Risk factors for stillborn pigs and mummified fetuses in two swine farms in southeastern Mexico

The objective of this study was to determine risk factors of stillbirth and mummified fetuses in 42,648 litters from two commercial pig farms in southeastern Mexico. Stillborn pigs were observed in 28.9% of the litters and the pig stillbirth incidence was 2.84%. Mummified fetuses occurred in 22.2% of the litters and the incidence was 2.36%. Data of litters with at least one stillborn pig and at least one mummified fetus were analyzed using binary logistic regression models. The categorical risk factors were farm (1 and 2); year of farrowing (2008 to 2012); season of farrowing (dry, rainy and windy); and parity number (1, 2,…, >7). Litter size was included as a continuous covariate (1 to 25 pigs).

The odds of mortality were greater in farm 2 as compared with farm 1 for litters with stillborn pigs or mummified fetuses. Year of farrowing, season of farrowing, parity number and litter size were significant (P < 0.01) risk factors for the occurrence of mummified fetuses; however, season was not significant for stillborn pigs (P > 0.01). Sows of parities ≥ 5 had higher odds of stillbirths than sows with lower parities. However, sows with 5 and 6 parities had higher odds of mummified fetuses in comparison to other parities (P < 0.05). The odds of a pig born death or a mummified fetus increased as liter size increased (P < 0.01). In conclusion, this study showed farm and parity number effects on stillborn pigs and mummified fetuses; season differences in the occurrence of at least one mummified fetus in the litter; and higher risk of stillbirth and mummified fetus as litter size increased.

Introduction

Genetics has improved litter size of sows; however, high prolificacy is associated with high occurrence of stillbirths and of mummified fetuses, which are important causes of pig losses in commercial swine herds (Dial et al 1992). The rate of pigs born dead in total pig born vary from 5 to 15% (Van der Lende 2000; Koketsu et al 2010), which is a very wide range. This means that in order to establish better management practices to reduce mortality rate, the parameter for each farm should be known. Also, several factors have been associated with stillbirth like litter size, infectious diseases, gestation length, parity number, farrowing length, farrowing interval, dystocia, high environmental temperature, body condition score and nutritional deficiencies (Leenhouwers et al 1999; Tantasuparuk et al 2000; Lucia Jr et al 2002). The occurrence of mummified fetuses has been associated with litter size, parity, infectious diseases, uterine capacity, environmental temperature and mycotoxins (Dial et al 1992; Mengeling et al 2000; Schneider et al 2003). However, risk factor influence on mortality rates may vary from one farm to another. Identification of the risk factors associated with stillbirth and the occurrence of mummified fetuses can aid in optimizing herd reproductive efficiency. Also, to the authors’ knowledge, there is no information of factors affecting pig mortality at birth or the occurrence of mummified fetuses under the tropical conditions of Mexico. The aim of this work was to estimate the incidence of and to determine some risk factors associated with the occurrence of stillbirth and mummified fetuses in two swine farms in southeastern Mexico.

Material and methods

Location of herds and data

Data were obtained from two full cycle commercial swine farms with breeding-herd inventories of 3,330 and 1200 sows. One farm was located in the south region of the state of Yucatan; Mexico and the other in the central region. Sows were of the Camborough 22 PIC line, ranging from parities one to 8 in farm 1 and from one to 13 in farm 2. The climate of the region is tropical sub-humid with rain during summer, average temperature of 26.6 °C and annual rainfall of 1100 mm. Information on sow identification, date of farrowing, parity of the sow, as well as the occurrence of stillbirth and mummified fetuses, were extracted from the records kept at the two farms in the PigChamp program, from 2008 to 2012. Sows were kept in open houses and during gestation and lactation they were kept in individual crates. From weaning to service the sows were kept in group pens.

Sows were fed commercial feed according to the productive stage. Fist parity sows (about 200 kg) were given approximately 2.6 kg/day of a feed with 3,000 kcal EM/kg, 16% crude protein and 0.8% lysine; whereas the sows with 300 kg body weight received 3.2 kg/day of feed. Both farms provide similar feeding programs. Sows were vaccinated against mycoplasma, leptospira, parvovirus, erisypelas, circovirus, hemophillus parasuis and E. coli pathogens. The region is free of aujesky’s disease, classic swine fever and influenza disease.

