Proceedings of the Society for Theriogenology Annual Conference 2014

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1 Proceedings of the Society for Theriogenology Annual Conference 2014 Aug. 6-9, 2014 Portland, OR, USA Next SFT Meeting: Aug. 5-8, 2015 San Antonio, TX, USA Reprinted in the IVIS website with the permission of the Society for Theriogenology

2 Chlamydia and Chlamydophilia in bovine reproduction Johannes Kauffold, a Axel Wehrend, b Haukur Sigmarsson a a Large Animal Clinic for Theriogenology and Ambulatory Services, Faculty of Veterinary Medicine, University of Leipzig, b Clinic for Obstetrics, Gynaecology and Andrology of Large and Small Animals with Veterinary Ambulance, Justus-Liebig-University, Giessen, Germany Abstract Infection with chlamydial bacteria, specifically Chlamydophila pecorum, C. abortus, and C. psittaci, is common in cattle. Infection can cause different diseases of which sub- and infertility are the most often observed clinical manifestations. While bulls are usually carriers of chlamydia bearing the risk of being vectors for an infection of females, either through natural mating or artificial insemination, heifers and cows can suffer a multitude of genital disorders. However, chlamydiosis in cattle is generally considered a (multi)factorial disease with factors being related to the environment, confinement or climate. This contribution will briefly describe chlamydial infection in cattle with specific focus on reproduction. Keywords: Chlamydia, Chlamydophilia, bovine, reproduction Introduction Chlamydiae are obligate intra-cellular gram-negative bacteria that cause different diseases in animals and humans. 1 In cattle, chlamydial infections can cause abortion, 2 polyarthritis, 3,4 encephalomyelitis, 5 keratoconjunctivitis, 6 pneumonia, 7 enteritis, 8 hepatitis, 9 vaginitis and endometritis, 10,11 infertility, 12,13 and chronic mastitis. 14 Besides clinical disease, Chlamydiae may be the cause of subclinical manifestation. 9,15-21 This is supported by observations in dairy herds with endemic infection and sub-optimal production records where other relevant pathogens were absent. Moreover, these observations have suggested a role for chlamydial infection as a multi-factorial disease complex. 22 This contribution will briefly review the current knowledge on chlamydial infection in cattle with emphasis on clinical reproduction. Taxonomy The order Chlamydiales has been re-classified regularly leading to the current taxonomy of the family Chlamydiaceae separated into the genera Chlamydophila and Chlamydia, with a total of nine species, namely, Chlamydophila abortus, C. pecorum, C. psittaci, C. pneumoniae, C. felis, C. caviae, Chlamydia trachomatis, Chlamydia suis and Chlamydia muridarum. Three new families were added, i.e. Parachlamydiaceae, Waddliaceae, and Simkaniaceae. 23 There are a number of chlamydial species that can be observed in cattle including C. pecorum, C. abortus, C. psittaci, and Chlamydia suis, with the first three being clearly the most prevalent species. 2,13,21,22,24-27,30-32 Prevalence Chlamydial infection is highly prevalent in the dairy cattle population worldwide, with seropositivity at herd level ranging from 45% to 100%. This suggests that chlamydial infections are ubiquitous in cattle. 33 Generally, serological data are difficult to interpret, as chlamydial antibodies can be the humoral response from an infection in any part of the body, and a bacteriologically positive result not necessarily means that the individual has developed antibodies. 32 For instance, in a recent survey conducted in six bull studs it was demonstrated that, while seropositivity was 51% the rate of PCR positivity in semen, preputial washes and feces was between 9% and 18%. Furthermore, serology failed to identify bulls shedding chlamydiae in their semen. 28 Similarly, in a study aimed to monitor the course of a natural chlamydial infection in calves it was found that 60% of the animals seroconverted after inoculation, whereas all were shedding the bacteria. 20 As aforementioned, C. pecorum, C. abortus and C. psittaci are the most prevalent species in cattle. However, there seem to be specimen, gender and topographical effects. For instance, the study of 251 Clinical Theriogenology Volume 6, Number 3 September 2014

