Female cattle slaughter and foetal wastage: A case study of the Lafenwa abattoir, Ogun state, Nigeria

Abstract In developing countries, indiscriminate slaughtering of pregnant ruminants and consequent foetal wastage (FW) are persistent practices, which have impacted the agricultural and economic advancement of such countries. Retrospective data from 2008 to 2016 of a municipal slaughterhouse in Ogun state, Nigeria was assessed for the current patterns of female cattle (FC) slaughter and FW. A total of 353,503 (mean/year: 29,457 ± 1651) FC were slaughtered, and 44,713 (12.65%; mean/year: 3,726 ± 584) FW estimated over a period of 9 years. There were significant yearly variations in throughput of FC and FW (p < 0.0001), and a strong and positive correlation between FC and FW (r = 0.74, p = 0.006). We report a significant increase in FC slaughter and FW. Action plans such as awareness programs among livestock stakeholders, review on slaughter reforms, enforcement of policies that encourage realistic and positive attitude geared towards sustainable livestock practices, animal welfare, food security, and prohibition of pregnant animal slaughtering are required.


PUBLIC INTEREST STATEMENT
The livestock industry in Nigeria has grown to about 19.5 million cattle, 115 million sheep and goat, and 160 million poultry according to the national agriculture resource survey, 2016. However, the country still struggles to meet the growing demand of an increasing population to animal meat proteins, while ending hunger, achieving food security, improving nutrition and sustainable agriculture by the year 2030 through the UN SDG 2 strategic objectives appearing unattainable. Our study provided information on a nine-year retrospective record of foetal wastage and female animal slaughter in a major abattoir in Nigeria and report the persistence of these practices. Foetal wastages significantly impact herd size negatively, and careful planning and formulation of policies through appropriate evidence-based approach are needed in livestock production management. Developing educational intervention strategies for livestock industry stakeholders and mechanisms to facilitate early detection of pregnant animals and the establishment of appropriate standards of best practices are required.

Introduction
Nigeria is endowed with ruminant livestock resources, e.g., cattle, sheep, and goat, which are estimated at 19.2 million, 38.5 million and 57.4 million, by Food and Agriculture Organization [FAO] (2014), respectively. The livestock annual growth rates are low to satisfy the requirements of the everincreasing human population of over 170 million (Alhaji et al., 2015). Although the amount of livestock production in Nigeria and other developing countries has marginally increased on average, persistent malnutrition and low intake of good quality animal protein (individual protein dietary intake is less than 9 kg, well below the United Nation's Food and Agricultural Organization-FAO (2013) recommendation of 41.9 kg/person) continues to be a significant public health threat especially in children (Müller, 2005;Schonfeldt & Hall, 2012). Malnutrition has been associated with a high prevalence of more than 80% infectious diseases (e.g., malaria, tuberculosis, measles, and HIV/AIDS), over 300,000 deaths, and about half of all mortalities in young African children (Müller, 2005).
Agricultural sustainability strategy such as mitigation of slaughtering of pregnant food animals in many developing countries needs to be addressed as a priority to increase the availability of quality animal protein. Although slaughtering of pregnant food animals and the fate of unborn foetuses are relatively new in the field of animal welfare, it has, however, gained importance in public debates globally (Maurer et al., 2016). Foetal wastage has primarily been related to substantial economic losses; scientific reports that foetuses can feel stress and pain from the second half of the gestation on (Bellieni & Buonocore, 2012;Maurer et al., 2016;More et al., 2017), and that globally, large numbers of abattoirs still slaughter pregnant animals. The magnitude of the slaughter of pregnant animals and consequent embryo losses has also been reported in Europe countries (More et al., 2017). The prevalence is, however, higher in African countries ranging from 1.3% to 45% (Nonga, 2015). In Nigeria, the magnitude of pregnant female cattle slaughter and the foetal wastage has been reported by several authors (Addass et al., 2010;Alhaji, 2011;Alhaji et al., 2015;Awoyomi et al., 2013;Cadmus & Adesokan, 2010;Ngbede et al., 2017;Nwakpu & Osakwe, 2007;Ogunbodede & Oladele, 2016;Raimi et al., 2017). Also, the associated economic losses have been estimated close to US$290 000 (Ngbede et al., 2017) and US$18,442,883.52 (Awoyomi et al., 2013).
To date, FW in Nigerian abattoirs is yet to be addressed by the industry stakeholders. Policies to ensure animal welfare, the prohibition of slaughtering of pregnant animals and protection of unborn foetuses are yet not given cognisant considerations. Only one study in central Northern Nigeria provided detailed information on the seasonal trend analysis of ruminant foetal wastage (Alhaji et al., 2015). The data provided in this present study would assist to develop a guide to future policy formation and strategic action plans for ensuring high animal welfare standards, protection of unborn animal foetuses and sustainable livestock practices.