Data regarding year and month of parity, parity number, litter size at birth, stillborn and mummified fetuses were used. No etiological diagnosis was made in stillbirth or mummified fetuses. Stillbirth was defined as a pig born dead or dying within 24 h after birth. Litter size included pigs born alive, stillborn and mummified.

Dependent variables (stillborn or mummified fetus) were categorized as 1, if there were at least one stillborn pig or mummified fetus in the litter. Descriptive statistics were generated by the UNIVARIATE procedure (SAS 2008). The dependence or independence of both traits was tested with the chi-square test using the FREQ procedure (SAS 2008). The association of the risk factors with sows having at least one stillborn pig or mummified fetus was determined by binary logistic regression analysis (SAS 2008). Potential risk factors included in the models as categories were: herd (1 and 2); year of farrowing, season of farrowing (dry season and windy); parity (1, 2,…,7 and >7). Litter size (range 1 to 25 piglets) was included as a continuous covariate. Data on sows with >7 parities were categorized in one group because of the small number of observations.

The probabilities of at least one stillborn or mummified fetus for litter sizes from 1 to 20 were calculated using the formula:

Where: a is the intercept; bi the value of the regression coefficients for the ith risk factor and Xi is the matrix of incidences.

Probabilities were calculated fixing sows from parity 1, from farm 2, farrowing in 2012, and in the windy season. Graphs were built using Excel software.

Results

Stillborn pigs and mummified fetuses were observed in 28.9% and 22.2% of the 42,648 litters, and the incidence rates were 2.84% and 2.36%, respectively. The frequencies of litters with 0, 1, 2 and 3 or more stillbirths were 71.1, 21.4, 1.4 and 0.39%, respectively. The values for mummified fetuses were 77.8, 16.7, 3.92 and 0.60%, respectively. 58.8% of the litters had zero stillbirths or mummies and 8.8% of the litters had both stillbirths and mummies. The chi-square test found a significant association between those two variables (P<0.01).

Tables 1 and 2 show the regression coefficients, the odd-ratios and the 95% confidence intervals resulting from the binary logistic regression analysis used to evaluate the association of the risk factors and stillbirth and mummified fetuses. Significant factors in the logistic regression analysis for stillbirth were farm, year of farrowing, parity number and litter size, plus season of farrowing for mummified fetuses (P<0.05).

Table 1. Risk factors associated with litters with at least one stillborn pig in two swine farms in Yucatan, Mexico, using a binomial logistic model.
Factor	Number of litters	Estimate	Standard error	Odds ratio	95% Confidence interval
Farm
1	34299	-0.571	0.029	0.57	0.53, 0.60
2	8349	0		1
Year of farrowing
2008	3152	0.274	0.046	1.32	1.20, 1.44
2009	6502	0.314	0.035	1.37	1.28, 1.47
2010	9972	0.249	0.031	1.28	1.21, 1.36
2011	10899	0.040	0.031	1.04	0.98, 1.11
2012	12123	0		1
Season of farrowing
Dry	13224	0.011	0.027	1.01	0.96, 1.07
Rainy	14201	0.014	0.027	1.01	0.96, 1.07
Windy	15223	0		1
Parity Number
1	10978	0		1
2	8920	-0.072	0.036	0.93	0.87, 0.99
3	7293	-0.053	0.035	0.95	0.89, 1.02
4	5784	0.015	0.037	1.02	0.94, 1.09
5	4601	0.156	0.040	1.17	1.08, 1.26
6	3427	0.393	0.043	1.48	1.36, 1.61
7	774	0.711	0.080	2.04	1.74. 2.38
>7	871	0.945	0.079	2.58	2.22, 3.01

