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

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

Mycoplasma hyorhinis infection of pigs Infeco por Mycoplasma hyorhinis em sunos

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 are subclinical, when M. hyorhinis becomes systemic it causes severe disease consisting of pleuritis, pericarditis, peritonitis and arthritis, mainly in 3 to 10-week-old pigs. In addition to polyserositis and arthritis, M. hyorhinis has been associated with a number of clinical presentations including rhinitis, pneumonia, otitis and conjunctivitis. However, the significance of 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. It appears that differences in M. hyorhinis strain virulence, the host immune response and concomitant infections all play 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

College of Veterinary Medicine, University of Minnesota. Corresponding author: Albert Rovira, DVM, MS, PhD Address: 1333 Gortner Ave Saint Paul, MN 55108 Email: rove0010@umn.edu / albertus2002@hotmail.com Phone: (612) 625-7702 Fax: (612) 624-8707

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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 polyserositis associated 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 um habitante normal do trato respiratorio de sunos. Embora a maioria das infeces sejam subclnicas, se o M. hyorhinis atingir a circulaco sangunea, esta bactria pode causar doena grave com pleurite, pericardite, peritonite e artrite, principalmente em sunos de 3 a 10 semanas de idade. Alm de polisserosite e artrite, M. hyorhinis tem sido relacionado a outras apresentaes clnicas, tais como rinite, pneumonia, otite e conjuntivite. Entretanto, ainda no se sabe qual seria o papel de M. hyorhinis nessas doenas. M. hyorhinis coloniza o epitlio ciliar do trato respiratrio. Mas os mecanismos utilizados por essa bactria para atingir a corrente sangunea ainda no so conhecidos. Existem evidencias de que diferenas de virulncia entre as diversas amostras de M. hyorhinis, a resposta imune do hospedeiro e outras infeces simultneas participariam desse processo. No Laboratrio de Diagnostico da Universidade de Minnesota, a maioria dos casos de serosite ou artrite so testados para M. hyorhinis por PCR. Desses casos, aproximadamente 55% das amostras de superfcies serosas e 12% das amostras de articulaes afetadas so positivas pelo PCR. Infeces com outros patogenos respiratrios so comuns em casos de polisserosite associada com M. hyorhinis. Na maioria dos casos, M. hyorhinis parece agir como patogeno secundrio. Apesar disso, M. hyorhinis um importante causador de doena e mortalidade em leites de creche na America do Norte. Descritores: Mycoplasma hyorhinis, Polisserosite, Artrite, Pneumonia, PCR.

I. INTRODUCTION
Mycoplasmas are the smallest free-living organisms capable of self-replication. Mycoplasma hyorhinis is one of the mycoplasmas that can cause disease in swine. Disease associated to M. hyorhinis was first described in the 1950s and extensively investigated in the 1960s and 1970s. During the last years there has been a renewed interest in this pathogen, perhaps due to the ability to easily detect it by PCR. The purpose of this review is to provide an overview of M. hyorhinis scientific knowledge accumulated during the last 60 years, from the findings of the early mycoplasma researchers to the latest reports. Information on the role of M. hyorhinis as a contaminant of cell culture lines 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 mycoplasma organisms. Mycoplasmas are the smallest free-living organisms capable of self-replication. They are highly pleomorphic due to the lack of a cell wall, thus they present a triple layer membrane. These organisms measure 0.2-0.3 m [17]. Mycoplasma hyorhinis was the first mycoplasma isolated from swine [40]. Because mycoplasmas have a small genome they have special requirements for in vitro culture. In general, initial isolation of mycoplasmas is performed in 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 to five days and measure 0.5 mm to 1 mm in diameter [25]. Colonies grow down in the agar and some areas grow over the 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 of different isolates to specific antisera [9]. This antigenic heterogeneity is, at least in part, determined by variable lipoproteins on the surface of the mycoplasma. M. hyorhinis possesses a highly complex system of variable lipoprotein expression which allows for tremendous surface variation, potentially contributing to avoid the host immune reaction

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

III. EPIDEMIOLOGY
M. hyorhinis is a common inhabitant of the respiratory tract of pigs that, under certain conditions can cause severe systemic disease. Isolation of M. hyorhinis associated with clinical disease has been reported in most swine producing countries of Europe, North America and Asia. However, because most studies have been done in slaughter pigs or in pigs submitted to diagnostic laboratories, there is little known about the epidemiology of M. hyorhinis in swine farms. It is assumed that piglets get infected from the sows or from older pigs and most of them do not develop disease [9,25,43]. Friis & Feenstra [10] studied clinical cases with typical lesions of serositis in 3 to 7-wek-old pigs submitted to a diagnostic laboratory in Denmark. M. hyorhinis was isolated from 82% of lungs, 35% of serosal surfaces, 27% of brains, 25 % of tonsils and 20% of joints of pigs with serositis. In a small sample of pigs with no respiratory or serosal lesions, M. hyorhinis was isolated from 87% of lungs, 37% of tonsils and 25% of brains but not from serosal surfaces or joints. In multiple studies M. hyorhinis was isolated from the respiratory tract of both healthy and diseased pigs. Typically, the rate of isolation was higher in diseased pigs than in healthy pigs. In normal pigs, the rate of isolation tended to be higher in studies that used younger pigs, compared to those using slaughter pigs. In another study with Danish pigs, M. hyorhinis was isolated from the tympanic cavities of 80% of pigs with otitis media and 52% of pigs with no lesions [11]. Schulman et al. [38] isolated M. hyorhinis from the nasal cavity of 49% of pigs with rhinitis submitted to a diagnostic laboratory in Finland, while 27% of pigs with no lesions of rhinitis were also positive. Similarly, they found 49% of lungs with pneumonia and 17% of normal lungs to be positive. In a different study 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 lungs positive and only 2% of normal lungs positive. In a recent study in Germany, 80% of pneumonic lungs and 37% of normal 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 and arthritis, mainly in 3 to 10-week-old pigs. Clinical signs vary depending on the serosal surfaces affected and include fever, dyspnea, swollen joints, lameness, reluctance to move and unthriftiness. Lameness can become chronic and last 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 characterized by 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 reproduced experimentally 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 clinical presentations 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 ubiquitous organism that grows easily in culture media and therefore isolation of M. hyorhinis from a diseased animal does not imply causality. In addition, only mild, self-limiting forms of rhinitis, otitis and pneumonia have been reproduced experimentally by inoculation of M. hyorhinis. The role of M. hyorhinis in swine pneumonia has been a question of debate for decades [16,27,41]. As described in the previous section, M. hyorhinis is isolated more frequently in pneumonic than in normal lungs. However, experimental inoculation of pigs with M. hyorhinis rarely produces pneumonia

