mycoplasma hyorhinis infection of pigs sinsui2010 02 a rovira et al

s9

Acta Scientiae Veterinariae. 38(Supl 1): s9-s15, 2010.

ISSN 1678-0345 (Print)ISSN 1679-9216 (Online)

Mycoplasma hyorhinis infection of pigs

Infecção por Mycoplasma hyorhinis em suínos

Albert Rovira1, Maria Jose Clavijo M.1 & Simone Oliveira1

I. INTRODUCTION

II. ETIOLOGY

III. EPIDEMIOLOGY

IV. CLINICAL SIGNS AND LESIONS

V. PATHOGENESIS

VI. DIAGNOSTICS

VI. TREATMENT

VII. CONCLUSION

VIII. REFERENCES

Acknowledgements:

We would like to thank Dr. Nubia Macedo for translating the abstract into Portuguese.

ABSTRACT

Mycoplasma hyorhinis is a common inhabitant of the respiratory tract of pigs. Although most infections aresubclinical, when M. hyorhinis becomes systemic it causes severe disease consisting of pleuritis, pericarditis, peritonitisand arthritis, mainly in 3 to 10-week-old pigs. In addition to polyserositis and arthritis, M. hyorhinis has been associatedwith a number of clinical presentations including rhinitis, pneumonia, otitis and conjunctivitis. However, the significanceof M. hyorhinis in these disease presentations is unclear. M. hyorhinis colonizes the cilia of the respiratory epithelium.However, the mechanisms that allow M. hyorhinis to become systemic and cause disease are not well understood. Itappears that differences in M. hyorhinis strain virulence, the host immune response and concomitant infections allplay a role. At the Minnesota Veterinary Diagnostic Laboratory, most cases of serositis or arthritis are tested for M.hyorhinis by PCR. Of these, approximately 55% of samples from serosal surfaces and 12% of samples from affected

1College of Veterinary Medicine, University of Minnesota.Corresponding author: Albert Rovira, DVM, MS, PhDAddress: 1333 Gortner AveSaint Paul, MN 55108Email: [email protected] / [email protected]: (612) 625-7702Fax: (612) 624-8707

s10

Rovira A, Clavijo MJ, Oliveira S. 2010. Mycoplasma hyorhinis infection of pigs. Acta Scientiae Veterinariae. 38 (Supl 1): s9-s15

joints were positive by PCR. Coinfections with other respiratory pathogens are common in cases of polyserositisassociated with M. hyorhinis. In most cases, M. hyorhinis seems to act as a secondary pathogen. Nevertheless, M.hyorhinis is an important contributor to disease and mortality in nursery pigs in North America.

Key-words: Mycoplasma hyorhinis, Polyserositis, Arthritis, Pneumonia, PCR.

RESUMO

Mycoplasma hyorhinis é um habitante normal do trato respiratorio de suínos. Embora a maioria das infecçõessejam subclínicas, se o M. hyorhinis atingir a circulacão sanguínea, esta bactéria pode causar doença grave compleurite, pericardite, peritonite e artrite, principalmente em suínos de 3 a 10 semanas de idade. Além de polisserositee artrite, M. hyorhinis tem sido relacionado a outras apresentações clínicas, tais como rinite, pneumonia, otite econjuntivite. Entretanto, ainda não se sabe qual seria o papel de M. hyorhinis nessas doenças. M. hyorhinis colonizao epitélio ciliar do trato respiratório. Mas os mecanismos utilizados por essa bactéria para atingir a corrente sanguíneaainda não são conhecidos. Existem evidencias de que diferenças de virulência entre as diversas amostras de M.hyorhinis, a resposta imune do hospedeiro e outras infecções simultâneas participariam desse processo. No Laboratóriode Diagnostico da Universidade de Minnesota, a maioria dos casos de serosite ou artrite são testados para M.hyorhinis por PCR. Desses casos, aproximadamente 55% das amostras de superfícies serosas e 12% das amostrasde articulações afetadas são positivas pelo PCR. Infecções com outros patogenos respiratórios são comuns emcasos de polisserosite associada com M. hyorhinis. Na maioria dos casos, M. hyorhinis parece agir como patogenosecundário. Apesar disso, M. hyorhinis é um importante causador de doença e mortalidade em leitões de creche naAmerica do Norte.