The odds of stillbirths or mummies were higher in farm 2 than in farm 1. In farm 1 the incidence of at least one stillbirth in the litter was 21.9% and 43.6% in farm 2; therefore, the odds of at least one stillbirth in the litter was almost twice for farm 2 compared to farm 1. For stillborn pigs the odds were 1.5 times greater for farm 2 as compared with farm 1. The odds of stillbirths or mummies tend to decrease with year of farrowing (Tables 1 and 2). Season has no effect on the stillbirth trait; however, the odds of mummified fetuses was highest in the rainy season. The odds of stillborn pigs tend to increase with parity number (Table 1). However, the effect of parity number on the presence of at least one mummified pig in the litter does not shown a clear linear effect. The lowest and highest odds for mummified fetuses occurred at parities 3 and 6, respectively. The probabilities of the presence of stillborn pigs or mummified fetuses increased as the litter size increased (Figure 1).

Table 2. Risk factors associated with litters with at least one mummified fetus in two swine farms in Yucatan, Mexico, using a binomial logistic model.
Factor	N	Estimate	Standard error	Odds ratio	95% Confidence limits
Farm
1	34299	-0.206	0.032	0.81	0.77, 0.87
2	8349	0		1
Year (Season) of farrowing
2008	3152	0.229	0.050	1.26	1.14, 1.39
2009	6502	0.355	0.038	1.43	1.32, 1.54
2010	9972	0.225	0.034	1.25	1.17, 1.34
2011	10899	0.186	0.033	1.20	1.13, 1.29
2012	12123	0		1
Season of farrowing
Dry	13224	0.045	0.030	1.05	0.99, 1.11
Rainy	14201	0.117	0.029	1.12	1.06, 1.19
Windy	15223	0		1
Parity Number
1	10978	0	0	1
2	8920	0.125	0.036	1.13	1.06, 1.22
3	7293	-0.008	0.038	0.99	0.92, 1.07
4	5784	0.041	0.040	1.04	0.96, 1.13
5	4601	0.108	0.043	1.11	1.02, 1.21
6	3427	0.135	0.090	1.21	1.01, 1.33
7	774	0.077	0.089	1.15	0.96, 1.36
7	871	0		1.08	0.91, 1.29

Discussion

The percentage of pigs born dead in total pigs born, obtained in this study (5.20%), managed under the tropical condition of Yucatan is within the range of rates (5 to 15%) reported for commercial pig farms in other countries (Van der Lende 2000; Leenhouwers et al 2001; Lucia Jr et al 2002; Borges et al 2005; Lawlor and Lynch 2007; Koketsu et al 2010). Stillbirths and mummified fetuses contributed almost equally to that percentage; however, in other countries the percentage of mummified fetuses had a greater contribution (Koketsu et al 2010).

With respect, to the percentage of stillbirths, the value obtained in this study (2.84%) is higher than the benchmark percentages reported for USA, Canada and Japan (1.63, 2.44 and 1.22%, respectively) by Koketsu et al (2010). Therefore, better management and bio-security measures should be implemented to reduce the percentage of stillbirths in the farms here studied. The frequency of litters with at least one stillbirth (28.9%) was lower than that (31.3%) reported by Borges et al (2005) in Brazil. Assistance at birth can help to increase litter size reducing the rate of stillbirths (Le Cozler et al 2002; Lucia Jr et al 2002).

The percentage of mummified fetuses in this study (2.36%) is lower than the values reported (4.5 to 6%) in USA, Canada and Japan (Koketsu et al 2010). However, those countries reported higher litter sizes than the farms here studied. Commonly, a higher probability of death is observed with increasing litter size. With respect to the incidence of at least one mummified fetus in the litter, the percentage was lower than the 42.1% reported by Borges et al (2005) in Brazil. Differences may be influenced by climatic, genetic, diseases, and management differences between farms or regions.

Benchmarking information by country shows differences in the rates of stillbirth and mummified fetus between farms (Koketsu et al 2010), which reflects differences in climate, management, genetic, diseases and nutrition between system, and prevalent diseases in different countries or regions. Year effect on the response variables here studied has been reported by other authors (Chu 2005; Espitia and Gelíndez 2011). The linear reduction of the odds for stillbirths, which suggest a lower incidence of stillbirth with year) and the trend of lower pig losses with year for mummies found in this study may be explained by better management and improvement of bio-security measurements with time. The effect of season of farrowing on stillbirth or mummified fetuses is less evident. Some authors reported to be found differences between seasons (Chu 2005; Segura-Correa et al 2007), whereas others did not (Espitia and Galíndez 2011). Pig losses associated to season of farrowing are mainly attributed to the effects of temperature and humidity.