Study location
The municipal slaughterhouse (SH) investigated is located in Abeokuta North local government area (latitude 3°19.665ʹE and longitude 7°09.775ʹN and has an area of 16,400 KM 2 ), Ogun State, Nigeria. Abeokuta's population is currently estimated at 532,856. Ogun borders Lagos State to the south, Oyo and Osun states to the north, Ondo to the east and the Republic of Benin to the west. Abeokuta is the capital and largest city in the state. The state's appellation is "Gateway to Nigeria", and was created in February 1976 from the former Western State. The 2006 National population census estimated the human population at 3,751,140.

The slaughterhouse layout
The slaughterhouse (SH) was an enclosed premise, which consisted of necessary facilities such as a lairage, meat markets, administrative block, veterinary officer post, slaughter slabs. Hygiene amenities, e.g., cooling room, hand washing, changing rooms and toilets, cleaning and disinfection of the abattoir premise, and animal waste management were inadequate or non-functional. Solid and liquid wastes were disposed of within and around receiving surface water banks, which also served as the source of water for meat processing.
The lairage, situated about 500 m North East (Lat: 7° 10ʹ 02.30" and Long: 003° 19ʹ 36.79") of the SH, received and rested trade cattle-at least 24 hours before slaughter. The SH at its full operations processes at least a total number of 150-200 heads of cattle daily, and supplies meat to the public within and around Abeokuta environs (Adebowale et al., 2016). Antemortem inspection and treatment of sick animals were performed within the lairage by veterinary officers in line with the Nigerian meat edict of 1978 to ensure animal health status before slaughter. The lairage led to two slaughter slabs-enclosed and open slaughter slabs, where floor processing and mixed operations (clean and dirty) were still common practices. Herein, post-mortem meat inspections were carried out by qualified veterinarians and para-veterinarians. The routine inspection protocol employed included visual inspection, palpation, and incision of visceral organs. Afflicted organs were routinely condemned partially or totally based on the extent of infection and veterinary personnel's judgment.
Veterinary officers were present at SH from 7 a.m. (commencement of animal slaughtering) to 11 a.m. (end time for slaughtering) from Mondays to Saturdays. Available data showed a decrease in total of the animal slaughtered yearly. For instance, there was 11.8% decrease in throughput of animals killed in 2016 compared to 2014 of which the economic recession and high costs of livestock production in the country may have contributed to this. There were eight veterinarians fully assigned for meat inspection at the SH. The veterinarian to animals slaughtered ration 1:10. Bovine is the only livestock specie killed in the SH.

Data source and collection
Our study at this moment investigated the current patterns and seasonal associations of foetal wastages at a municipal slaughterhouse in Ogun State, Nigeria. The study involved the following: 1). Visits and inspections the facility; 2). Collection of the 9-year historical data (2008-2016), and 3). Analysis of patterns of FC slaughter and FW. For this study, a retrospective slaughterhouse (SH) study design was employed. Secondary data on the number of female cattle animals' (FC) slaughtered and foetal wastage (FW) from 2008 to 2016 were obtained from abattoir records provided by the Veterinary Department services, Ogun State Ministry of Agriculture. The data were considered suitable based on records of various parameters (FC slaughtered and FW) under investigation presented by the veterinary department. To better understand the pattern in FW about seasons, the months were divided into early dry, early rainy, late rainy, and late dry, according to Alhaji et al. (2015). Seasons were defined as groups of months, with a). Late dry: January to March, b). Early rain: April to June, c). Late rain: July to September, and d). Early dry: October to December.
Information on the number of pregnant animals slaughtered during this period was not available from the abattoir records provided by the department of veterinary services. Researchers visited the abattoir facility and noted its location, layout, facilities, and processes.