3 Kemmerling et al investigated vaginal swabs and revealed 56% positive for C. psittaci, 37% positive for C. abortus and 8% positive for C. pecorum. 21 In contrast, stud bulls were mostly C. psittaci positive in semen and preputial washings, while C. pecorum prevailed in fecal samples. 28 In Asia, specifically Taiwan, it seems that C. abortus is the most prevalent genital chlamydial species. 27 In the United States, previous studies have mostly demonstrated C. pecorum and C. abortus, while C. psittaci was not found. 17,19 But even within Europe, i.e. Austria and Switzerland, the most prevalent chlamydial species, respectively, were also found to be different. 2,30,33,34 Generally, the different chlamydial species found in cattle can infect different organs not uncommonly at the same time. On the other hand there seems to be a genital tropism, with C. abortus and C. psittaci being the ones that are mostly infecting the genital tract. 21,28,35 Mixed infections with two or more chlamydial species at the same time are always possible. 22 Routes of transmission Chlamydiae can be shed by almost all secretions and excretions (vaginal, ocular, and nasal fluids, semen, urine etc.), with fecal shedding being the most important route. Also, the bacteria can be found in aborted material such as fetuses as well as placentae. 20,21,28,36,37 Animals usually infect themselves via the horizontal route through ingestion or inhalation. Venereal transmission seems possible. 38,39 However, available data still raise questions for example of the bacterial load in semen that is necessary for an infection, the pathogenicity of different species, and possibly also the survivability of Chlamydiae after extension of semen during semen processing. Vertical transmission has yet not been reported. Effects of chlamydial infection on health and fertility Generally, infection with chlamydia is considered a multifactorial disease, with several factors related to housing, climate, hygiene etc. being contributors. Until recently, chlamydial infection was considered a sporadic event in cattle with no clinical signs or a sub-clinical course that does not have effects on the animal soundness. In a more recent study, however, where 100 randomly-selected dairy farms were investigated for the effects of chlamydial infection on production traits, a clear relationship was found to average annual milk production (8681 vs kg in infected vs. non-infected animals), number of lactations/animal (2.4 vs. 2.9), rates of abortion, premature calving and perinatal calf deaths (P<0.001). 21 Most importantly, the study revealed that sanitation was better on Chlamydia negative farms again supporting the fact of a multifactorial genesis of Chlamydia-associated disease and that management factors can have a positive effect on the occurrence of the disease. 13 Besides general health, Chlamydiae, specifically C. abortus and C. pecorum have been shown to effect milk yield, either by inflammation or subclinical disease. 14 An infection with chlamydia may cause sub- or infertility. Infected bulls may suffer from vesiculitis, 40 or may not be affected at all. 28,29 Interestingly, infected bulls did not show impaired semen quality as measured on the basis of standard semen parameters. 28 As aforementioned, regardless of being diseased, bulls can shed Chlamydia via semen, and shedding can be intermitted which then puts some difficulties on diagnostics and interpretation of diagnostic results. An interesting finding by an in vitro study conducted by our group is that Chlamydia bind to specific receptors of the sperm membrane (spermadhesines) that are necessary for the sperm to be bound to oviductal cells of the sperm reservoir, i.e. the utero-tubal junction. While this may lead to a reduced capability of sperm to be attached to oviductal cells (and may thus impair the fertility and survivability of the sperm), this mechanism may also be part of an active transmission process of Chlamydia through semen. 