaths were used and for each

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ELECTRICAL WATERBATH STUNNING OF POULTRY Table 3. Technical settings (electrical current type AC/DC, voltage, frequency, and resulting estimated average electrical current through the animal) of the electrical waterbath applied in the 7 visited slaughterhouses for each poultry type and the corresponding survival rate.

Slaughterhouse 2 3 5 6

7

9 16

Poultry type

Number of animals (n)

AC or DC

Voltage (V)

Frequency (Hz)

B61 B6 LSL2 ISA3 B54 B5 B6 B6 B5 B6 BB5 BB ISA B5 B6 B5 B5

100 100 100 100 23 77 36 64 100 99 82 18 101 100 100 100 100

AC AC AC AC AC6 DC7 AC6 DC7 AC AC AC AC AC DC DC DC DC

40 70 150 150 546 2807 546 2807 50 50 100 120 140 100 95 27 (line 1) 100 (line 2)

120 800 50 50 1,2006 1,5007 1,2006 1,5007 199 199 199 199 199 1,000 1,000 111 (line 1) 1,100 (line 2)

Average electrical current/animal ± SD8 (mA)

Survival rate (%)

26.7 ± 4.6 92.1 ± 7.4 41.4 ± 5.6 58.5 ± 3.1 174.2 ± 13.9 232.3 ± 13.09 192.9 ± 12.1 253.3 ± 17.79 124.7 ± 11.39 139.5 ± 11.99 215.8 ± 43.79 266.6 ± 43.69 146.3 ± 17.69 95.1 ± 7.0 99.6 ± 6.0 37.0 ± 6.0 (line 1) /10 (line 2)

99.0 98.0 68.0 72.0 100.0 100.0 100.0 100.0 96.0 97.0 52.4 5.6 85.1 98.0 99.0 97.0 100.0

1

Broiler 6 wk old. LSL laying hen. 3 ISA laying hen. 4 Broiler 5 wk old. 5 Broiler breeder. 6 Original settings. 7 Settings after changing the waterbath equipment. 8 Standard deviation. 9 According to the requirements of the European Regulation No 1099/2009. 10 Data unknown. 2

waterbath 100 animals were tested): 500 5-wk-old broilers, 499 6-wk-old broilers, 100 white laying hens (Lohmann Selected Leghorn; LSL), 201 brown laying hens (ISA brown; ISA), and 100 broiler breeders. The visited slaughterhouses, the applied technical settings of the electrical waterbath, and the corresponding survival rate after stunning are shown in Table 3. The survival rate ranged from 96.0 to 100%, 97.0 to 100%, 68.0%, 72.0 to 85.1%, and 5.6 to 52.4% in 5-wk-old broilers, 6wk-old broilers, LSL laying hens, ISA laying hens, and broiler breeders, respectively. When frequencies higher than or equal to 1,100 and 1,200 Hz were applied, the survival rate measured 100% in 5-wk-old broilers and 6-wk-old broilers, respectively. Within the ISA laying hens, a frequency of 50 Hz resulted in less birds surviving the electrical stunning procedure. All tested LSL laying hens were stunned with a frequency of 50 Hz and this also resulted in a lower survival rate. Within the broiler breeders, a higher electrical current per animal resulted in less animals surviving the waterbath. All slaughterhouses used the same settings when we determined survival rate compared to the settings during the survey study, except for 2 slaughterhouses (3 and 6) that had installed a new electrical waterbath installation. In addition, one of those 2 slaughterhouses changed their electrical waterbath equipment again inbetween 2 visits during the survival rate data collection. During the registration of the technical settings in slaughterhouses 2 and 7, it became clear that the ap-

