Abstract
To prove the effect of postparturient swine urogenital disease (SUGD) on reproductive performance, culled sows with SUGD in their previous history (n = 1363) were subjected to retrospective lifetime production analysis. The sows were assigned to parity groups 1, 2 to 6, and > 6. Bacterial flora of vulval discharges were evaluated.
Parity 1 sows had a lower percentage of SUGD than did sows of parity 2 to 6 and parity > 6 (P < 0.05 and P < 0.01, respectively). Compared with parity 2 to 6 sows, parity 1 and parity > 6 sows had lower (P < 0.001) conception, farrowing and adjusted farrowing rates, lifetime average total born, live-born litter sizes, stillbirth rates, and weaning litter weights compared with animals culled for other reasons than SUGD. The conclusions are that high parity sows have a higher occurrence of postparturient SUGD and that higher parity sows with postparturient SUGD have a lower performance compared with lower parity sows with postparturient SUGD.
Résumé
Effets des maladies génito-urinaires post-partum sur les performances reproductrices à vie des truies. Afin de prouver l’effet des maladies génito-urinaires post-partum (MGUP) sur les performances reproductrices, des truies de réforme présentant une histoire antérieure de MGUP (n = 1363) ont fait l’objet d’une étude rétrospective de leur production à vie. Les truies ont été assignées à des groupes selon le rang de portée : 1, 2 à 6, > 6. La flore bactérienne et les écoulements vulvaires ont été évalués. Les truies du groupe primipare avaient un pourcentage inférieur de MGUP par rapport au groupe 2 à 6 et au groupe > 6 (P < 0,05 et P < 0,01 respectivement). Comparé aux truies du groupe 2 à 6, le groupe 1 et le groupe > 6 montraient un taux de conception, un taux de mise bas brut et ajusté, un nombre moyen de porcelets nés totaux, un nombre de nés vivants, un pourcentage de mortinatalité et du poids des portées au sevrage, des valeurs inférieures (P < 0,001) à celles des animaux éliminés pour d’autres raisons que les MGUP. Les conclusions montrent que les truies ayant eu plusieurs portées ont une plus grande incidence de MGUP et que les truies ayant eu plusieurs portées et ayant eu des MGUP ont eu une moins bonne performance comparée aux truies ayant eu moins de portées et ayant eu des MGUP.
(Traduit par Docteur André Blouin)
Introduction
Urogenital infections in gilts and sows significantly influence herd fertility (1). Urinary tract infection (UTI), postparturient swine urogenital disease (SUGD), or both, are often found in combination with the mastitis metritis agalactia syndrome (MMA) (2) and may contribute to a decrease in farrowing rates (3), and an increase in abortions (4) and sow mortality (5,6). Vulval discharges are often associated with chronic endometritis or with SUGD (2,7). While some discharges are considered physiologically normal, others — especially purulent discharges — are pathological and interfere with the subsequent fertility of females (8). Metritis is frequently present in conjunction with UTI (9). Sows suffering bacteriuria have a lower subsequent reproductive performance compared with healthy sows (10).
Sows with UTI have a higher prevalence of SUGD compared with sows with a healthy urinary tract (11,12). Biksi et al (13) found a positive correlation between cystitis (urocystitis) and endometritis. Bilkei et al (12) examined 101 sows that had been culled for SUGD and found gross inflammatory changes in the urinary bladder and urethra in all cases; 50% of these necropsied sows also had uterine changes. In a similar investigation (9), 61% of sows culled for SUGD were found to have inflammatory changes involving both the urogenital tract and the mammary glands. Waller et al (2) found a significant negative effect of excessive postparturient vulval discharges (> 50 mL/d) on the subsequent conception, and on farrowing and adjusted farrowing rates in sows.
The objective of the present study was to evaluate the effects SUGD on reproductive performance of sows of different parities.