Descritores: Mycoplasma hyorhinis, Polisserosite, Artrite, Pneumonia, PCR.

I. INTRODUCTION

Mycoplasmas are the smallest free-living organisms capable of self-replication. Mycoplasma hyorhinis isone of the mycoplasmas that can cause disease in swine. Disease associated to M. hyorhinis was first described inthe 1950’s and extensively investigated in the 1960’s and 1970’s. During the last years there has been a renewedinterest in this pathogen, perhaps due to the ability to easily detect it by PCR. The purpose of this review is to providean overview of M. hyorhinis scientific knowledge accumulated during the last 60 years, from the findings of the earlymycoplasma researchers to the latest reports. Information on the role of M. hyorhinis as a contaminant of cell culturelines is not covered in this review.

II. ETIOLOGY

Mycoplasmas were first described in 1898 as the causal agent of contagious bovine pleuropneumonia [32].These organisms were later classified as mollicutes [7], which is a class that contains 111 other mycoplasmaorganisms. Mycoplasmas are the smallest free-living organisms capable of self-replication. They are highly pleomorphicdue to the lack of a cell wall, thus they present a triple layer membrane. These organisms measure 0.2-0.3 ìm [17].Mycoplasma hyorhinis was the first mycoplasma isolated from swine [40]. Because mycoplasmas have a smallgenome they have special requirements for in vitro culture. In general, initial isolation of mycoplasmas is performedin a rich liquid media that must contain brain heart infusion and swine and/or horse serum among other components.From positive liquid cultures, single M. hyorhinis colonies can be isolated on solid media, where they grow in two tofive days and measure 0.5 mm to 1 mm in diameter [25]. Colonies grow down in the agar and some areas grow overthe central embedded area giving the colony the appearance of “fried eggs” [17].

M. hyorhinis is a heterogeneous species as was originally shown by the variable serologic reactions ofdifferent isolates to specific antisera [9]. This antigenic heterogeneity is, at least in part, determined by variablelipoproteins on the surface of the mycoplasma. M. hyorhinis possesses a highly complex system of variable lipoproteinexpression which allows for tremendous surface variation, potentially contributing to avoid the host immune reaction


s11

[46]. In addition to this antigenic heterogeneity, several experimental inoculation studies have shown differences invirulence in vivo [13,27].

III. EPIDEMIOLOGY

M. hyorhinis is a common inhabitant of the respiratory tract of pigs that, under certain conditions can causesevere systemic disease. Isolation of M. hyorhinis associated with clinical disease has been reported in most swineproducing countries of Europe, North America and Asia. However, because most studies have been done in slaughterpigs or in pigs submitted to diagnostic laboratories, there is little known about the epidemiology of M. hyorhinis inswine farms. It is assumed that piglets get infected from the sows or from older pigs and most of them do not developdisease [9,25,43]. Friis & Feenstra [10] studied clinical cases with typical lesions of serositis in 3 to 7-wek-old pigssubmitted to a diagnostic laboratory in Denmark. M. hyorhinis was isolated from 82% of lungs, 35% of serosalsurfaces, 27% of brains, 25 % of tonsils and 20% of joints of pigs with serositis. In a small sample of pigs with norespiratory or serosal lesions, M. hyorhinis was isolated from 87% of lungs, 37% of tonsils and 25% of brains but notfrom serosal surfaces or joints. In multiple studies M. hyorhinis was isolated from the respiratory tract of both healthyand diseased pigs. Typically, the rate of isolation was higher in diseased pigs than in healthy pigs. In normal pigs, therate of isolation tended to be higher in studies that used younger pigs, compared to those using slaughter pigs. Inanother study with Danish pigs, M. hyorhinis was isolated from the tympanic cavities of 80% of pigs with otitis mediaand 52% of pigs with no lesions [11]. Schulman et al. [38] isolated M. hyorhinis from the nasal cavity of 49% of pigswith rhinitis submitted to a diagnostic laboratory in Finland, while 27% of pigs with no lesions of rhinitis were alsopositive. Similarly, they found 49% of lungs with pneumonia and 17% of normal lungs to be positive. In a differentstudy performed on slaughtered pigs in Norway, 37% of pneumonic lungs were positive for M. hyorhinis while only 6%of normal lungs were positive [8]. In other studies the rate of M. hyorhinis isolation from pneumonic lungs was 62%[9,29] and 74% [1]. More recent studies have used PCR to detect M. hyorhinis in field samples with similar results.Caron et al. [4] tested lungs from Canadian slaughter pigs for M. hyorhinis by PCR and found 13% of pneumonic lungspositive and only 2% of normal lungs positive. In a recent study in Germany, 80% of pneumonic lungs and 37% ofnormal lungs from slaughter pigs were positive for M. hyorhinis by PCR [33].

