Introduction

Atrophic rhinitis is an infectious bacterial disease described in the early nineteenth century (Franque, 1830 - Germany). Thus, after nearly two centuries of existence, its infectious aetiology is precisely recognised a century later (Ratke, 1938 - Carlstrom, 1940) and there is still clinical evidence on pig farms around the world. It has occurred to a greater or lesser degree throughout this time and has been significantly prevalent in this first decade of the 21st century.

The first thing I would like to point out is that two sets of well-defined clinical symptoms are encompassed, at the same time, within this infectious disease. They are:

• Progressive Atrophic Rhinitis (PAR) caused by toxigenic type D Pasteurella multocida as its primary agent either alone or together with other infectious agents, the most characteristic of which is Bordetella bronchiseptica.
  
  
• Regressive or Non-progressive Atrophic Rhinitis (RAR), caused by toxigenic Bordetella bronchiseptica. This concept was coined by Pederson and Nielsen in 1983.

Both bacteria spread easily among the swine population, especially when control measures implemented are insufficient to eliminate them within the carriers existing on the farm.

The pigs themselves are the main transmitters of Bordetella bronchiseptica (breeders, piglets, fattening pigs and replacement gilts), and Pasteurella multocida is also able to spread to other animals such as rats, cats, dogs, birds, chickens, sheep, goats, cattle, horses, and even to humans (zoonoses). Without a doubt, the ability to persist and transmission of both bacteria on farms is very high.

The characteristic lesion caused by both bacteria is bone hypoplasia of nasal turbinates, of which pigs have two on each side: two ventral and two dorsal, so a total of four. The severity of infection is determined by the intensity of the damage in each of the four turbinates (conchae) and the nasal septum that can lead to a more or less alarming clinical atrophic rhinitis, which is linked to a more or less pronounced lateral or facial torsion, marked tearing, and even nasal haemorrhages. From what we have previously mentioned, the severity of clinical cases is higher in cases of progressive atrophic rhinitis caused initially by toxigenic Pasteurella multocida.

Another common factor in both clinical aspects of atrophic rhinitis (PAR and RAR) is the considerable loss of growth with the added factor of individual variability among pigs, which creates a great heterogeneity in the fatteners, which is affected by a high percentage of smaller pigs and an increase in the number of days at the fattening period and aggravated by the economic setback in the schedule of charges at the abattoir and the associated treatment costs.

Thus atrophic rhinitis is a disease with significant economic impact on our farms, which should lead us to take effective preventive measures for control and containment. We should also take into account that when we monitor farms that have demonstrated clinical symptoms, their absence during certain periods does not guarantee that the infection is absent from the breeders, so we may find clinical relapses over time.

Aethiology

The primary origin of atrophic rhinitis is found in the toxigenic strains of the bacteria, Pasteurella multocida and Bordetella bronchiseptica. The conditions for growth and colonisation of both bacteria needed to produce sufficient amounts of toxins are also determined by other infectious agents, both viral and bacterial, which can damage the nasal mucosa, as well as by multi-factorial environmental factors in regard to adverse management and infrastructure. Each and every one of these associated factors aggravates - to a greater or lesser extent - the clinical presence of atrophic rhinitis on each farm.

Both Pasteurella multocida and Bordetella bronchiseptica are Gramnegative bacteria of a similar size and aerobes with a coccobacilli shape. Both bacteria are involved in upper and lower respiratory tract disorders within the familiar Porcine Respiratory Disease Complex. We also know that pigs with atrophic rhinitis are more susceptible to respiratory complications.

We know the antigenic variation of both strains of Pasteurella multocida, as well as Bordetella bronchiseptica that to a certain extent determine which clinical features appear with the variable severity stemming from them.

Within these extrinsic factors, which play a decisive influence in the severity of atrophic rhinitis, we should point out the following:

Management and infrastructural factors:

• High proportion of nulliparous gilts: high annual renewal rate.
• Large farms with many animals in one space.
• High density of pigs.
• Frequent transfer and mixtures of animals.
• Poor adoption practices - cession of lactation.
• Insufficient control of surroundings (air renewal, oxygen concentration, levels of gases, variations in temperature of comfort, relative humidity).
• Mix of animals of different ages and/or origins.
• Deficient bio-safety practices: cleaning, washing, disinfection and depopulation.
• Physical contact of pigs with dogs, cats, rats or birds.