Materials and methods
From August 2003 to August 2004, 1363 sows culled from 11 Slovakian swine herds because of SUGD were subjected to retrospective lifetime production analysis. All sows were F1 crosses of large white boars × Landrace sows and were mated to purebred Duroc or Hampshire boars. The sows were assigned to 3 parity groups (parity 1, n = 331; parity 2 to 6, n = 450; parity > 6, n = 582). Sows culled for reasons other than SUGD (n = 3499) served as the control group. The units were located in the same geographic area, had received feed from the same feed company, and were managed similarly.
Gestating sows were organized into groups of 10 to 16 and housed on partially (20% to 35%) solid floors. Lactating sows were housed, unrestricted, in individual farrowing crates with 4.0 to 5.0 m2 of space per animal. The selected units had a history of an increased number of sows with vulval discharges (20.2%, sχ̄ = 5.5% of inventoried females) during the past 3 y. Natural mating was practised in these units. During pregnancy, the sows were routinely vaccinated against infection with Erysipelothrix rhusiopathiae, Streptococcus spp., Escherichia coli, and, during lactation, parvovirus.
Postparturient SUGD was routinely diagnosed by the farm manager according to an early SUGD diagnostic system (Table 1), namely, excessive (> 50 mL/d) vulval discharge (3), elevated temperature, diminished milk production, and reduced appetite. Sows diagnosed with SUGD were treated with an intrauterine infusion of antibiotics (according to a sensitivity test), parenteral antibiotics for 3 d [according to sensitivity test], oxytocin (Oxytocin; TAD, Cuxhaven, Germany), 10 IU/d; and, on the day of diagnosis of SUGD, prostaglandin F2α (Estrumate; Essex, Germany), 175 μg, IM. The vulval discharges of 136 sows with SUGD in their previous history and those of 350 sows culled due to reasons other than SUGD were subjected to routine bacteriological examination.
Table 1.
Diagnosis of postparturient swine urogenital disease (SUGD). Sows suffering excessive (> 50 mL/d) postparturient vulval discharges were examined for 3 d postpartum and diagnosis of SUGD was made if a sow had a total score of at least ++++ based on the severity of fever, milk production, and appetite (26)
| Parameter | Score 1 | Score 2 | Score 3 |
|---|---|---|---|
| Fever ºC | 40.0–40.3 | 40.4–40.6 | Over 40.6 |
| + | + + | + + + | |
| Milk production | Hypogalactia | Agalactia without clinical signs of mastitis | Agalactia with clinical signs of mastitis |
| + | + + | + + + | |
| Appetite | Diminished appetite | Moderate anorexia | Total anorexia |
| + | + + | + + + |
Hypogalactia — hungry, lethargic but otherwise healthy-looking, piglets that have regular suckling periods; Agalactia without clinical signs of mastitis — weak, hungry dehydrated piglets that have no regular suckling periods or no suckling at all; Agalactia with clinical signs of mastitis — swollen, painful, mammary glands with piglets not suckling; Diminished appetite — more than 50% but not all the daily food provided (3 kg) eaten; Moderate anorexia — less than 50°C (< 1.5 kg) of the daily food provided eaten; Total anorexia — no food eaten at all
The parameters evaluated were as follows:
A — Parity at culling.
B — Bacteriological examination of the discharges.
C — Percentage of SUGD in a group (modified after Bilkei and Horn, 1991).
D — Average litter size over all parities (number of piglets, including antepartum and intrapartum stillbirths, excluding obviously “old” mummies with characteristic dark color and small size). Piglets were classified as antepartal stillbirth (APSB), if the fetus was fully developed, but the skin was greyish and connective tissue was bright red and edematous; the liver, lungs, and spleen were similarly red/brown; and the body cavities contained serosanguineous fluids.
E — Average live-born litter size over all parities.
F — Average intrapartum stillbirth (IPSB) over all parities (IPSB were normal in size and had the external appearance of a live-born piglet).
G — Average numbered mummies over all parities.
H — Average weaning litter weights over all parities.
I — Conception, farrowing, and adjusted farrowing rates over all parity groups.