Data analysis
Data were entered into Excel spreadsheet (2016) and exported into computer statistical analysis software GraphPad Prism 8.0 for further analysis. For the descriptive statistics, the total number of female cattle animals (FC) slaughtered and foetal wastage (FW) from 2008 to 2016 were computed. The annual, monthly, and seasonal frequencies of both variables (FC slaughtered and FW) were estimated. Descriptive rates of distribution were presented as line graph plots with the standard error of the mean to demonstrate the data variability. One-way ANOVA or Kruskal-Wallis tests were used to compare the mean variations in numbers of FC slaughtered and FW annually, monthly and seasonally. For further comparisons, Dunnett's multiple tests were performed using the year 2008 and month January as references due to their lowest record rates of FW. Differences were considered statistically significant at P < 0.05.
Prior all analyses normality tests of datasets were carried out using Shapiro-Wilk test and Kolmogorov-Smirnov test (p >.05). Where datasets violate the assumption of normality, a nonparametric Kruskal-Wallis test was used.  Tables 1 and 2). There was a statistically significant variation in the yearly slaughter of animals (p < 0.0001). Figure 1(a and b) show the annual and monthly distributions of FC slaughtered during this study period. The seasonal pattern of slaughtering showed FC were most killed during the early dry (93,173; mean 10,353 ± 1165), and lowest during the late dry seasons (84,265, mean 9363 ± 2056). However, no seasonal effect was observed (p = 0.28). Figure 1(c) presents the seasonal pattern in FC slaughtered.

Foetal wastage data
Between 2008 and 2016, the total number of foetal wastage (FW) estimated was 44,713 (mean 3726 ± 584 per year). The prevalence of FW was estimated at 12.6% based on the total number of female animals slaughtered during the period of investigation. For every eight FC slaughtered, one foetal wastage was reported. The highest throughput of FW was observed for 2016 (5,699, mean 475 ± 67) and the month August (4,398, mean 489 ± 61; Tables 1 and 2). There was a statistically significant variation in yearly (p < 0.0001) and monthly wastage (p = 0.0007). FW was significantly higher in August (p = 0.02) and October (p = 0.03). An upward trend in FW across the years was observed except in 2011 and 2012. Figure 2(a and b) are the yearly, and monthly distributions of FW investigated in this study. The seasonal pattern of FW was highest during the late rains (12,485, mean 462 ± 82) and lowest in the late dry (9,587; mean 360 ± 99). A seasonal effect was observed with p = <0.0001. The scatter plot showed a strong, positive, statistically significant monthly correlation between FC slaughtered and FW (r = 0.74; 95% CI = 0.28 to 0.92; p = 0.006). Figure 2(c) shows the seasonal pattern of FW and Figure 2(d) presents the relationship pattern between FC and FW.

Economic implication of foetal wastage
The economic implication of the foetal wastage was estimated for the total number of foetal wastage by the amount worth in Naira (₦) if foetuses were allowed to grow into adults. An adult cattle of about 250 kg costs ₦ 230,000. So, for a period of 9 years, a total of₦ 1,142,640,000 ($ 2,943,886.22) and ₦ 94,530,000 ($ 234,546.14) annually are lost. The current exchange rate is 1 USD to ₦ 388.14