Nutritional factors:

• Flour feed with a high percentage of finely ground particles and dust.
• Losses of feed due to fissures, breakage in silos, distributors, etc.
• Balance of nutrients and digestible calcium/phosphorus ratio in growth and development phases.
• Nutritional deficiencies or imbalances that affect the immune system and/or digestive flora, unbalancing them.

Genetic factors: the role of heredity in the presentation of atrophic rhinitis was suggested three decades ago; it was considered highly variable according to lines and breeds of pigs (LW>LN). It was thought there was a genetic predisposition between lines and strains of toxigenic Pasteurella multocida that varied in susceptibility. Nowadays we know that the risk is in the those genetics that are carriers from the source farm which are multipliers of the toxigenic bacteria Pasteurella multocida and/or Bordetella bronchiseptica.

Epidemiology

Bordetella bronchiseptica and Pasteurella multocida very effectively colonise the mucosa of the respiratory tract after infection. These two bacteria are highly prevalent in the swine population to a greater degree than the clinical cases of atrophic rhinitis. With no problem, we could refer to this as an “iceberg disease”, in which only a small part of the health problem of our pigs is seen.

To correctly understand how clinical signs of atrophic rhinitis appear more or less suddenly on a farm, which we believed to be disease free, we should start with the idea that the infection and/or transmission of these two bacteria take place in the early phases of a piglet's life. We can isolate both bacteria in young piglets, especially at weaning. Bordetella bronchiseptica can cause respiratory problems even in those animals only a week old. It also easily colonises organs of the upper respiratory apparatus.

Young replacement gilts are considered a key factor in the origin and/or spread of atrophic rhinitis; they are active disseminators of both bacteria. The presence of clinical signs in them is definitive, although their absence does not exclude the fact that they may be carriers. Hence, an exhaustive knowledge of the state of health in regard to atrophic rhinitis, both progressive and regressive, of our replacement animals (self-replacement or purchase of gilts from outside) is essential in prevention and control programmes.

The infection cycle can be maintained on a farm over time by a very small group of gilts and/or breeders that are carriers, in which the bacteria are found in tonsils and intestines.

The entrance of positive replacement gilts into negative populations will give rise to rapid spread of both progressive and regressive atrophic rhinitis.

Breeder-carrier sows play a crucial role in the spread of infection within a farm and transmit both bacteria during lactation to offspring and/or piglets adopted by negative mothers. Similarly, the transmission of both bacteria between breeders (replacement gilts, sows in production and boars) is quite effective. At this point, we must consider the greater risk of transmission on farms where the sows are housed in groups for at least half of their production cycle and/or effective life. Neither bacteria involved in atrophic rhinitis are transmitted via semen or embryo transfer.

In addition to this vertical sow to piglet transmission in the early stages of life, horizontal transmission by aerosol and faecal matter intake between piglets when 5 to 8 weeks old is no less important. The greatest elimination of both bacteria takes place within 2-3 weeks after weaning, at the same time the starter phase begins. At this stage, the infection may become endemic if the associated factors mentioned above are favourable. The infection can be enhanced and spread rapidly among the population of both sows and especially susceptible piglets, and give rise to clinical symptoms of progressive or regressive atrophic rhinitis, with the aggravating circumstance that it usually occurs at a later age (fattening pigs), and this can lead to confusion at the time of first contact and subsequent decisions. We can thereby ensure that infections in a pig’s early age are vital for the later development of the disease.

Infections can last for months and are related to the degree and intensity of the infection. Likewise, the degree of lesions and clinical signs are in relation to whether the infection is early or late. The earlier it occurs, the more serious it is.

Passive protection of piglets from naturally infected sows makes it possible to reduce clinical incidence, but not their infection, which means the health risk remains when the piglets are weaned and, of course, when they go on to the growth and finishing phase.