plied electrical current type was AC and not DC, as it had previously been communicated by the slaughterhouses during the survey study. As shown in Table 3, based on the average values across all animals tested, only slaughterhouses 6 and 7 seemed to fulfill the requirements of the European Regulation 1099/2009 regarding the minimum electrical current per animal depending on the applied frequency level. However, the legislation requires that every chicken receives a minimum average electrical current. When examining the data in detail, the percentage of animals not receiving the required minimum electrical current was 0% in broiler breeders and laying hens, and ranged from 0 to 2.6% in broilers. To verify this finding of broilers not receiving the required minimum electrical current, measurements on 100 animals per type of bird were repeated in those 2 slaughterhouses (Table 4). It should be noted that both slaughterhouses applied different settings compared to the first set of measurements. Similar to the original findings, based on the average electrical current per animal, calculated for all the data within each poultry type and slaughterhouse, both slaughterhouses attained the legal requirements, with the exception of 5-wk-old broilers in slaughterhouse 7. When examining the distribution of the data on estimated electrical current per animal, we found that 37.9% (5-wk-old broilers in slaughterhouse 6), 28.8% (6-wk-old broilers in slaughterhouse 6), and 7.1% (6-wk-old broilers in slaughterhouse 7) of

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DEVOS ET AL. Table 4. Technical settings (electrical current type AC/DC, voltage, frequency, and resulting average electrical current through the animal) of the electrical waterbath applied in slaughterhouses 6 and 7 during the second visit for each broiler type and the corresponding survival rate.

Slaughterhouse 6 7

Poultry type

Number of animals (n)

AC or DC

Voltage (V)

Frequency (Hz)

B51 B62 B5 B6

100 100 100 100

DC DC AC AC

270 270 40 40

1,280 1,280 99 99

Average electrical current/animal ± SD3 (mA)

Survival rate (%)

± ± ± ±

100.0 99.0 97.0 94.0

202.2 205.4 94.8 114.3

16.24 15.04 8.5 11.14

1

Broiler 5 wk old. Broiler 6 wk old. Standard deviation. 4 According to the requirements of the European Regulation No 1099/2009. 2 3

the animals received an average electrical current below the values required in the European Regulation No 1099/2009.

DISCUSSION Inventory of Poultry Slaughterhouses Although several stunning methods are authorized according to European legislation, the majority of Belgian poultry slaughterhouses (72%) used the electrical waterbath that is still the most commonly used commercial stunning method in Europe (European Commission, 2013). Other stunning methods were gas stunning (13%), head-only stunning (6%), and dry stunning (3%). In the present study, head-only stunning was only applied in small slaughterhouses as this particular method, where the head of the bird is placed manually in contact with the 2 electrodes, cannot be performed in slaughterhouses with a high slaughter capacity. In recent years, this method has been adapted for use in commercial slaughterhouses: head-only stunning using cone-shaped restrainers and a head-only waterbath stunning system (Lambooij et al., 2010, 2014; Lines et al., 2011; European Commission, 2013), but none of the Belgian poultry slaughterhouses applied this type of stunning. Ritual slaughter was applied in a substantial number of the slaughterhouses (43%), but 83% of the customers of these abattoirs allowed stunning before slaughter. Only 2 of the 28 slaughterhouses that were included in the inventory did not apply stunning. A study performed in Italy investigated the prevalence of religious slaughter in slaughterhouses for cattle, small ruminants, and poultry (Cenci-Goga et al., 2010). They reported that 1.31% of poultry were slaughtered without stunning, but this result may not be representative for the entire country as only 18% of all Italian slaughterhouses participated in the study. Velarde et al. (2014) evaluated current practices during religious slaughter in selected countries. They visited 6 poultry slaughterhouses (3 in Germany, 2 in Spain, and 1 in Italy) of which 5

applied stunning, either by the electrical waterbath or by exposing the animals to a gas mixture.

Survey of Current Practices in Belgian Slaughterhouses A large variation with regard to the use of electrical waterbath stunning was seen, and previous studies have shown that some waterbath types or settings are more efficient compared to others (Sparrey et al., 1993; Wilkins et al., 1999; Raj et al., 2006a,c). A survey performed in the Netherlands showed a large variation among Dutch poultry slaughterhouses in terms of dimensions of the waterbath, the applied voltage and frequency, the resulting electrical current, and the exposure time (Hindle et al., 2010). The electrical waterbaths in Belgian poultry slaughterhouses differed in terms of manufacturer, length of the waterbath, number of animals simultaneously in the bath, etc. Also, the applied technical settings showed a large variation, with both the voltage and frequency settings ranging from low to high (26 to 150 V and 50 to 1,300 Hz). These variations led to variations in estimated average electrical current per animal. When higher frequencies are used, a higher electrical current is required to induce an affective stun, i.e., sufficient electrical current flowing through the animals (Raj et al., 2006a,c). Although lower frequencies are more likely to induce an effective stun, they also lead to more carcass defects and thus downgrading (Wilkins et al., 1999). On the other hand, it could be that even low-frequency pulsed DC causes cardiac arrest in conscious birds that makes the use of it questionable on welfare grounds (Raj et al., 2006a). Also, European Regulation No 1099/2099 defines stunning as “any intentionally induced process which causes loss of consciousness and sensibility without pain, including any process resulting in instantaneous death.” Thus, inducing cardiac arrest in conscious birds is not allowed by Europe (European Union, 2009). The use of sine wave AC is more effective in inducing a successful stun compared to pulsed DC because a lower voltage and electrical current can be used