Pattern of female cattle slaughtering
This study was conducted to determine the pattern of female cattle (FC) slaughter and foetal wastage practice in a slaughterhouse (SH) in Southwestern Nigeria. Our findings revealed that the ratio of female to male animals slaughtered in the SH was 5:1, i.e., female cattle animals are five times more likely to be slaughtered than male. Several studies within Nigeria ( Ogunbodede & Oladele, 2016; Baba et al., 2018). The heterogeneous data on the female animal slaughter in the different studies can be attributed to firstly, variations in study designs, especially investigation periods. Secondly, the production management system types, i.e. whether intensive or highly extensive, may be factors for high rates of female animals and subsequent pregnant ones presented for slaughter. Female animals raised in an intensive management system, especially for milking, breeding, or meat production are less likely to be sent for slaughter except where there are health or reproductive issues. However, in many developing countries, including Nigeria where extensive rearing systems are practised with no controlled breeding, no records and diagnostic tools for early pregnancy detection, selling of female animals and pregnant ones for slaughtering are usually high (Alhaji et al., 2015;Hassan et al., 2016). On-farm diagnostic facilities for early detection of pregnant animals are absent, and routine pregnancy diagnoses may not be performed or documented as most cattle rearers in Nigeria are nomads or pastoralists with little or no education. To promote, sound economic livestock management and sustainability in developing countries, animals presented at abattoirs for slaughter should be males, and reproductively inactive females (Fayemi & Muchenje, 2013). Also, cattle farmers, especially the nomads, can be educated on and provided with userfriendly rapid test kits at subsidised rates by the government to ascertain pregnancy status of female animals before selling off to the abattoirs. The slaughtering of high rates of female animals which are maybe a key predictor for foetal wastage has consequent impacts on livestock industry productivity, sustainability (as more females are required in reproductive and milk production processes than males), and food security in Nigeria. This practice has been observed as a critical factor for protein malnutrition in African countries and a possible constraint to future livestock populations on the continent (Fayemi & Muchenje, 2013)  The total throughput of FC slaughtered reported in this study during 9 years was 353,503 (mean 29,457 ± 1,651). Comparing our data with a previous study conducted by Cadmus and Adesokan (2010), there was a decreased pattern in the number of FC slaughtered at the slaughterhouse. The decrease may be attributed to the current economic crisis faced by the country, which has resulted in high livestock management and production costs. We observed FC slaughter peaked in 2015 and especially in December (characterised by high sales due to Christmas festivities and ceremonies) but declined again by 12.5% in 2016. Although there was no seasonal effect on the FC slaughtered, the annual trend indicated FC slaughter occurred most times during the early dry, i.e. October-December (93 173; mean 10,353 ± 1165). The outcome is not surprising as other authors have reported similar pattern at different abattoirs in past studies (Cadmus & Adesokan, 2010;Ngede et al., 2012;Alhaji et al., 2015;Hassan et al., 2016;Raimi et al., 2017). Sales and butchering of female animals and consequent slaughtering of pregnant females becomes higher at the late rains and as the dry season progresses because, during drought season, sparse feed supply, dangers of poor nourishment, loss of body conditions, diseases and death become intense mostly due to trypanosomosis. A reduction in slaughtering during the late dry (January-March) compared with other seasons was observed similar to what was described by Cadmus and Adesokan (2010) for the slaughterhouse. However, this was contrary to what we anticipated, as explained previously. One explanation for this is that more cows are disposed to mating and conceiving during rainy seasons because of feed lush, which results in calving during the next early rainy season when there is abundant food for them and their offspring (Ngbede et al., 2017). Pregnancies at the late stage may then be evident to farmers, who would prefer to keep the heifers to calve, and nourish their young ones during the next early rains, and also to generate more profits.