Piglets from carrier mothers are infected from the second week of life onwards (up to six weeks), whereas if these sows are well vaccinated against Bordetella bronchiseptica and toxigenic Pasteurella multocida, the infective potential moves to 14-18 weeks when the development of progressive atrophic rhinitis is not feasible in intensive production with sacrifice at 22-25 weeks.

Thus is not uncommon to see on unvaccinated farms the transfer of piglets to fattening units that we believe are healthy, and when they reach 12-16 weeks of life, they show a severe progressive atrophic rhinitis. This is due to high toxin production by Pasteurella multocida type D between 8-10 weeks of age, coinciding with entry into the fattening period.

Both Bordetella bronchiseptica and Pasteurella multocida are sensitive to most disinfectants, as well as to low humidity and high temperatures (> 60 ºC for less than 15 minutes). Infection pressure can be reduced by the systemic depopulation between batches, washing with hot water and use of disinfectants.

Pathogenesis

The different types of mucin produced in the nasal mucosa of pigs at different ages tell us how both Bordetella bronchiseptica and Pasteurella multocida colonise the mucosa. Bordetella bronchiseptica colonises and adheres to the nasal mucosa where it preferentially attacks the ciliated epithelial cells. It multiplies on the mucosal surface and produces toxins that spread through the bone tissue of the turbinates causing degenerative, proliferative and inflammatory changes in the nasal epithelium with loss of cilia. There are variations between different strains according to their toxigenic capacity. Of the four turbinates, the two ventral ones are usually the most commonly affected. In severe cases, we see both the dorsal and ventral turbinates affected. Susceptibility to this degree of turbinate atrophy is reduced as the pig increases in age.

The modifications to the nasal epithelium caused by Bordetella bronchiseptica are a great breeding ground for favouring the proliferation of toxigenic type D Pasteurella multocida to produce epithelial hyperplasia, atrophy of the turbinates, mesenteric cell proliferation, osteolysis, and atrophy of nasal glands.

In controlled infections in piglets, it is feasible to have a partial or total regeneration of the epithelium of the turbinates, so that the degree of hypoplasia they undergo is related to a delay in their growth.

If we understand the importance of the nasal mucosa as a first line of organic defence, the partial or total destruction of the turbinates in cases of both progressive and regressive atrophic rhinitis leads to greater susceptibility to respiratory complications and other opportunistic infectious agents, whether from bacteria, viruses or parasites.

We can conclude that pathogenically the toxins of both bacteria are different and produce alterations of nasal turbinates by different mechanisms, which give rise to the symptoms of both regressive and progressive atrophic rhinitis.

Lesions and Clinical Signs

To gain a better understanding of clinical symptoms of atrophic rhinitis, we should give a prior explanation of the clinical set of lesions it causes. The gross lesions of both progressive and regressive atrophic rhinitis are centred on the nasal cavity and adjacent structures. The main lesions we can find are:

• Atrophy of ventral and dorsal turbinates indistinctly or separately in each individual with large variations in location and severity. In severe cases, these structures may even disappear.
• Atrophy and/or deviation of the nasal septum that may be symmetric or asymmetric, with upward or sideways deviation of the snout.
• Formation of mucopurulent exudates in the nasal cavity, which on occasion may be accompanied by blood.

We may observe in clinical pictures of atrophic rhinitis secondary complications, such as respiratory symptoms of the lower respiratory tract with lesions from bronchopneumonia in apical and cardiac lobes of the lung.

The microscopic lesions that serve as a reference after the obvious gross lesions are:

• Fibrosis of osseous plates of nasal turbinates.
• Inflammation of the laminates of the nasal mucosa with degenerative processes.
• The clinical symptoms of atrophic rhinitis may go unnoticed when they first appear, and even more so in cases of regressive atrophic rhinitis, in spite of the clinical evidence of the severe forms of progressive atrophic rhinitis.