These parameters are those routinely evaluated in this geographic area.
Statistical analysis
Data associated with each parity group were analyzed separately by using a statistical analytical system (SAS/ STAT User’s Guide, Version 6; Cary, North Carolina, USA) (14). The CATMOD procedure was used to analyze fertility parameters (dependent variables), including 21-day conception rate, farrowing rate, and adjusted farrowing rate (defined as number of females farrowed/ number of females mated minus number of females that failed to farrow for nonreproductive reasons). Independent variables included breeding month and treatments not related to reproduction. Parity category, interaction between parity categories and duration of previous lactation (treated as continuous variables) were included in the model. Previous weaning-to-mating interval category and its interaction with parity category were included in the model.
The general linear model (GLM) procedure of thee statistical analytical system (14) was used for analysis of litter size data. Dependent variables were number of total born, live-born, stillborn, and mummified fetuses. Independent variables included litter conception month and treatments not related to reproduction.
Age at first mating (d), treated as a continuous variable, was included in the model for parity 1 sow data. Parity category and duration of previous lactation, treated as a continuous variable, were included in the model. Previous postweaning-mating-interval and its interaction with parity category were included in the model. Standard errors for the means and probability comparison between the means were calculated
Results
Parity at culling was 3.91, sχ̄ = 0.39 in sows culled due to SUGD and 4.72, sχ̄ = 0.71 (P < 0.05) in sows culled other reasons than SUGD. The percentage of animals culled due to SUGD differed between parity categories (Table 2).
Table 2.
Proportion of sows per parity category culled due to swine urogenital disease (SUGD) or due to other reasons in 11 Slovakian indoor production units
| Parity | Group 1 Sows culled due to SUGD (n = 1363) | Group 2 Sows culled for reasons other than SUGD (n = 3499) |
|---|---|---|
| 1 | 331 (24.3%)a,A | 1123 (32.1%)a,B |
| 2 to 6 | 450 (33.0%)b,A | 1345 (38.4%)b,B |
| > 6 | 582 (42.7%)c,C | 1031 (29.5%)a,D |
P < 0.05 in a column
P < 0.01 in a column
P < 0.05 in a row
P < 0.01 in a row
Bacteriological examination of vulval discharges revealed the presence of either Clostridium spp, Actinobaculum suis, Pseudomonas aeruginosa, Klebsiella spp, Citrobacter, Pasteurella multocida, Proteus spp, gram-positive streptococci (especially enterococci, S. faecalis), staphylococci (St. albus, St. epidermis, St. aureus), Erysipelothrix rhusiopathiae, or E. coli (E. coli was found in each vulval discharge).
Compared with parity 2 to 6 sows, parity 1 and parity > 6 sows had lower (P < 0.001) conception, farrowing, adjusted farrowing rates (Table 3), lifetime average total born, live-born litter sizes, and lower stillbirth rates (Table 4). Mummified rates were higher in parity > 6 than in other parities (Table 4). Parity 1 sows had no significant differences in weaning litter weights regardless of the reason for culling. In animals culled due to SUGD in their previous history, parity 2 to 6 sows had higher weaning litter weights than parity 1 and parity > 6 sows (P < 0.05 and P < 0.01, respectively). Parity 2 to 6 and > 6 sows that had SUGD had lower weaning litter weights than animals culled for other reasons (Table 5).
Table 3.