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ELECTRICAL WATERBATH STUNNING OF POULTRY

to induce unconsciousness (Raj et al., 2006a,c). All slaughterhouses in the present study used a constant voltage, multiple bird stunner which means that birds entering the waterbath represent parallel resistors and thus receive an electrical current depending on their impedance (Sparrey et al., 1993). The voltage should be high enough to deliver the recommended minimum average electrical current to each bird and it is the latter factor that is important for inducing an effective stun (Sparrey et al., 1993; EFSA, 2004). But with a constant voltage stunner, it is possible that some birds receive insufficient electrical current to render them unconscious (Wilkins et al., 1999). A constant electrical current stunner measures the impedance of the birds and adjusts the voltage in order to deliver the pre-set minimum electrical current to the birds (Sparrey et al., 1993; Wilkins et al., 1999). Although this is beneficial in terms of animal welfare, this system was not being used in any of the visited slaughterhouses, probably because of the high processing speed that makes it difficult to isolate each bird long enough to deliver the pre-set electrical current, as also previously shown by Bilgili (1999). Although it may improve stunning efficiency, salt was added to the water in only 1 slaughterhouse. Research has indicated that addition of salt can improve the electrical conductivity during the first 20 to 30 min of processing which could increase the chances of inducing a successful stun at the start of slaughter. After 30 min of slaughter, the resistance of the water in the bath is reduced due to dirt and fecal matter originating from the birds passing through (Perez-Palacios and Wotton, 2006). That certain personnel of an abattoir are knowledgeable about the technical details of the installed waterbath equipment is important when aiming at delivering an effective stun. Although EFSA has already recommended that the electrical current type (including the waveform), the frequency, and the minimum electrical current for each bird should be included in the European Regulation, only the frequency and the minimum electrical current were included (EFSA, 2004). Addition of the electrical current type could not only be beneficial for the standardization of technical settings in all poultry slaughterhouses, it could also improve the knowledge of the used equipment as in about half of the slaughterhouses, the applied electrical current type was unknown to the people working with the electrical waterbath. Alternating current, as already mentioned, is more effective compared to DC (Raj et al., 2006a,c), which means that the required voltage to induce unconsciousness depends on the applied electrical current type. The configuration of the shackles and slaughter line can have an influence on the occurrence of wing flapping. The space that is foreseen for the shanks on the shackles could not be adjusted to the size of the birds in the visited slaughterhouses although several of them slaughtered multiple poultry types or different ages or