IV. CLINICAL SIGNS AND LESIONS

Most infections are limited to the upper respiratory tract and sometimes the lung and are subclinical.Experimentally, intranasal inoculation with M. hyorhinis generally results in subclinical infection [9,13,27,31]. However,when M. hyorhinis becomes systemic it can cause severe disease consisting of pleuritis, pericarditis, peritonitis andarthritis, mainly in 3 to 10-week-old pigs. Clinical signs vary depending on the serosal surfaces affected and includefever, dyspnea, swollen joints, lameness, reluctance to move and unthriftiness. Lameness can become chronic andlast up to six months. The polyserositis consists of fibrinous or fibrinopurulent pleuritis, pericarditis and/or peritonitis.If the pig survives, lesions progress to chronic serositis with formation of adhesions [6,35]. The arthritis is characterizedby hypertrophy and hyperemia of the synovial membrane and lymphocyte infiltration with a serosanguinolent exudate,sometimes containing fibrin [2]. In chronic arthritis, pannus formation and articular erosion have been described [25].Ultrastructural changes have been described elsewhere [5]. Polyserositis and arthritis have been reproducedexperimentally by intraperitoneal inoculation [2,5,10,13,15,26,28,35,40] and, in some cases, by intranasal inoculation[13,15,25] of M. hyorhinis.

In addition to polyserositis and arthritis, M. hyorhinis has been associated with a number of clinicalpresentations including rhinitis, pneumonia, otitis and conjunctivitis [30,31,38,43]. However, the significance of M.hyorhinis in these disease presentations is unclear. It is important to remember that M. hyorhinis is a ubiquitousorganism that grows easily in culture media and therefore isolation of M. hyorhinis from a diseased animal does notimply causality. In addition, only mild, self-limiting forms of rhinitis, otitis and pneumonia have been reproducedexperimentally by inoculation of M. hyorhinis. The role of M. hyorhinis in swine pneumonia has been a question ofdebate for decades [16,27,41]. As described in the previous section, M. hyorhinis is isolated more frequently inpneumonic than in normal lungs. However, experimental inoculation of pigs with M. hyorhinis rarely produces pneumonia

s12


and, when it does, it is mild and only observed in a small percentage of the infected pigs [9,20,27]. Currently, M.hyorhinis is considered a secondary invader of pneumonic lesions.

V. PATHOGENESIS

M. hyorhinis has been detected by immunofluorescence and/or immunohistochemistry on the ciliary areaof the epithelium in nasal cavity, auditory canal, trachea and bronchi of asymptomatic pigs [20,30]. In pigs withpolyserositis, M. hyorhinis antigen has been reported within pleural, pericardial and synovial lesions [15,26,34]. Inpigs with pneumonia, M. hyorhinis was detected coating the bronchiolar epithelium and in the bronchial and alveolarexudate [15,29]. However, the mechanisms that allow M. hyorhinis to colonize the respiratory tract and to becomesystemic and cause disease are not well understood. It seems that pathogen factors, host factors and environmentalfactors all play a role. There are no known virulence factors for M. hyorhinis. However, differences in virulence betweenstrains have been demonstrated in experimental inoculation studies [13,27,36].