Average fertility per reproductive cycle and parity group of sows culled due to swine urogenital disease (SUGD) during a 12-month period in 11 large Slovakian indoor production units (data of sows culled for other reasons than SUGD* in brackets)
| Parity | CR % (CR% of * sows) | FR % (FR% of * sows) | AFR % (FR% of * sows) |
|---|---|---|---|
| 1 | 82.4 sχ̄ = 1.1a (90.4 sχ̄ = 1.1a) | 80.5 sχ̄ = 1.4a (80.1 sχ̄ = 1.7a) | 81.2 sχ̄ = 1.3a (85.1 sχ̄ = 1.2a) |
| 2 to 6 | 87.9 sχ̄ = 1.9b (90.1 sχ̄ = 1.9a) | 83.9 sχ̄ = 2.0b (81.9 sχ̄ = 1.9a) | 86.9 sχ̄ = 1.2b (84.0 sχ̄ = 1.2a) |
| > 6 | 81.0 sχ̄ = 1.1a (87.9 sχ̄ = 1.5a) | 79.1 sχ̄ = 3.9a (79.6 sχ̄ = 2.4a) | 80.1 sχ̄ = 3.2a (80.0 sχ̄ = 2.9b) |
CR — Conception rate; FR — Farrowing rate; AFR — Adjusted farrowing rate; sχ̄ — Standard error of the mean
P < 0.001 in a column
Table 4.
Average least — squares means for litter size by parity category per reproductive cycle of sows culled due to swine urogenital disease (SUGD) during a 12-month period in 11 large Slovakian indoor production units (data of sows culled for other reasons than SUGD in brackets)
| Parity
|
|||
|---|---|---|---|
| Litter data | 1 n (n control sows) | 2 to 6 n (n control sows) | > 6 n (n control sows) |
| Total born | 9.9, sχ̄ = 0.41a (10.1, s sχ̄ = 0.22a) | 11.4, s sχ̄ = 0.24b (11.1, s sχ̄ = 0.21b) | 10.0, s sχ̄ = 0.20a (11.1, s sχ̄ = 0.19b) |
| Born alive | 8.6, s sχ̄ = 0.29a (8.8, s sχ̄ = 0.33a) | 11.0, s sχ̄ = 0.31b (10.7, s sχ̄ = 0.19b) | 8.5, s sχ̄ = 0.22a (9.6, s sχ̄ = 0.21b) |
| Stillborn | 1.26, s sχ̄ = 0.02a (1.31, s sχ̄ = 0.02a) | 0.44, s sχ̄ = 0.27b (0.41, s sχ̄ = 0.02b) | 1.5, s sχ̄ = 0.04a (1.46, s sχ̄ = 0.02a) |
| Mummies | 0.16, s sχ̄ = 0.02a (0.10, s sχ̄ = 0.02a) | 0.12, s sχ̄ = 0.04a (0.12, s sχ̄ = 0.02a) | 1.11, s sχ̄ = 0.02b (0.91, s sχ̄ = 0.02a) |
sχ̄ — Standard error of the mean
P < 0.001
Table 5.
Average weaning litter weights (at day 28 of lactation) per reproductive cycle and by parity group of sows culled due to swine urogenital disease (SUGD) during a 12-month period in 11 large Slovakian indoor production units
| Weaning litter weights (kg)
|
||
|---|---|---|
| Parity groups | Sows culled due to swine urogenital disease (SUGD) (n = 1363) | Sows culled for reasons other than swine urogenital disease (SUGD) (n = 3499) |
| 1 | 70.4, sχ̄ = 3.1a,A | 71.1, sχ̄ = 4.0a,A |
| 2 to 6 | 75.9, sχ̄ = 2.7b,A | 79.9, sχ̄ = 4.2b,B |
| > 6 | 60.9, sχ̄ = 7.1c,A | 64.2, sχ̄ = 4.1c,B |
sχ̄ — Standard error of the mean
P < 0.05 in a column
P < 0.01 in a column
P < 0.05 in a row
Discussion
Although some of the chosen parameters (D, E, F, and G) do not relate directly to SUGD, they were evaluated in the present study to determine if they had any association with SUGD.
The high (> 20%) occurrence of UTI, SUGD, or both, in a pig breeding herd endangers profitability (7,10,12). In the production units evaluated here, the sow vulval discharges may have contributed to postparturient SUGD. Unfortunately, prepartum urine analyses were not done. Consistent with the present results, the negative relationship between UTI, SUGD, and subsequent reproductive parameters in breeding sows have been reported previously (7,9–12,15–20). Because of the “dynamic changes” (16) in the microflora of the cranial vagina (and probably in the lower urinary tract) of the sows and the high potential for developing postparturient SUGD, animals repeatedly suffering UTI, SUGD, or both, should be culled without delay (12).