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both. A study performed by Gentle and Tilston (2000) already demonstrated that shackling is painful. Therefore, when large-size birds are shackled they will experience more pressure on their shanks, which may cause more wing flapping, because these animals experience more pain (Gentle and Tilston, 2000). In most of the visited abattoirs the slaughter line showed one or several bends between the place where the birds were shackled and the stunning device which may lead to an increase in wing flapping (Gregory and Bell, 1987). Although in more than half of the slaughterhouses visited in our study gradual inclines in the line were seen, this should not lead to an increase in wing flapping according to Gregory and Bell (1987). Because wing flapping could lead to birds missing the waterbath or experiencing pre-stun electric shocks (Gregory, 1989), EFSA (2004) has recommended a time interval of 12 s between the moment of shackling and stunning to reduce the prevalence and duration of wing flapping. Except for 1 slaughterhouse, the time interval between shackling and stunning always exceeded this 12 s. The prevalence of wing flapping itself was not evaluated during the present study. European Regulation No 1099/2009 requires that slaughterhouses monitor the efficiency of stunning and prescribes several conditions with regard to the waterbath equipment: birds may not hang on the shackles for longer than 1 min when they are still conscious, the waterbath should be provided by an electrically insulated entry ramp, overflow of water at the entrance of the waterbath should be prevented, the height of the waterbath needs to be adjustable to the size of the birds, and there has to be a system that makes contact with the breast of the birds to prevent wing flapping from the moment of shackling until the entrance of the waterbath (European Union, 2009). Several slaughterhouses did not fulfill one or more of these criteria. However, it should be noted that until 2019 December 8 these conditions only apply to new slaughterhouses or to new equipment that is installed in already existing slaughterhouses. The European Regulation also requires that slaughterhouses monitor the efficiency of stunning but do not state which indicators they should use for this purpose (European Union, 2009). When such monitoring took place in the visited slaughterhouses, a variety of parameters were used to assess unconsciousness in the birds, without any kind of uniformity between the slaughterhouses. In the majority of the slaughterhouses, the neck cut was performed bilaterally resulting in severing of the major blood vessels to the brain, and consequently the birds die through loss of blood supply to the brain (EFSA, 2012). In the remaining slaughterhouses, only 1 jugular vein and 1 carotid artery were severed (unilateral neck cut). Although it was not observed in the present study, cutting the back of the neck is another alternative in which case one or more vertebral arteries

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DEVOS ET AL.

are severed, but none of the carotid arteries are severed that increases the risk of resumption of consciousness during bleeding, and the time needed to kill the birds is relatively long (Gregory and Wotton, 1986; Gregory, 1998). When comparing an unilateral cut with a bilateral cut, severing both carotid arteries is preferred as the onset of brain failure is faster (Gregory and Wotton, 1986)

Survival Rate after Electrical Waterbath Stunning It was clear that a lot of variation existed in the amount of electrical current, not only between slaughterhouses but also between the visits to the same slaughterhouse. When electrical waterbath stunning is being applied, the European Regulation No 1099/2009 prescribes that each chicken has to receive a minimum average electrical current of 100, 150, or 200 mA when frequencies of less than 200 Hz, from 200 to 400 Hz, or from 400 to 1,500 Hz are used, respectively (European Union, 2009). When considering the average electrical current of all tested animals within a certain poultry type and slaughterhouse, only 2 slaughterhouses currently seem to reach this legal requirement. However, the individual data showed a large spread, and a certain proportion of the broilers in these 2 slaughterhouses received an electrical current that was below the required minimum level. Only the broiler breeders and ISA laying hens in one of these 2 slaughterhouses all received an electrical current level that attained the European requirements. A possible explanation for this observation could be that most of the broilers in the visited slaughterhouses were ritually slaughtered, implying that technical settings were selected to induce unconsciousness in the animals without killing them. On the other hand, all the broiler breeders and laying hens were not ritually slaughtered, possibly explaining why they received a higher electrical current. Because high voltages or low frequencies are associated with more carcass quality defects (Barbut, 2002), it could be that slaughterhouses applied milder stunning settings for broilers than for both laying hens and broiler breeders. According to the same regulation, animals need to be exposed to the electrical current for a minimum duration of 4 s. All visited slaughterhouses in this study met that requirement. In the present study, the survival rate ranged from 96 to 100%, 97 to 100%, 68%, 72 to 85%, and 6 to 52% in 5-wk-old broilers, 6-wk-old broilers, LSL laying hens, ISA laying hens, and broiler breeders, respectively. The mortality rate, due to electrical stunning, reported in previous studies showed a wide range from 0 to 99% in both broilers and laying hens (Gregory and Wotton, 1987, 1994; Gregory et al., 1991; Wilkins et al., 1998; Raj et al., 2006b; Hindle et al., 2010). As already mentioned above, the observed high survival rate in broilers

in the present study could be due to the fact that a large part was ritually slaughtered or because the settings were chosen in order to obtain an acceptable carcass quality. The application of a frequency of 50 Hz led to a lower survival rate in both LSL and ISA laying hens. Low frequencies are associated with an increased risk of inducing ventricular fibrillation, leading to cardiac arrest (Kettlewell and Hallworth, 1990). Increasing the stunning current may lead to an increased incidence of ventricular fibrillation (Gregory et al., 1991), which could explain the lower survival rate in broiler breeders that received a higher average individual electrical current.