The higher odds of stillbirths as parity number increased, agree with the results of other authors (Le Cozler et al 2002; Borges et al 2005; Segura-Correa et al 2007; Weber et al 2009). This may be partially explained by the fact that higher-parity sows usually farrow larger litters (Dial et al 1992; Lucia Jr et al 2002). Also, this association could be attributed to excessive fatness (Muirhead and Alexander 1997; Canario et al 2006) and/or to poor uterine muscle tone that could lead to less efficient labor and prolonged farrowing in older sows (Lucia Jr et al 2002; Canario et al 2006). However, according to Muirhead and Alexander (1997), stillbirth occurrence in greater than parity 5 sows is more influenced by the prolonged farrowing than by large litter size. Other authors have reported a higher rate of stillborn pigs for parity 1 and for parity 5 or greater in comparison to sows of parity 2 to 5 (Borges et al 2005). Canario et al (2006) mentioned that the increased likelihood of stillborn pigs in parity 1 sows might be due to insufficient size of the birth canal in the young gilts. The trend to lower odds for stillbirths in parity 2, observed in this study, it is probably explained by the lower litter size at that parity, as result of the phenomenon known as the second-litter syndrome (a smaller litter size in the second litter as compared with the first litter of a sow).

The higher odds of stillborn pigs for large litters agree with other studies (Muirhead and Alexander 1997; Leenhouwers et al 1999; Lucia Jr et al 2002; Chu 2005; Weber et al 2009). This can be explained by the prolonged duration of parturition and sow uterine capacity (Leenhouwers et al 1999; Weber et al 2009), and to the reduction in sow muscle tone after repeated farrowing leading to an increasing probability of dystocia and pig mortality at birth (Canario et al 2006; Lucia Jr et al 2002). Also, larger litters are usually associated with lower birth weights and prolonged farrowing (Dial et al 1992; Borges et al 2005), which contributes to increase the odds of stillborns. Stillborn pigs in small litters are commonly associated with fetus reabsorbing due to diseases such as parvovirus or other pathogenic agents. In this study only 20.3, 3.56, 0.85 and 0.36% of the litters had 1, 2, 3 or >3 stillbirths.

A greater occurrence of mummified fetuses in larger litters is commonly attributed to an insufficient uterine space to maintain the development and survival of fetuses (Wu et al 1988; Muirhead and Alexander 1997). However, disease, a factor not studied here, is also known to affect the occurrence of stillbirths and mummified fetuses. Generally, in an average litter size, the presence of one mummy indicates a physiological death whereas the presence of multiple mummies raises suspicions of an infectious cause of reproductive failure (Sims and Glastonbury 1996). The clinical signs include a low total number born and a high number born dead/mummified leaving a very low number born alive. However, sows infected with parvovirus in early pregnancy can cause a reduction in litter size without the presence of mummies (Lawlor and Lynch 2007). In this study only 16.3, 3.45, 0.76 and 0.46% of the litters had 1, 2, 3 or >3 mummified fetuses. This emphasizes the importance of litter size as a non-infectious factor for the occurrence of mummification, in the present study.

Conclusions

The rates of stillborn pigs or mummified fetuses observed in this study (2.84 y 2.36%) are within the range of values reported for commercial pig farms. Under the tropical conditions of this study, season seems to be an important factor on mummified fetuses. To reduce the rate of stillborn pigs or mummified fetuses, sows with five or more parities that are expected to give birth to large litters should be given more attention.

References

Borges V F, Bernardi M L, Bortolozzo F P and Wentz I 2005 Risk factors for stillbirth and foetal mummification in four Brazilian swine herds. Preventive Veterinary Medicine 70: 165–176.

Canario L, Cantoni E, Le Bihan E, Caritez J C, Billon Y, Bidanel J P and Foulley J L 2006 Between-breed variability of stillbirth and its relationship with sow and piglet characteristics. Journal of Animal Science 84: 3185-3196.