The higher occurrence of vulval discharge in sows of higher parities has been reported previously (3,7,10,19– 21), as have lower production levels in animals with a history of vulval discharges (3).
Many recent publications have focused on reasons for culling or the cause of sow mortality due to UTI, SUGD, or both (1,4,5,6,22–26), or age-related occurrence of UTI/SUGD (9,10–13,17,18). As in this study, parity at culling markedly influences the economic well-being in a pig breeding unit (5).
Coliforms are often isolated from sows with vulval discharges (1,9–12,17,18,20). Because cultures from single discharges often yield several species of bacteria, spontaneously occurring infections of the cranial vagina, urethra, and bladder are probably the results of an initial infection with 1 infectious agent that is subsequently overgrown by opportunistic organisms.
Alternatively, the cranial vagina may be colonized initially by multiple facultative pathogens belonging to the indigenous flora of the cranial vagina. Vulval discharges and UTI are often present in breeding animals and culled sows (9,10,18,20). The urinary tract is a “dynamic microbiological ecosystem” (16), and components of its flora can increase and decrease depending of the production status of the animal and stresses imposed on animals when they are transferred to the farrowing barn, during parturition, or when they are exposed to possible secondary infections in a new environment (10). The dominant bacterial species in the urinary bladder and vestibulum vaginae can change spontaneously (11). Soon after parturition, the urogenital organs are probably colonized simultaneously by multiple organisms from the cranial vagina and urinary bladder, which may include indigenous microbes, bacterial contaminants, and pathogens (3,13,23,24). Further, the reproductive tract of sows is susceptible to infection after farrowing because of the periparturient increase in the number of both nonpathogenic microflora and facultative pathogens in the caudal vagina and urinary bladder (17,18). While most bacteria are eliminated within 12 to 30 h after farrowing, facultative pathogens may overgrow nonpathogenic microflora and establish mildly invasive endometritis (11). Biksi et al (13) examined the urogenital organs of 499 sows and found that animals affected by urocystitis were 3.5 times more likely to have endometritis than animals without urocystitis. Urinary tract infections and vulval discharge predispose to MMA (9,11,16,18,19). The breakdown of uterine tissue provides a medium that favors the growth of a variety of opportunistic microorganisms coming from the urinary bladder, vestibulum vaginae, or both (23). Retention of remnants of the placenta may predispose sows to mild metritis and endometritis (13). Bilksi et al (13) stated that the sensitivity of macroscopic methods was not higher than 18.1% in cases of endometritis and 47.9% in cases of urocystitis, while the sensitivity of bacteriologic culture for the diagnosis of the same conditions was 31.8% and 63.0%, respectively. Biksi et al (13) also found that a large proportion of the animals examined did not show inflammatory lesions. Consistent with data in the literature (11,18,19), Biksi et al (13) found that the species of bacteria isolated from the urinary bladder and endometrium were representative of the normal fecal flora. These findings support the present findings and the suspected etiology of periparturient diseases, namely, bacteria from the fecal, vaginal, and vesical flora. As older sows have a higher prevalence of vulval discharge (17), it is reasonable to suggest that older sows with vulval discharge suffer a higher percentage of SUGD. The low predictive value of a positive bacteriological culture reflects the diagnostic dilemma often stated in the literature (10–12,17,18,22,25,26). In order to reach a firm diagnosis, Biksi et al (13) suggested the need to use histopathologic examination in combination with bacteriological examination of both uterus and urinary bladder.
Increased prefarrowing serum estradiol concentrations, increased numbers of leucocytes (lymphocytes and neutrophils, immunglobulin-bearing mononuclear cells), and an increased phagocytic capacity of polymorphonuclear leucocytes in the periparturient uterus have been recorded in postparturient sows. These alterations may increase the sow’s response to infectious agents for only a short period after parturition (23). Ascending invasion from the urinary bladder via mucosal surfaces, blood vessels, or lymphatic vessels is likely during the periparturient period (15).