The host genetics also seem to play a role in the severity and the presentation of disease. Magnusson etal. [28] inoculated two lines of pigs selected for high and low immune response intraperitoneally with M. hyorhinis.They found that pigs selected for high immune response tended to develop arthritis while in pigs selected for lowimmune response the disease presented as polyserositis [28]. In a different study, pigs appeared to become moreresistant with age [13].

Environmental factors such as coinfections with other pathogens or stressful events are probably animportant contributor to expression of disease. Kinne et al. [20] reported an effect of stress on the development ofpneumonia after inoculation with M. hyorhinis. Several studies reported an increased rate of M. hyorhinis isolationfrom pigs infected with PRRSV [19,21,22,39], PCV2 [18] or Bordetella bronchiseptica [14] and suggested a synergisticeffect of these coinfections.

VI. DIAGNOSTICS

Clinical signs and lesions of M. hyorhinis polyserositis are undistinguishable from those produced by otherbacteria, mainly Haemophilus parasuis. Therefore, for an accurate diagnosis, isolation or detection of M. hyorhinisfrom characteristic lesions is required. Isolation of Mycoplasma hyorhinis requires special media but can beaccomplished relatively easily [25]. Detection of Mycoplasma hyorhinis antigen in serosal surfaces and joint tissueby immunohistochemistry or immunofluorescence has been reported [15,26,34]. Binder et al. [3] reported thatimmunofluorescence was less sensitive than culture for lung samples. Several protocols for detection of Mycoplasmahyorhinis DNA by PCR from clinical samples have been published [4,22] and PCR is currently performed in somediagnostic laboratories. Serological tests have also been developed and an antibody response has been observed inpigs 1 to 2 weeks after inoculation [6,12,35]. However, serology is not available in routine diagnostic laboratories.

During the last years, we have observed an increase in the number of cases of M. hyorhinis polyserositis.It is not clear whether that reflects a real increase in the prevalence of this disease or it is the result of an improvedability to detect M. hyorhinis due to the introduction of PCR. At the Minnesota Veterinary Diagnostic Laboratory, mostcases of serositis or arthritis received are tested for M. hyorhinis. Of these, approximately 55% of samples fromserosal surfaces and 12% of samples from affected joints were positive by PCR [37]. Coinfections with other respiratorypathogens are common in cases of polyserositis associated with M. hyorhinis. In a study involving 320 cases ofpolyserositis and arthritis submitted to the Minnesota Veterinary Diagnostic Laboratory, cases that tested positive forM. hyorhinis were also more likely to be positive for PRRSV, H. parasuis, S. suis, P. multocida, B. bronchiseptica andswine influenza virus. The association with H. parasuis was particularly strong. Most cases of polyserositis wereeither positive for both pathogens (40%) or negative for both pathogens 28%) by PCR [37]. This could indicate asynergistic mechanism or, more likely, that both pathogens are secondary to a common triggering factor such asrespiratory disease.


s13

VI. TREATMENT

Because mycoplasmas don’t have a cell wall, they are naturally resistant to certain antibiotics such aspenicillins and cephalosporins. However, several in vitro antimicrobial studies have shown that M. hyorhinis is susceptibleto multiple antibiotics. In one study where the minimal inhibitory concentration of 51 antimicrobial agents was evaluatedby serial broth dilution, M. hyorhinis was susceptible to lincomycin, clindamycin, furaltadona, kanamycin and allsulfonamides. In contrast M. hyorhinis was found to be resistant to all cephalosporines and penicillins [44]. Other invitro studies tested 18 different antibiotics by broth and agar dilution and found that this pathogen was highly susceptibleto oxytetracyclin, lincomycin and tylosyn, however it was also demonstrated that M. hyorhinis was highly resistant toerythromycin [24,42,45]. Recent studies have shown that macrolide-resistant M. hyorhinis strains quadrupled in thelast decade in Japan, allegedly due to multiple use of antimicrobial agents as chemotherapy [23]. Unfortunately, thereare no published reports of the efficacy of these antibiotics under field conditions. It has been reported that antibiotictreatment of M. hyorhinis infections is only successful when applied at the early stages of disease [43].