General Conclusion It was concluded that a large variation in slaughter and stunning practices exists among slaughterhouses in Belgium. Further research should explore the effect of the different settings on inducing a successful stun and on carcass quality, and explore if the observed variation also exists in other EU member states.

ACKNOWLEDGMENTS This research was funded by the Belgian Federal Public Service Health, Food Chain Safety and Environment and the Department of Environment & Spatial Development (formerly the Environment, Nature and Energy Department (LNE)) of the Flemish government through contract RF 13/6275 VERDO-KIP.

REFERENCES Barbut, S. 2002. Stunning of poultry. Pages 109–127 in Poultry Products Processing: An Industry Guide. S. Barbut, ed. CRC Press, Boca Raton, FL. beSTAT-FOD economie. 2017. Slachtstatistieken. Accessed Sept. 2017. http://statbel.fgov.be/nl/statistieken/cijfers/economie/ landbouw/verwerking/geslacht/. Bilgili, S. F. 1999. Recent advances in electrical stunning. Poult. Sci. 78:282–286. Cenci-Goga, B. T., C. Mattiacci, G. De Angelis, P. Marini, A. Cuccurese, R. Rossi, and B. Catanese. 2010. Religious slaughter in Italy. Vet. Res. Commun. 34 Suppl 1:139–143. EFSA. 2004. Opinion of the Scientific Panel on Animal Health and Welfare on a request from the Commission related to welfare aspects of the main systems of stunning and killing the main commercial species of animals. EFSA J. 45:1–29. EFSA. 2012. Scientific opinion on the electrical requirements for waterbath stunning equipment applicable for poultry. EFSA J. 10:2757–2837. European Commission. 2013. Report from the Commission to the European Parliament and the Council on the various stunning methods for poultry. Accessed Oct. 2017. https://ec.europa.eu/food/sites/food/files/animals/docs/aw practice slaughter com 2013 915 report en.pdf. European Commission. 2015. EU Market Situation for Poultry - Committee for the Common Organisation of the Agricultural Markets 19 February 2015. Accessed May 2017. http://ec.europa.eu/agriculture/sites/agriculture/files/russianimport-ban/pdf/russian-ban-meat-19-02-2015-poultry en.pdf. European Union. 2009. Council Regulation (EC) No 1099/2009 of 24 September 2009 on the protection of animals at the time of killing. Off. J. Eur. Union L303:1–30.

Downloaded from https://academic.oup.com/ps/advance-article-abstract/doi/10.3382/ps/pey181/4999969 by University of Winnipeg user on 24 May 2018

ELECTRICAL WATERBATH STUNNING OF POULTRY FASFC. 2014. Lijst erkende inrichtingen. Accessed Febr. 2014. http://www.afsca.be/bo-documents/inter inricht levensmid N.PDF. Gentle, M. J., and V. L. Tilston. 2000. Nociceptors in the legs of poultry: Implications for potential pain in pre-slaughter shackling. Anim. Welf. 9:227–236. Gerritzen, M. A., B. Lambooij, H. Reimert, A. Stegeman, and B. Spruijt. 2004. On-farm euthanasia of broiler chickens: Effects of different gas mixtures on behavior and brain activity. Poult. Sci. 83:1294–1301. Gregory, N. G. 1989. Stunning and Slaughter. Pages 31–63 in Processing of Poultry. G. C. Mead, ed. Elsevier Applied Science, London, NY. Gregory, N. G. 1995. Stunning and Slaughter. Pages 31–45 in Processing of Poultry. G. C. Mead, ed. Springer US, Boston, MA. Gregory, N. G. 1998. Stunning and Slaughter. Pages 223–240 in Animal Welfare and Meat Science. N. G. Gregory, ed. CABI Publishing, Oxon, UK; New York, NY, USA. Gregory, N. G., and J. C. Bell. 1987. Duration of wing flapping in chickens shackled before slaughter. Vet. Rec. 121:567–569. Gregory, N. G., L. J. Wilkins, and S. B. Wotton. 1991. Effect of electrical stunning frequency on ventricular fibrillation, downgrading and broken bones in broilers, hens and quails. Br. Vet. J. 147:71– 77. Gregory, N. G., and S. B. Wotton. 1986. Effect of slaughter on the spontaneous and evoked activity of the brain. Br. Poult. Sci. 27:195–205. Gregory, N. G., and S. B. Wotton. 1987. Effect of electrical stunning on the electroencephalogram in chickens. Br. Vet. J. 143:175–183. Gregory, N. G., and S. B. Wotton. 1994. Effect of electrical stunning current on the duration of insensibility in hens. Br. Poult. Sci. 35:463–465. Heath, G. B. S., D. J. Watt, P. R. Waite, and J. M. Ormond. 1981. Observations on poultry slaughter. Vet. Rec. 108:97–99. Hindle, V. A., E. Lambooij, H. G. M. Reimert, L. D. Workel, and M. A. Gerritzen. 2010. Animal welfare concerns during the use of the water bath for stunning broilers, hens, and ducks. Poult. Sci. 89:401–412. Kettlewell, P. J., and R. N. Hallworth. 1990. Electrical stunning of chickens. J. Agric. Eng. Res. 47:139–151. Lambooij, E., H. G. M. Reimert, and V. A. Hindle. 2010. Evaluation of head-only electrical stunning for practical application: assessment of neural and meat quality parameters. Poult. Sci. 89:2551–2558.