41 Any part of the genital tract of a cow or heifer can be infected. Swabs taken from different parts of the genital tract including vagina and uterus 30 but also the oviduct (Kauffold et al., unpublished) frequently proved positive for Chlamydia. Sporadic abortion can occur. 2,26,34 Also, sporadic cases of endometritis and vaginitis due to chlamydial infection has been described. 11,17,30 Interestingly, the fact that Chlamydia was found in different oviductal segments suggests that, as in humans, laboratory animals but also swine, 42 the oviduct is a target organ for an infection. Whether or not this may have consequences for oviductal functions is yet not known. However, the fact of an oviductal postitivity per se suggests that Chlamydia may damage or interfere with oviductal functions either structurally Clinical Theriogenology Volume 6, Number 3 September

4 and/or functionally. An oviductal infection may be the ideal explanation of subfertility or rebreeding of cows and heifers, that otherwise do not show any clinical disease. Conclusions There is clear evidence that chlamydiae are endemic in the cattle population. It is also clear that bacteria can cause clinical disease. However, subclinical cases are the predominant manifestation. Suband infertility are the most often seen clinical signs. Any part of the genital tract can be infected. Whether or not an infection results in structural and/or functional damage is dependent on a multitude of factors related to e.g. environment, confinement or climate. Thus, management measures that are aimed to improve these factors are beneficial toward avoiding chlamydiosis in cattle. References 1. Storz J, Kaltenboeck B: Diversity of chlamydia-induced diseases. In: Woldehiwet Z, Ristic M, editors. Rickettsial and chlamydial diseases of domestic animals. Oxford (UK): Pergamon Press; p Borel N, Thoma R, Spaeni P, et al: Chlamydia-related abortions in cattle from Graubunden, Switzerland. Vet Pathol 2006;43: Storz J,Smart RA, Marriott ME, et al: Polyarthritis of calves: isolation of psittacosis agents from affected joints. Am J Vet Res 1966;27: Twomey DF, Griffiths PC, Hignett BC, et al: Suspected chlamydial polyarthritis in a calf in the UK. Vet Rec 2003;152: McNutt SH, Waller EF: Sporadic bovine encephalomyelitis. Cornell Vet 1940;30: Otter A, Twomey DF, Rowe NS, et al: Suspected chlamydial keratoconjunctivitis in British cattle. Vet Rec 2003;152: Wilson MR, Thomson RG: Chlamydia pneumonia of calves. Res Vet Sci 1968;9: Doughri AM, Yong S, Storz J: Pathologic changes in intestinal chlamydial infection of newborn calves. Am J Vet Res 1974;35: Reggiardo C, Fuhrmann TJ, Meerdink GL, et al: Diagnostic features of chlamydia infection in dairy calves. J Vet Diagn Invest 1989;1: Wittenbrink MM, Schoon HA, Bisping W, et al: Infection of the bovine female genital tract with Chlamydia psittaci as a possible cause of infertility. Reprod Domest Anim 1993;28: Wittenbrink MM, Schoon HA, Schoon D, et al: Endometritis in cattle experimentally induced by Chlamydia psittaci. Zentralbl Veterinarmed B 1993;40: DeGraves FJ, Kim T, Jee J, et al: Reinfection with Chlamydophila abortus by uterine and indirect cohort routes reduces fertility in cattle preexposed to Chlamydophila. Infect Immun 2004;72: Wehrend A, Failing K, Hauser B, et al: Production, reproductive, and metabolic factors associated with chlamydial seropositivity and reproductive tract antigens in dairy herds with fertility disorders. Theriogenology 2005;63: Biesenkamp-Uhe C, Li Y, Hehnen HR, et al: Therapeutic Chlamydophila abortus and C. pecorum vaccination transiently reduces bovine mastitis associated with Chlamydophila infection. Infect Immun 2007;75: Shewen PE: Chlamydial infection in animals: a review. Can Vet J 1980;21: Bodetti TJ, Viggers K, Warren K, et al: Wide range of Chlamydiales types detected in native Australian mammals. Vet Microbiol 2003;96: DeGraves FJ, Gao D, Hehnen HR, et al: Quantitative detection of Chlamydia psittaci and C. pecorum by high-sensitive real-time PCR reveals high prevalence of vaginal infection in cattle. J Clin Microbiol 2003;41: Borel N, Doherr MG, Vretou E, et al: Seroprevalences for ovine enzootic abortion in Switzerland. Prev Vet Med 2004;65: Jee J, DeGraves FJ, Kim T, et al: High prevalence of natural Chlamydophila spp. infection in calves. J Clin Microbiol 2004;42: Reinhold P, Jaeger J, Liebler-Tenorio E, et al: Impact of latent infections with Chlamydophila species in young cattle. Vet J 2008;175: Kemmerling K, Müller U, Mielenz M, et al: Chlamydophila species in dairy farms: polymerase chain reaction prevalence, disease association, and risk factors identified in a cross-sectional study in western Germany. J Dairy Sci 2009;92: Reinhold P, Sachse K, Kaltenboeck B: Chlamydiaceae in cattle: commensals, trigger organisms, or pathogens? Vet J 2011;189: Everett KDE, Bush RM, Andersen AA: Amended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int J Syst Bacteriol 1999;49: Clinical Theriogenology Volume 6, Number 3 September 2014

5 24. Wittenbrink MM, Horchler H, Bisping W: [The occurrence of Chlamydia psittaci in the genital tract and feces of slaughtered female cattle]. Zentralbl Veterinarmed B 1988;35: Sting R: Chlamydia psittaci Infektionen bei Kühen und weiblichen Schafen im nördlichen Baden-Württemberg. Tierärztliche Umschau1997;52: Cavirani S, Cabassi CS, Donofrio G, et al: Association between Chlamydia psittaci seropositivity and abortion in Italian dairy cows. Prev Vet Med 2001;50: Wang FI, Shieh H, Liao YK: Prevalence of Chlamydophila abortus infection in domesticated ruminants in Taiwan. J Vet Med Sci 2001;63: Kauffold J, Henning K, Bachmann R, et al: The prevalence of chlamydiae in bulls from six bull studs in Germany. Anim Reprod Sci 2007;102: Teankum K, Pospischil A, Janett F, et al: Prevalence of chlamydiae in semen and genital tracts of bulls, rams and bucks. Theriogenology 2007;67: Petit T, Spergser J, Aurich J, et al: Prevalence of Chlamydiaceae and Mollicutes on the genital mucosa and serological findings in dairy cattle. Vet Microbiol 2008;127: Kaltenboeck B, Hehnen HR, Vaglenov A: Bovine Chlamydophila spp. infection: do we underestimate the impact on fertility? Vet Res Commun 2005;29: Sachse K, Vretou E, Livingstone M, et al: Recent developments in the laboratory diagnosis of chlamydial infections. Vet Microbiol 2009;135: Godin AC, Bjorkman C, Englund S et al: Investigation of Chlamydophila spp. in dairy cows with reproductive disorders. Acta Vet Scand 2008;50: Ruhl S, Casson N, Kaiser C, et al: Evidence for Parachlamydia in bovine abortion. Vet Microbiol 2009;135: Kaltenboeck B, Heinen E, Schneider R et al: OmpA and antigenic diversity of bovine Chlamydophila pecorum strains. Vet Microbiol 2009;135: Perez-Martinez JA, Storz J: Chlamydial infections in cattle Part 1. Mod Vet Pract 1985;66: Longbottom D, Coulter LJ: Animal chlamydioses and zoonotic implications. J Comp Pathol 2003;128: Storz J, Carroll EJ, Stephenson EH, et al: Urogenital infection and seminal excretion after inoculation of bulls and rams with Chlamydiae. Am J Vet Res 1976;37: Amin AS, Darwish GM, Ziada MS, et al: Trial to control Chlamydia psittaci in processed buffalo semen. Assist Vet Med J 1999;40: Storz J, Carroll EJ, Ball L, et al: Isolation of a psittacosis agent (Chlamydia) from semen and epididymitis of bulls with seminal vesiculitis syndrome. Am J Vet Res 1968;29: Eckert T, Goericke-Pesch S, Kauffold J, et al. Role of chlamydiae in bovine seamen [abstract]. Reprod Domest Anim 2014:49: Kauffold J, Melzer F, Berndt A, et al: Chlamydiae in oviducts and uteri of repeat breeder pigs. Theriogenology 2006;66; Clinical Theriogenology Volume 6, Number 3 September