The present results indicate that in sows that have had a history of periparturient diseases and vulval discharge, parity markedly influences both the occurrence of vulval discharge and reproductive performance. As no herds were included without SUGD problems, the present results might apply only to herds that are comparable with the selected study herds.
References
- 1.Bilkei G, Bölcskei A, Clavadetscher E, et al. Bericht über den peripartalen Krankheitskomplex der Muttersau in der industriellen Schweinezucht. 4te Mitteilung: Die Auswirkungen der prophylaktischen oraler Medikamentgabe auf das Auftreten des peripartalen Krankheitskomplexes der Muttersau mit der Anamnese von urinary tract infection (UTI) und vaginal-vulvalem Ausfluss (vaginal — vulval discharge) Berl Münch Tierärztl Wochenschr. 1995a;108:8–13. [PubMed] [Google Scholar]
- 2.Thornton EJ, Wilson RJ, Connaughton I, et al. Effect of subclinical urogenital infection on reproductive performance in the sow. Proc 15th Int Pig Vet Soc Congr, Birmingham, England, 1998:236.
- 3.Waller CM, Bilkei G, Cameron RDA. Effect of periparturient disease and/or reproductive failure accompanied by excessive vulval discharge and weaning to mating interval on sow reproductive performance. Aust Vet J. 2002;80:545–549. doi: 10.1111/j.1751-0813.2002.tb11033.x. [DOI] [PubMed] [Google Scholar]
- 4.Bilkei G, Bölcskei A, Goos T. Pathogene Befunde aus dem Urogenitaltrakt ausgemerzter Muttersauen aus einem Grossbestand. Tierärztl Prax. 1995;23:37–41. [PubMed] [Google Scholar]
- 5.D’Allaire S, Drolet R. Culling and mortality in breeding animals. In: Leman AD, Straw BE, Mengeling WL, D’Allaire SD, Taylor DJ, eds. Diseases of Swine, 7th ed. Wolfe Publ 1992:861–871.
- 6.Karg H, Bilkei G. Causes of sow mortality in Hungarian indoor and outdoor pig production units. Berl Münchn Tierärztl Wochenschr. 2002;115:366–368. [PubMed] [Google Scholar]
- 7.Baumann B, Bilkei G. The effect of postpartal prostaglandin F2α application on some of the subsequent reproductive parameter of the sows with or without antepartal vulvovaginal discharge. The Pig Journal. 2001;47:35–41. [Google Scholar]
- 8.Stelzer P, Bilkei G, Clavadetscher E, et al. Scheidenausfluss ante partum als Risikofaktor für postpartale Erkrankungen der Sau und frühpostnatale Ferkelverluste. Berl Münch Tierärztl Wochenschr. 1997;110:320–323. [PubMed] [Google Scholar]
- 9.Bilkei G, Goos T. Evaluation of the occurrence of SUGD (Swine Urogenital Disease) in large pig production units. Proc 13th Int Pig Vet Soc Congr, Bangkok, Thailand. 5–11 July 1994:472.
- 10.Mauch C, Bilkei G. The influence of prepartal bacteriuria on the reproductive performance of the sow. Dtsch tierärztl Wochenschr. 2004;111:166–172. [PubMed] [Google Scholar]
- 11.Bilkei G, Bölcskei A, Goos T, et al. Die Beteiligung von E. coli an puerperalen Urogenitalinfektionen bei Altsauen. Tierärztl Umschau. 1994;49:471–476. [Google Scholar]
- 12.Bilkei G, Bölcskei A, Goos Th, et al. Bericht über den peripartalen Krankheitskomplex der Muttersau in der industriellen Schweinezucht. 3te Mitteilung: Schlachtbefunde von Altsauen mit der Anamnese von peripartalen Erkrankungen. Berl Münch Tierärztl Wochenschr. 1994;107:405–408. [PubMed] [Google Scholar]
- 13.Biksi I, Takacs N, Vetesi F, et al. Association between endometritis and urocystitis in culled sows. Acta Vet Hung. 2002;50:413–423. doi: 10.1556/AVet.50.2002.4.4. [DOI] [PubMed] [Google Scholar]
- 14.SAS/STAT® User’s Guide, Version 6. Cary, North Carolina: SAS Institute Inc 1990.