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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 area of the epithelium in nasal cavity, auditory canal, trachea and bronchi of asymptomatic pigs [20,30]. In pigs with polyserositis, M. hyorhinis antigen has been reported within pleural, pericardial and synovial lesions [15,26,34]. In pigs with pneumonia, M. hyorhinis was detected coating the bronchiolar epithelium and in the bronchial and alveolar exudate [15,29]. However, the mechanisms that allow M. hyorhinis to colonize the respiratory tract and to become systemic and cause disease are not well understood. It seems that pathogen factors, host factors and environmental factors all play a role. There are no known virulence factors for M. hyorhinis. However, differences in virulence between strains 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 et al. [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 low immune response the disease presented as polyserositis [28]. In a different study, pigs appeared to become more resistant with age [13]. Environmental factors such as coinfections with other pathogens or stressful events are probably an important contributor to expression of disease. Kinne et al. [20] reported an effect of stress on the development of pneumonia after inoculation with M. hyorhinis. Several studies reported an increased rate of M. hyorhinis isolation from pigs infected with PRRSV [19,21,22,39], PCV2 [18] or Bordetella bronchiseptica [14] and suggested a synergistic effect of these coinfections.

VI. DIAGNOSTICS
Clinical signs and lesions of M. hyorhinis polyserositis are undistinguishable from those produced by other bacteria, mainly Haemophilus parasuis. Therefore, for an accurate diagnosis, isolation or detection of M. hyorhinis from characteristic lesions is required. Isolation of Mycoplasma hyorhinis requires special media but can be accomplished relatively easily [25]. Detection of Mycoplasma hyorhinis antigen in serosal surfaces and joint tissue by immunohistochemistry or immunofluorescence has been reported [15,26,34]. Binder et al. [3] reported that immunofluorescence was less sensitive than culture for lung samples. Several protocols for detection of Mycoplasma hyorhinis DNA by PCR from clinical samples have been published [4,22] and PCR is currently performed in some diagnostic laboratories. Serological tests have also been developed and an antibody response has been observed in pigs 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 improved ability to detect M. hyorhinis due to the introduction of PCR. At the Minnesota Veterinary Diagnostic Laboratory, most cases of serositis or arthritis received are tested for M. hyorhinis. Of these, approximately 55% of samples from serosal surfaces and 12% of samples from affected joints were positive by PCR [37]. Coinfections with other respiratory pathogens are common in cases of polyserositis associated with M. hyorhinis. In a study involving 320 cases of polyserositis and arthritis submitted to the Minnesota Veterinary Diagnostic Laboratory, cases that tested positive for M. hyorhinis were also more likely to be positive for PRRSV, H. parasuis, S. suis, P. multocida, B. bronchiseptica and swine influenza virus. The association with H. parasuis was particularly strong. Most cases of polyserositis were either positive for both pathogens (40%) or negative for both pathogens 28%) by PCR [37]. This could indicate a synergistic mechanism or, more likely, that both pathogens are secondary to a common triggering factor such as respiratory disease.

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VI. TREATMENT
Because mycoplasmas dont have a cell wall, they are naturally resistant to certain antibiotics such as penicillins and cephalosporins. However, several in vitro antimicrobial studies have shown that M. hyorhinis is susceptible to multiple antibiotics. In one study where the minimal inhibitory concentration of 51 antimicrobial agents was evaluated by serial broth dilution, M. hyorhinis was susceptible to lincomycin, clindamycin, furaltadona, kanamycin and all sulfonamides. In contrast M. hyorhinis was found to be resistant to all cephalosporines and penicillins [44]. Other in vitro studies tested 18 different antibiotics by broth and agar dilution and found that this pathogen was highly susceptible to oxytetracyclin, lincomycin and tylosyn, however it was also demonstrated that M. hyorhinis was highly resistant to erythromycin [24,42,45]. Recent studies have shown that macrolide-resistant M. hyorhinis strains quadrupled in the last decade in Japan, allegedly due to multiple use of antimicrobial agents as chemotherapy [23]. Unfortunately, there are no published reports of the efficacy of these antibiotics under field conditions. It has been reported that antibiotic treatment 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 disease and mortality in nursery pigs in North America.

VIII. REFERENCES
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