VII. CONCLUSIONS

Mycoplasma hyorhinis has been recognized as a cause of polyserositis and arthritis in pigs for decades.However, in the last years we have observed an increase in the rate of detection of this pathogen. In most cases, M.hyorhinis seems to act as a secondary pathogen. Nevertheless, M. hyorhinis is an important contributor to diseaseand mortality in nursery pigs in North America.

VIII. REFERENCES

[1] Assunção P., De la Fe C., Kokotovic B., González O. & Poveda J.B. 2005. The occurrence of mycoplasmas in the lungs of swinein Gran Canaria (Spain). Veterinary Research Communications. 6: 453-462.

[2] Barthel C.H., Duncan J.R. & Ross R.F. 1972. Histologic and histochemical characterization of synovial membrane from normal andMycoplasma hyorhinis-infected swine. American Journal of Veterinary Research. 33(12): 2501-2510.

[3] Binder A., van Wees C., Likitdecharote B. & Kirchhoff H. 1989. Fluorescence serological and culture detection of Mycoplasmahyopneumoniae and Mycoplasma hyorhinis in swine lungs. Berl Munch Tierarztl Wochenschr. 102(1): 11-13.

[4] Caron J., Ouardani M. & Dea S. 2000. Diagnosis and differentiation of Mycoplasma hyopneumoniae and Mycoplasma hyorhinisinfections in pigs by PCR amplification of the p36 and p46 genes. Journal of Clinical Microbiology. 38(4): 1390-1396.

[5] Duncan J.R. & Ross R.F. 1969. Fine structure of the synovial membrane in Mycoplasma hyorhinis arthritis of swine. American Journalof Pathology. 57(1): 171-186.

[6] Duncan J.R. & Ross R.F. 1973. Experimentally induced Mycoplasma hyorhinis arthritis of swine: pathologic response to 26thpostinoculation week. American Journal of Veterinary Research. 34(3): 363-366.

[7] Edward D.G. & Freundt E.A. 1956. The classification and nomenclature of organisms of the pleuropneumonia group. Journal of GeneralMicrobiology. 14: 197-207.

[8] Falk K., Høie S. & Lium B.M. 1991. An abattoir survey of pneumonia and pleuritis in slaughter weight swine from 9 selected herds. II.Enzootic pneumonia of pigs: microbiological findings and their relationship to pathomorphology. Acta Veterinaria Scandinavica. 32(1): 67-77.

[9] Friis N.F. 1971. Mycoplasmas cultivated from the respiratory tract of Danish pigs. Acta Veterinaria Scandinavica. 12(1): 69-79.

[10] Friis N.F. & Feenstra A.A. 1994. Mycoplasma hyorhinis in the etiology of serositis among piglets. Acta Veterinaria Scandinavica. 35(1):93-98.

[11] Friis N.F., Kokotovic B. & Svensmark B. 2002. Mycoplasma hyorhinis isolation from cases of otitis media in piglets. Acta VeterinariaScandinavica. 43(3): 191-193.

[12] Gois M., Franz J., Kuksa F., Pokorný J. & Cerný M. 1972. Immune response of gnotobiotic piglets infected with mycoplasmahyorhinis. Zentralbl Veterinarmed B. 19(5): 379-390.

[13] Gois M. & Kuksa F. 1974. Intranasal infection of gnotobiotic piglets with Mycoplasma hyorhinis: differences in virulence of the strainsand influence of age on the development of infection. Zentralbl Veterinarmed B. 21(5): 352-361.

[14] Gois M., Kuksa F. & Sisák F. 1977. Experimental infection of gnotobiotic piglets with Mycoplasma hyorhinis and Bordetella bronchiseptica.Zentralbl Veterinarmed B. 24(2): 89-96.

s14


[15] Gois M., Pospisil Z., Cerny M. & Mrva V. 1971. Production of pneumonia after intransal inoculation of gnotobiotic piglets with threestrains of Mycoplasma hyorhinis. Journal of Comparative Pathology. 81(3): 401-410.