- 15.Armstrong CH, Hooper BE, Martin CE. Microflora associated with agalactia syndrome of sows. Am J Vet Res. 1968;29:1401–1407. [PubMed] [Google Scholar]
- 16.Berner H. Die Bedeutung chronischer Erkrankungen der Harnwege bei der Entstehung von Puerperalstörungen und Mastitiden der Muttersau. Dtsch Tierärztl Wochenschr. 1971;78:233–256. [PubMed] [Google Scholar]
- 17.Bilkei G, Bölcskei A, Goos T, et al. Bericht über den peripartalen Krankheitskomplex der Muttersau in der industriellen Schweinezucht. 1ste Mitteilung: Peripartaler Verlauf der Bakteriurie der Sauen mit vaginal-vulvalem Ausfluss in einem modernen Schweinezuchtbetrieb. Berl Münch Tierärztl Wochenschr. 1994;107:327–330. [PubMed] [Google Scholar]
- 18.Bilkei G, Bölcskei A, Goos T, et al. Bericht über den peripartalen Krankheitskomplex der Muttersau in der industriellen Schweinezucht. 2te Mitteilung: Der Einfluss der präpartaler Bakteriurie auf das peri-, bzw. postpartale Auftreten von Puerperalerkrankungen bei Muttersau mit Anamnese von urinary tract Infektion (UTI) und vaginal — vulval discharge. Berl Münch Tierärztl Wochenschr. 1994;107:373–376. [PubMed] [Google Scholar]
- 19.Dial GD, Marsh WE, Polson DD, et al. Reproductive Failure: Differential Diagnosis. In: Leman AD, Straw BE, Mengeling WL, D’Allaire SD, Taylor DJ, eds. Diseases of Swine, 7th ed. Wolfe Publ, 1992:88–138.
- 20.Sanders LMG, Bilkei G. Urogenital diseases and their effect on reproductive performance in high-parity sows. Tijdschrift voor Diergeneeskunde. 2004;129:108–112. [PubMed] [Google Scholar]
- 21.Dee SA. Porcine urogenital disease. In: Veterinary Clinics of North America. Food Animal Practice, Swine Reproduction. 1992;8:641–660. doi: 10.1016/s0749-0720(15)30709-x. [DOI] [PubMed] [Google Scholar]
- 22.Almond GW, Richards RG. Evaluating porcine reproductive failure by use of slaughter checks. Compend Cont Educ Pract Vet. 1986;14:542–546. [Google Scholar]
- 23.Gertenbach W, Bilkei G. Erysipelas: Potential involvement in urogenital disease of the sow. J Swine Health Prod. 2002;10:205–207. [Google Scholar]
- 24.Hoffmann CW, Bilkei G. Chronic Erysipelas of the Sow — a Subclinical Manifestation of Reproductive Problems. Reprod Dom Anim. 2002;37:119–120. doi: 10.1046/j.1439-0531.2002.00339.x. [DOI] [PubMed] [Google Scholar]
- 25.Meredith MJ. Bacterial endometritis. In: Morrow DA, ed. Current Therapy in Theriogenology. 2nd ed. Philadelphia: WB Saunders, 1992:953–956.
- 26.Bilkei G, Horn A. Beitrag zur Therapie des Metritis-, Mastitis-, Agalaktie (MMA) Komplexes der Schweine. Berl Münch Tierärztl Wochenschr. 1991;104:421–423. [PubMed] [Google Scholar]