Chu M X 2005 Statistical analysis of stillbirths in different genotypes of sows. Asian-Australian Journal of Animal Science 18(10): 1475-1478.

Dial G D, Marsh W E, Polson D D and Vaillancourt J P 1992 Reproductive failure: Differential diagnosis. In: Leman A D, Straw B E, Mengeling W L, D’Allaire S, Taylor D J, editorss. Diseasesof Swine. 7th edition Ames, Iowa: Iowa State University Press, pp 88–137.

Espitia A and Galíndez R 2011 Estudio de algunos factores genéticos y no genéticos que afectan el número de momias y la mortalidad al nacimiento de cerdos Duroc y Hampshire. Revista Facultad de Agronomía (UCV) 37(1): 38-44.

Koketsu Y, Sasaki Y, Ichikawa H and Kaneko K 2010 Benchmarking in animal agriculture: concepts and applications. Journal of Veterinary Epidemiology 14:105-117.

Lawlor P G and Lynch P B 2007 A review of factors influencing litter size in Irish sows. Irish Veterinary Journal 60: 359-366.

Le Cozler Y, Guyomarc’h C, Pichodo X, Quinio P Y and Pellois H 2002 Factors associated with stillborn and mummifies piglets in high-prolific sows. Animal Research 51: 261-268.

Leenhouwers J I, de Almeida Junior C A, Knol E F and van der Lende T 2001 Progress of farrowing and early postnatal pig behavior in relation to genetic merit for pig survival. Journal of Animal Science 79: 1416–1422.

Leenhouwers J I, Van der Lende T, Knol E F 1999 Analysis of stillbirth in different lines of pig. Livestock Production Science 57: 243–253.

Lucia Jr T, Correˆa M N, Deschamps J C, Bianchi I, Donin M A, Machado A C, Meincke W and Matheus J E M 2002 Risk factors for stillbirth in two swine farms in the south of Brazil. Preventive Veterinary Medicine 53: 285–292.

MengelingW L, Langer K M and Vorwald A C 2000 The effect of porcine parvovirus and porcine reproductive and respiratory syndrome virus on porcine reproductive performance. Animal Reproduction Science 60-61: 199–210.

Muirhead M R and Alexander T J L 1997 Managing Pig Health and the Treatment of Disease. A Reference for the Farm. 5M Enterprises, Sheffield, pp. 133–226.

Schneider L G, Costi G, Wentz I, Bortolozzo F P and Borchardt-Neto G 2003 Avaliação da mumificação fetal suína em uma granja industrial. Revista Brasileira de Reprodução Animal 27 (4): 678–683.

Segura-Correa J C, Alzina-López A and Solorio-Rivera J L 2007 Evaluation of three models and risk factors associated with stillborn piglets in Yucatan, Mexico. Técnica Pecuaria en México 45(2): 227-236.

Sims L D and Glastonbury J R W 1996 Neonatal mortality. In: Sims L D, Glastonbury J R W (Editors.), Pathology of the Pig. A Diagnostic Guide. The Pig Research and Development Corporation, Barton, pp 423-432.

Tantasuparuk W, Lundeheim N, Dalin A M, Kunavongkrit A and Einarsson S 2000 Reproductive performance of purebred Landrace and Yorkshire sows in Thailand with special reference to seasonal influence and parity number. Theriogenology 54: 481–496.

Van der Lende T 2000 Embryonic and fetal mortality in swine: causes, consequences and how to prevent these losses. In: Proceedings of the 7th Simpósio Internacional de Reprodução e Inseminação Artificial em Suınos, Foz do Iguaçu, Brazil, pp. 243–252.

Weber R, Keil N M, Fehr M and Horat R 2009 Factors affecting piglet mortality in loose farrowing systems on commercial farms. Livestock Science 124: 216-222.

Wu M C, Hentzel M D and Dziuk P J 1988 Effect of stage of gestation, litter size and uterine space on the incidence of mummified fetuses in pigs. Journal of Animal Science 66 (12): 3202–3207.