[16] Gois M., Valícek L. & Sovadina M. 1968. Mycoplasma hyorhinis, a causative agent of pig pneumonia. I. Zentralbl Veterinarmed B. 15(2):230-240.

[17] Hayflick F. & Chanock R.M. 1965. Mycoplasma species of man. Bacteriological Reviews. 29: 185-221.

[18] Kawashima K., Katsuda K. & Tsunemitsu H. 2007. Epidemiological investigation of the prevalence and features of postweaningmultisystemic wasting syndrome in Japan. Journal of Veterinary Diagnostic Investigation. 19(1): 60-68.

[19] Kawashima K., Yamada S., Kobayashi H. & Narita M. 1996. Detection of porcine reproductive and respiratory syndrome virus andMycoplasma hyorhinis antigens in pulmonary lesions of pigs suffering from respiratory distress. Journal of Comparative Pathology.114(3): 315-323.

[20] Kinne J., Johannsen U., Neumann R., Mehlhorn G. & Pfutzner H. 1991. The pathology and pathogenesis of experimentalMycoplasma hyorhinis infection of piglets with and without thermomotoric stress. 1. Pathologico-anatomic, histologic andimmunomorphologic study results. Zentralbl Veterinarmed A. 38(4): 306-320.

[21] Kixmöller M., Ritzmann M., Eddicks M., Saalmuller A., Elbers K. & Fachinger V. 2008. Reduction of PMWS-associated clinicalsigns and co-infections by vaccination against PCV2. Vaccine. 26(27-28): 3443-3451.

[22] Kobayashi H., Morozumi T., Miyamoto C., Shimizu M., Yamada S., Ohashi S., Kubo M., Kimura K., Mitani K., Ito N. & YamamotoK. 1996. Mycoplasma hyorhinis infection levels in lungs of piglets with porcine reproductive and respiratory syndrome (PRRS). Journalof Veterinary Medical Science. 58(2): 109-113.

[23] Kobayashi H., Nakajima H., Shimizu Y., Eguchi M., Hata E. & Yamamoto K. 2005. Macrolides and lincomycin susceptibility ofMycoplasma hyorhinis and variable mutation of domain II and V in 23S ribosomal RNA. Journal of Veterinary Medical Science. 67(8): 795-800.

[24] Kobayashi H., Sonmez N., Morozumi T., Mitani K., Ito N., Shiono H. & Yamamoto K. 1996. In vitro susceptibility of Mycoplasmahyosynoviae and M. hyorhinis to antimicrobial agents. Journal of Veterinary Medical Science. 58(11):1107-1111.

[25] Kobisch M. & Friis NF. 1996. Swine mycoplasmoses. Revue scientifique et technique (International Office of Epizootics). 15(4):1569-1605.

[26] L’Ecuyer C. & Boulanger P. 1970. Enzootic pneumonia in pigs: identification of a causative mycoplasma in infected pigs and in culturesby immunofluorescent staining. Canadian Journal of Comparative Medicine. 34(1): 38-46.

[27] Lin J.H., Chen S.P., Yeh K.S. & Weng C.N. 2006. Mycoplasma hyorhinis in Taiwan: diagnosis and isolation of swine pneumoniapathogen. Veterinary Microbiology. 115(1-3): 111-116.

[28] Magnusson U., Wilkie B., Mallard B., Rosendal S. & Kennedy B. 1998. Mycoplasma hyorhinis infection of pigs selectively bred forhigh and low immune response. Veterinary Immunology and Immunopathology. 61(1): 83-96.

[29] Meyling A. 1971. Mycoplasma suipneumoniae and Mycoplasma hyorhinis demonstrated in pneumonic pig lungs by the fluorescentantibody technique. Acta Veterinaria Scandinavica. 12(1): 137-141.

[30] Morita T., Muraki Y., Awakura T., Shimada A. & Umemura T. 1993. Detection of Mycoplasma hyorhinis in porcine eustachitis. Journalof Veterinary Medical Science. 55(3):475-477.

