The effect of diseases of the urogenital track, such as endometritis and cystitis, is considered an important determinant of farms’ economic output and animals’ welfare status31. Biksi et al. (2002) reported positive association between cystitis and endometritis, while Gmeiner et al. (2007)32 suggested the existence of a bidirectional reservoir of infections, with non-specific and opportunistic pathogens, between the uterus and the urinary tract. In our study, we estimated the prevalence of UTI in culled sows from 3 Greek swine herds through histopathological evaluation of the urinary bladder, urine culture and urinalysis. Furthermore, we investigated possible associations between histopathologically defined cystitis2,11 and the results of urinalysis and urine culture.
The estimated prevalence of cystitis was within the previously reported range of prevalences in culled sows from 27 to 53%2,11,16. Interestingly, these studies demonstrated a high frequency of cystitis, affecting anywhere between 1/3 and ½ culled sows. Similar to the findings of Bellino et al (2013) and Grattarola et al (2010), we found that that bacteriuria was less frequent, by almost 50%. Relevant to previous studies15,33 we also detected E.coli isolates as the leading cause of bacteriuria, accounting for approximately 50% of all incidents, followed by Staphylococcus spp.; these microbes were cumulatively responsible for over 70% of incidents. Most likely, these cases were the result of ascending infections which are deemed common because of the female’s short urethra and the physiological relaxation of the sphincter muscle peripartum. These bacteria which originate from the animals’ intestinal tract, populate the environment of pig houses and ascend and colonize the lower part of the urinary tract11,34,35. Interestingly, we found only 2 sows infected with Actinobacillus suis, a specific contaminant of the urinary tract with descending significance compared to data reported in the past mainly due the wide application of artificial insemination11,36
The E. coli and the other Gram-negative (Enterobacter spp.) and Gram-positive (Staphylococcus spp., Enterococcus spp.) isolates were resistant to the vast majority of antibiotics considered, a finding in line with previous relevant reports15,37. Based on our findings, the narrow range of options for antimicrobial treatment of urinary tract infections in the studied herds only includes cephalosporins or polymyxins; both last-resort categories of drugs against multi-resistant bacteria strains of major significance in human health38.
We found that almost 1 out of 3 tested sows had turbid urine. Importantly, among sows with bacteriuria urine turbidity was recorded in almost 2 out of 3 animals. Urine turbidity was associated with presence of sediment, which in turn, was associated with crystalluria. Urine may sometimes contain less sediment compared to the amount observed in the bladder through ultrasonographic depiction39. However, our collection method of mid-stream urine after gentle shaking of urinary bladders for about a minute led to a rather homogenous distribution of urine sediment. We microscopically examined the detected sediment, and recorded all of its constituents, i.e. red blood cells, leukocytes and crystals. In our data, crystalluria was highly associated with presence of urine sediment. Crystals in urine may be either the result of small abnormalities in the mineral composition of the feed, such as imbalance in calcium and phosphorus intake40, and/or the result of insufficient water consumption and/or, alternatively, be induced by local infections41.
Researchers postulated that higher parity predisposes both to endometritis and to cystitis5,26,42,43. In our data, parity was not associated either with histologically confirmed cystitis or with bacteriuria, similarly to reports from Biksi et al. (2002) and Piassa et al. (2015). Moreover, we found no among-herd or among-season variation in cystitis or bacteriuria frequency. Sows with proteinuria were more likely to have histological lesions consistent with acute or chronic cystitis than those without proteinuria or were more likely to have positive urine cultures than those without proteinuria. Proteinuria is the presence of abnormal protein level in urine, a consequence of either abnormal transglomerular passage of proteins, because of increased permeability of glomerular capillary wall and their subsequent impaired reabsorption by the epithelial cells of the proximal tubuli44, or because of the breakdown of urea by bacteria, in an alkaline environment (urine Ph > 8). Grahofer et al. (2020) in their recent report of biomarkers for diagnosis of cystitis in sows identified and proposed as one of the most reliable and sensitive urinalysis biomarkers, in comparison to the gold standard of histopathology, the presence of proteinuria. In human medicine, Carter et al (2006)46 also found an association between proteinuria and bacteriuria but the causative relationship remains undefined.
Although in previous studies15,35 researchers reported no correlation between the presence of cystitis and urine pH, we found that higher pH values were associated with increased odds of bacteriuria or, with decreased odds for a sow to have lesions of acute and/or chronic cystitis, compared to having a normal bladder. It has been shown that alkaline pH supported the development of certain urinary sediment and was associated with bacteriuria. Nonetheless, a causative relationship between alkaline urinary Ph and bacteriuria is difficult to establish because it is affected by several factors22. In some studies the acid-base balance of the diet correlated to the urinary pH and to the total bacteria colony forming units in urine43,47. Lowering of urine pH was proposed as a mean to inhibit or control urinary bacterial overgrowth36. In sows with urinary tract infection, urine alkalization may result from urea transformation into ammonia by the bacterial flora48. Therefore, high urine pH may be the result of the presence and the metabolism of bacteria, or may preceded or even triggered the colonization of the urinary tract with bacteria. In the cross-sectional context of this study inferences about the exact role and the potential causal effect of urine pH in urinary tract infections are not justified.
Presence of sediment was associated with higher odds of bacteriuria. Kauffold et al, (2010) reported, using ultrasonography, that sows with UTI, defined by high bacterial count and macroscopic/biochemical urine abnormalities, were more likely to have high or moderate amounts of sediment in urine than those without UTI. Recently, Grahofer et al. (2020), also concluded that evaluation of presence of sediment is useful to detect sows with cystitis and bacteriuria.
In conclusion, in this study in culled sows from three Greek farms we found that cystitis was quite frequent affecting almost half of the animals tested, while more than half animals with bacteriuria had histologically confirmed cystitis. We found that in most cases microbiota isolated from urine was mainly part of the normal intestinal flora which points to environmental and managerial involvement in the causality of UTI. Proteinuria was associated with both cystitis and bacteriuria. Furthermore, urine turbidity, existence of sediment and crystalluria were highly associated, with almost 2 out of 3 sows with bacteriuria having turbid urine. Therefore, urine turbidity and proteinuria appear as valuable diagnostic tools for UTI of sows.