We can clearly identify the clinical display of progressive atrophic rhinitis in fatteners, which is characterised by:

• Lateral or frontal deviation of the snout.
• Tearing and accumulated dirt in the corner of the eye due to occlusion of the nasolacrimal duct. This does not always have a linear direct relationship with atrophic rhinitis.
• Sneezing with or without nasal exudates.
• Epistaxis: blood in one or both of the nasal orifices.
• Facial deformations: wrinkles on the snout and face.
• Nasal hypertrophy on the sides of molars.
• Evident delay of between 16-19 per cent in growth rates with reference to the average rates quoted in the literature, which may exceed 30 per cent in conventional pigs depending on severity.
• Considerable increases of pigs with delayed growth, which leads to loss of maximum value when slaughtered.

Symptoms of regressive atrophic rhinitis are no less frequent in which clinical signs can be observed in young piglets (3-4 weeks of age or earlier) that, despite being less apparent, do not have a lower economic impact on production. In piglets affected by regressive atrophic rhinitis we can find:

• Frequent sneezing (we must differentiate coughing from sneezing).
• Snorts with mucopurulent nasal exudates of varying degrees.
• Less appetite than is normal for their physiology with delayed growth (25-40 grams per day).

Diagnosis

Diagnosing progressive atrophic rhinitis a priori is easier than diagnosing regressive atrophic rhinitis; it is based on clinical symptomatology. However on farms where large amounts of antibiotics are used, these external clinical symptoms may be hidden or masked.

In both cases, in addition to clinical diagnosis, we should ensure and confirm the disease with the aid of the following diagnostic techniques:

1. Post-mortem diagnosis based on a transversal cut of a pig's snout at the level of the first to second upper premolar, and assessing the degree of atrophy of each one of the four nasal turbinates. There are various techniques for creating these lesions (0 to 5), but they vary according to the instructor, in addition to not keeping a linear direct relation with the severity of the forms of atrophic rhinitis. A minimum number of snout samples are needed per batch so that the diagnosis is significant (20 per cent).
   
   
2. Subsequent bacteriological exam using pulmonary wash on live pig samples as well as those from the abattoir. It is much more precise than a study based on nasal swabs or nasal exudates samples. They should be shipped to the laboratory in phosphate saline solution and refrigerated (4-8ºC). The seedings are done in blood agar or MacConkey agar enriched with glucose 1 per cent. Analysis based on tonsils and lungs is frequently used as a basis for diagnosis. The determination of toxigenic strains is not easy using bacteriological culture techniques, which means it is highly unlikely that we will receive a definitive diagnosis.
   
   
3. Serology by detection of agglutinating antibodies in serum. The information from this technique is less specific than that from bacteriological culture in specific mediums. Serology does not differentiate between antibodies of infected pigs or vaccinated pigs. If they are not vaccinated, serology can help us in the primary diagnosis of atrophic rhinitis.
   
   
4. PCR technique specific for toxigenic strains of type D Pasteurella multocida.

We must take into account the following pathologies in regard to differential diagnosis of atrophic rhinitis:

• Infections by cytomegalovirus: rhinitis by inclusion bodies.
• Influenza virus.
• Aujeszky's disease.
• Porcine Reproductive and Respiratory Syndrome Virus.
• Poorly designed feeders and drinkers that determine maxillary deformations.

Prevention and Control

Occasional and/or isolated measures of treatment or handling are not sufficient for effectively resolving problems of either progressive or regressive atrophic rhinitis.

Precise knowledge of the farm or productive structure is critical for understanding the source of the problem while, at the same time, a laboratory diagnosis is needed to support the epidemiological and clinical diagnosis for the purpose of developing a programme of measures for treatment, control and future prevention of both progressive and regressive atrophic rhinitis.

To do so, we must consider all management and treatment measures, the surroundings, genetics, nutrition and specific vaccination procedures for preventing this infectious disease that has such a great economic impact on production. The economic losses in each case will justify the measures taken, because the return on investment for each of them is considerable.

Basis for the principal objectives of these measures should be the following points:

1. Reduce the prevalence - infection pressure of Bordetella bronchiseptica, and Pasteurella multocida, both in the future breeder gilts, as well as sows, piglets and fattening pigs.
   