[31] Morita T., Ohiwa S., Shimada A., Kazama S., Yagihashi T. & Umemura T. 1999. Intranasally inoculated Mycoplasma hyorhiniscauses eustachitis in pigs. Veterinary Pathology. 36(2): 174-178.

[32] Nocard E. & Roux E. 1990. Classic in infectious diseases. The microbe of Pleuropneumonia. 1896. Reviews of Infectious Diseases. 12:354-358.

[33] Palzer A., Ritzmann M., Wolf G. & Heinritzi K. 2008. Associations between pathogens in healthy pigs and pigs with pneumonia.Veterinary Record. 162(9): 267-271.

[34] Potgieter L.N. & Ross R.F. 1972. Demonostration of Mycoplasma hyorhinis and Mycoplasma hyosynoviae in lesions of experimentallyinfected swine by immunofluorescence. American Journal of Veterinary Research. 33(1): 99-105.

[35] Roberts E.D., Switzer W.P. & Ramsey F.K. 1963. Pathology of the visceral organs of swine inoculated with Mycoplasma hyorhinis.American Journal of Veterinary Research. 24: 9-18.

[36] Ross R.F. & Switzer W.P. 1963. Comparison of isolates of Mycoplasma hyorhinis by indirect hemagglutination. American Journal ofVeterinary Research. 24: 622-627.

[37] Rovira A. 2009. Review of Mycoplasma hyorhinis. In: Proceedings of the 36th Allen D. Leman Swine Conference (Saint Paul, U.S.A.).pp.87-88.

[38] Schulman A., Estola T. & Garry-Andersson A.S. 1970. On the occurrence of Mycoplasma hyorhinis in the respiratory organs of pigs,with special reference to enzootic pneumonia. Zentralbl Veterinarmed B. 17(5): 549-553.

[39] Shimizu M., Yamada S., Murakami Y., Morozumi T., Kobayashi H., Mitani K., Ito N., Kubo M., Kimura K. & Kobayashi M. 1994.Isolation of porcine reproductive and respiratory syndrome (PRRS) virus from Heko-Heko disease of pigs. Journal of VeterinaryMedical Science. 56(2): 389-391.

[40] Switzer W.P. 1955. Studies on infectious atrophic rhinitis. IV. Characterization of a pleuropneumonia-like organism isolated from thenasal cavities of swine. American Journal of Veterinary Research. 16(61Part 1): 540-544.

[41] Taylor-Robinson D. 1975. The importance of mycoplasmas in respiratory infections. Developments in biological standardization. 28:86-100.


s15

[42] Ter Laak E.A., Pijpers A., Noordergraaf J.H., Schoevers E.C. & Verheijden J.H. 1991. Comparison of methods for in vitro testing ofsusceptibility of porcine Mycoplasma species to antimicrobial agents. Antimicrobial Agents and Chemotherapy. 35(2): 228-233.

[43] Thacker E.L. 1996. Mycoplasmal Diseases. In: Straw B.E., Zimmerman J.J., D´Allaire S. & Taylor D.J. (Eds). Diseases of swine. 9th ed.Ames: Blackwell Publishing, pp.701-717.

[44] Williams P.P. 1978. In vitro susceptibility of Mycoplasma hyopneumoniae and Mycoplasma hyorhinis to fifty-one antimicrobial agents.Antimicrobial Agents and Chemotherapy. 14(2): 210-213.

[45] Wu C.C., Shryock T.R., Lin T.L., Faderan M. & Veenhuizen M.F. 2000. Antimicrobial susceptibility of Mycoplasma hyorhinis.Veterinary Microbiology. 76(1): 25-30.

[46] Yogev D., Rosengarten R., Watson-McKown R. & Wise K.S. 1991. Molecular basis of Mycoplasma surface antigenic variation: anovel set of divergent genes undergo spontaneous mutation of periodic coding regions and 5' regulatory sequences. EMBO Journal.10(13): 4069-4079.

www.ufrgs.br/favet/revista

Supl 1

mycoplasma hyorhinis infection of pigs sinsui2010 02 a rovira et al

Documents