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Lambooij, E., H. G. M. Reimert, M. T. W. Verhoeven, and V. A. Hindle. 2014. Cone restraining and head-only electrical stunning in broilers: Effects on physiological responses and meat quality. Poult. Sci. 93:512–518. Lines, J. A., A. B. M. Raj, S. B. Wotton, M. O’Callaghan, and T. G. Knowles. 2011. Head-only electrical stunning of poultry using a waterbath: a feasibility study. Br. Poult. Sci. 52:432–438. Perez-Palacios, S., and S. B. Wotton. 2006. Effects of salinity and the use of shackle/leg sprays on the electrical conductivity of a commercial waterbath stunner for broilers. Vet. Rec. 158:654–657. Raj, A. B. M., M. O’Callaghan, and S. I. Hughes. 2006a. The effects of amount and frequency of pulsed direct current used in water bath stunning and of slaughter methods on spontaneous electroencephalograms in broilers. Anim. Welf. 15:19–24. Raj, A. B. M., M. O’Callaghan, and S. I. Hughes. 2006b. The effects of pulse width of a direct current used in water bath stunning and of slaughter methods on spontaneous electroencephalograms in broilers. Anim. Welf. 15:25–30. Raj, A. B. M., M. O’Callaghan, and T. G. Knowles. 2006c. The effects of amount and frequency of alternating current used in water bath stunning and of slaughter methods on electroencephalograms in broilers. Anim. Welf. 15:7–18. Raj, A. B. M., and A. Tserveni-Gousi. 2000. Stunning methods for poultry. Worlds Poult. Sci. J. 56:291–304. Sch¨ utt-Abraham, I., H.-J. Wormuth, and J. Fessel. 1987. Vergleichende Untersuchungen zur tierschutzgerechten Elektrobet¨ aubung verschiedener Schlachtgefl¨ ugelarten. Berl. Munch. Tierarztl. Wochenschr. 100:332–340. Sparrey, J. M., P. J. Kettlewell, M. E. R. Paice, and W. C. Whetlor. 1993. Development of a constant current water bath stunner for poultry processing. J. Agric. Eng. Res. 56:267–274. Velarde, A., P. Rodriguez, A. Dalmau, C. Fuentes, P. Llonch, K. V. von Holleben, M. H. Anil, J. B. Lambooij, H. Pleiter, T. Yesildere, and B. T Cenci-Goga. 2014. Religious slaughter: evaluation of current practices in selected countries. Meat Sci. 96:278–287. Wilkins, L. J., N. G. Gregory, S. B. Wotton, and I. D. Parkman. 1998. Effectiveness of electrical stunning applied using a variety of waveform-frequencycombinations and consequences for carcase quality in broiler chickens. Br. Poult. Sci. 39:511–518. Wilkins, L. J., S. B. Wotton, I. D. Parkman, P. J. Kettlewell, and P. Griffiths. 1999. Constant current stunning effects on bird welfare and carcass quality. J. Appl. Poult. Res. 8:465–471.

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