Foetal wastage patterns
The data revealed that 12.6% of foetuses were wasted based on the total number of female animals slaughtered in the period between 2008 and 2016. This outcome is similar to a few previous studies that were conducted in the year 2013 at the same slaughterhouse investigated. Oduguwa et al. (2013) and Awoyomi et al. (2013) reported a 10.7% and 10.3% foetal wastage within a three-month retrospective and one-year prospective surveys, respectively. A similar outcome was observed in an abattoir in Ebonyi, and Yola states, Nigeria (9.2%, Nwakpu & Osakwe, 2007 and 14.4%;Ardo et al., 2013), Kumasi, Ghana (18.4%, Atawalna et al., 2013), Bukoba Municipal abattoir, Tanzania (15.6%, Nonga, 2015. Furthermore, the prevalence of FW from our study was twice those reported by Cadmus and Adesokan (2010) at 6% for the same SH. The length of study (2005)(2006)(2007), lapses and poor practices in record keeping due to inability to identify cases of foetal loss may have contributed (Cadmus & Adesokan, 2010) to this discrepancy. Also, the population of slaughtered cattle may have increased from the time of the study (Cadmus & Adesokan, 2010) to 2018. Lower rates of FW compared to what our data indicated have also been documented by other authors from different locations in Nigeria. Data as low as 2.4% (Benue; Adeyemi et al., 2016); 3.9% (Benue; Abdulkadir et al., 2008); 3.8% (Minna; Adama et al., 2011);4.5% (Minna;Alhaji et al., 2015); 4.5% (Jos; Dunka et al., 2017) Mutwedu et al. (2019) in the Democratic Republic of Congo recorded a fetal recovery rate of 26.3% (over twice observed in our study). The diverse data on foetal wastage in different parts of the country may be explained similarly as previously described for FC. Firstly, variations in study designs and investigation periods. Secondly, the production management system type, highly extensive may be factors for high rates of pregnant animals presented for slaughter and subsequent foetal loss. Thirdly, best practices and standards in record keeping may have varied from one abattoir to another, which may have introduced bias in the observed trends and seasonality. Fourthly, studies of mating and conception patterns have not been linked to pregnancy age and seasonal as well as migratory patterns of herders, as transit can take months on the hooves, from the north of the country to the south, with pockets of lush vegetation increasing conception along the way.
Our analytic study investigated foetal wastage across seasons. The data indicate that female cattle animal (FC) slaughter was highest during the early dry, while foetal wastage (FW) was significantly elevated during the late rains (p = <0.0001) and early dry (p = 0.0008) compared with the late rains when there was the least wastage. This observation was slightly varied from what has been reported by previous studies which concluded that foetal losses amongst cattle occur more often in the dry seasons in slaughterhouses and abattoirs across Nigeria (Cadmus & Adesokan, 2010;Ngbede et al., 2017;Nwakpu & Osakwe, 2007).
The seasonal component of study by Alhaji et al. (2015) reported a single peak (≤7%) per year, with the highest foetal wastage rates observed from the middle to later months of the year (May-October, i.e. early rains through the early dry). Another study, which was a year incidence report by Awoyomi et al. (2013), did not report any seasonal association with FW. This period may be too short to detect any seasonal change in the incidence of foetal wastage. We should also bear to mind that many factors may come to play in the differences in seasonality's in FC slaughtered and FW reported. Seasonal drifts may be affected by various circumstances such as record-keeping practices, occasions, and festivities, economic status and improved living standards, as well as uncertainties and risks such as drought, diseases and animal movements by pastoralists for greener pastures (Alhaji et al., 2015). Another logical reason, especially for more FW at early dry and late rains, may be correlated to high numbers of female animals and subsequent slaughtering of pregnant ones during this period.
The economic losses associated with indiscriminate slaughtering of pregnant animals in abattoirs in Nigeria have been quantified and reported to be huge (running into millions of dollars annually) and findings from this study support other previous findings in the country and other African countries (Alhaji & Odetokun, 2013;Awoyomi et al., 2013;Bokko, 2011;Nma, 2011;Nonga, 2015;Tamirat et al., 2015). The cyclic trends and patterns of pregnant animal slaughtering and subsequent foetal wastage will continue until improvements in legislation/ policies and best standard practices for abattoirs concerning meat inspections and animal welfare are enhanced in the country. This study further underscores the need to enforce legislation and policy currently existing, to prevent foetal wastage and ensure adherence by farmers. Also, the need to improve on antemortem diagnostic skills and facilities for early detection of pregnant animals, especially at first trimesters is essential. Further, estimation of meat protein loss and economic impact of FW, i.e. monetary, should be comprehensively examined.

Conclusions and recommendations
The study indicated indiscriminate slaughter of FC persists as a widespread practice in abattoirs in Nigeria. This practice may impact the productivity and sustainability of livestock and by implication, the livestock industry in the country. Further, inadequacies in routine antemortem facilities and veterinary inspection of animals, which are crucial for early detection and mitigation of pregnant animals slaughtering are highlighted. Also, this study indicates that data and surveillance systems for tracking FC slaughter and FW to help develop effective mitigation plans to prevent pregnant FC slaughter and FW in the country are inadequate. To meet the country's animal protein demand by the ever-increasing human populations, there is an urgent need for educational intervention to create awareness for livestock farmers and industry stakeholders on the extent of the problem especially the economic and public health consequences. Animal welfare policies and strategies that prohibit indiscriminate pregnant animals slaughter, enforced and implemented with incentives or penalties, are urgently needed. Mechanisms to facilitate the early detection of pregnant animals (including adequate training, establishment and implementation of appropriate standards of best practices) and prevent inappropriate slaughtering are also needed.