   
2. Reduce the lesion scores in the nasal mucosa and turbinates to neutralise the economic losses stemming from them on the pigs’ production yields (growth, conversion).
   
   
3. Reduce the lesions for avoiding secondary bacterial infections that aggravate the process and its symptoms.
   
   
4. Improve conditions of environmental comfort that facilitate respiratory efficiency and the use of nutrients.

The first prevention measure against atrophic rhinitis would be preventing the entrance to the firm of the Bordetella bronchiseptica and toxigenic type D Pasteurella multocida bacteria, by means of unapparent carriers such as future breeder gilts. The following steps are needed to do so:

• Know the health origin of the replacement gilts, along with the treatment and vaccinations on the farm from which they come, with the firm commitment of the parties to be free of both progressive and regressive atrophic rhinitis.
• Absence of apparent clinical signs upon entry and during the strict nine-week quarantine phase.
• Vaccination and re-vaccination with a 3-to-4-week interval during the quarantine with an inactivated vaccine that contains both bacteria (Bordetella bronchiseptica and toxigenic type D Pasteurella multocida).

Once the gilts have entered the test farm, the use of a specific vaccination schedule is prescribed with a vaccine mentioned which includes:

• Primary vaccination: two doses, at 8-7 and 4-3 weeks prior to the indicated farrowing date. In acute cases, we can give a blanket double vaccination to the entire breeder herd, regardless of the state of reproduction in which they are found.
• Revaccination in the following gestation with a single dose between four and three weeks prior to the estimated farrowing date.

These highly effective vaccination measures, should, at all times, be accompanied by the prescribed measures shown in practice to be positive, listed below:

1. Strict depopulation practices: cleaning, washing, disinfection and time empty between production batches of lactating sows, piglets and fattening pigs. Washing will be even more effective if done with hot water.
   
   
2. Reduce the density of animals in the same space.
   
   
3. Strict measures of biosecurity: absence of cats, dogs, birds, rats; as well as contact with pigs with other susceptible production animals such a sheep, goats, cattle or horses.
   
   
4. Maintain correct environmental conditions on the farm: air renewal, gases and oxygen concentration, ranges of temperature and relative humidity, environmental dust, etc).

The additional combined use of therapeutic measures with vaccines that prevent Bordetella bronchiseptica and toxigenic type D Pasteurella multocida help us reduce the lesion severity and associated symptoms, particularly the acute clinical cases, while simultaneously improving production rates of infected pigs, both piglets and fatteners.

The main antibiotics that have been shown to be sensitive to Bordetella bronsicheptica and toxigenic Pasteurella multocida are:

• Tetracyclines: oxytetracycline, chlortetracycline and doxycycline.
• Sulfonamides + trimetoprim.
• Macrolides: tylosin, lincomycin, tilmicosin, tulathromycin.
• Florfenicol, enrofloxacins, ceftiofur sodium, tiamulin and penicillins.

It is important to choose the correct antibiotic, taking into account the age, dosage rate, timing, withdrawal periods and costs per pig. The combined use of therapeutics should always be assessed when using efficacious vaccination schedules, as well as the environmental, biosecurity, management and control of replacement gilts.

Bibliography

1. Cheville, N.F. 1999. Introduction to Veterinary Pathology. Iowa State University Press.
2. Martineau, J.P. 1997. Maladies d’èlevage des porc. Editions France Agricole.
3. Muirhead M. and T. Alexander. 2001. Manejo sanitario y Tratamiento de las enfermedades del cerdo. Interamericana Ediciones.
4. Plonait, H. 2001. Manual enfermedades del cerdo. Editorial Acribia
5. Rushton, J. 2009. The economics of animal health production. Cabi
6. Schwartz K.J. 2005. Manual enfermedades del porcino. Suis.
7. Sinis L.D. 1996. Pathology of the Pig. Pig Research and Development Corporation.
8. Straw B. 2006. Diseases of Swine. 9th Edition. Blackwell Publishing.
9. Taylor D.J. 1999. Pig Diseases. 7th Edition. St. Edmundsbury Press.

Further Reading Find out more information on atrophic rhinitis by clicking here.

November 2012