DOI: 10.1002/vms3.665 ORIGINAL ARTICLE Health status of free-ranging pure and cross-mixed miniature swine population from Northeast Spain Vicente Soler1 Encarna Casas2 Francesc Closa-Sebastià2 Albert Sanz3 Jaume Martorell1,4 1 Servei dt’Animals Exòtics, Fundació Hospital Clínic Veterinari, Universitat Autònoma de Abstract Barcelona, Barcelona, Spain Background: Miniature pigs have gained popularity as companion animals in the recent 2 Vets and Wildlife, Terrasa, Spain years in Spain. Due to the fact that their abandonment and crossing breeds with wild 3 Servei de Prevenció en Salut Animal, Departament dt’Agricultura, Ramaderia, Pesca boars can cause severe problems, investigation about the health status is needed. i Alimentació, Generalitat de Catalunya, Gran Objectives: The aim of this study was to determine their health status according to the Vía de les Corts Catalanes, Barcelona, Spain 4 clinical findings during physical examination and the results of antibody serology tests Departament de Medicina i Cirurgía Animals, Facultat de Veterinaria, Universitat Autònoma against selected infectious diseases. de Barcelona, Barcelona, Spain Methods: Two-hundred and eleven miniature pigs (Sus scrofa) were included in the Correspondence study. Their origin, age, sex, housing conditions and diet were recorded. Jaume Martorell, Servei dt’Animals Exòtics, Results: The housing of the animals ranged from wild animals to ones living in ani- Fundació Hospital Clínic Veterinari, Universitat Autònoma de Barcelona, 08193, Bellaterra, mal sanctuaries. The diet varied from a natural one in the wild to commercial and Barcelona, Spain. homemade food. Thirty animals out of two-hundred and eleven were hybrids between Email: jaumem3@gmail.com miniature pigs and wild boars according to morphological characteristics. Antibody serology techniques of Influenza A virus, Hepatitis E virus, brucellosis, tuberculosis, African swine fever, Classical swine fever and Aujeszky’s disease was performed. The prevalence for Influenza A was 5.30%, for Hepatitis E was 5.35% and the rest tested negative. It is important to control and monitor these zoonotic infections to prevent Public Health problems. Conclusions: The results obtained from this investigation demonstrated that the ani- mals’ health status in this study is optimal and the diseases prevalence is similar or minor when compared to previous studies. This study confirms the hybridization of miniature pig and wild boar in Catalonia. KEYWORDS health status, hybrid, miniature pig, serology, Spain 1 INTRODUCTION Miniature pigs’ husbandry depends on the captivity purposes, and environment enrichment is essential to avoid boredom and to pre- Miniature pigs (Sus scrofa domesticus) are subspecies of the domestic vent destructive behaviour (Amalraj et al., 2018). Mini pigs are omniv- pig. There are 45 different breeds of miniature pigs described world- orous, but a restricted low energy diet is recommended in pigs kept wide (Amalraj et al., 2018). They have gained popularity as companion as pets to prevent obesity. The most appropriate diet for miniature animal in the recent years (Sipos et al., 2007). pigs should be approximately 12% protein, 2% fat and 12%–15% fibre This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Veterinary Medicine and Science published by John Wiley & Sons Ltd. 170 wileyonlinelibrary.com/journal/vms3 Vet Med Sci. 2022;8:170–176. SOLER ET AL . 171 (Tynes, 1999). The most common problems observed in pet minipigs 2 MATERIALS AND METHODS are parasitic infections, skin disorders, gastrointestinal, urogenital, res- piratory, reproductive tract disorders and locomotor problems (Amal- This study included 211 miniature pigs of different ages and sexes from raj et al., 2018; Sipos et al., 2007). a North-East region of Spain (Catalonia) during December 2018 to Jan- Currently, the abandonment of miniature pigs and crossing breeds uary 2020. Thirty animals out of two hundred and eleven were hybrids with wild boars can cause problems in public health since the animals between miniature pig and wild boar according to morphological char- inhabit in urban or semi-urban areas where their control and eradica- acteristics (Delibes–Mateos & Delibes, 2013). Hybrids may show char- tion is difficult, thus requiring more strict regulations to control owner- acteristics of both animals as a more compact body and longer legs, ship to prevent uncontrolled breeding and infection among wild boars, longer hair or even absence thereof, long snout or also appearance semi-wild pigs and farm pigs (Delibes–Mateos & Delibes, 2013; Royal of animals with flat snout (Figure 1). All the animals came from the Decree 1392/2012). Notifiable diseases in pigs in Spain include, among provinces of Barcelona (Vallés Oriental, Vallés Occidental, Baix Llobre- others brucellosis, African swine fever (ASF), classical swine fever (CSF) gat and Bages) and Tarragona (Tarragonés and Baix Penedés) (Figure 2). and Aujeszky’s disease (AD). The origin of the animals ranged from free-living in the wild to pigs Due to the lack of information on infectious diseases in miniature rescued from different animal sanctuaries. Data collection was divided pigs, the data have been extrapolated from farm pigs (VanderWaal & in sex, age, feeding, housing, region of Catalonia and relevant clinical Deen, 2018) and from previous studies in wild boar (Closa-Sebastià findings. The animals were divided in three age categories: piglet (less et al., 2011). than 3 months), young adults (between 3 and 6 months) and adults Brucellosis is an important human pathogen causing zoonosis (Pilo (more than 6 months). The animals’ diets were classified according to et al., 2015). In pigs, brucellosis can provoke abortions, infertility and the information collected from the animal sanctuaries and the veteri- orchitis (Escobar et al., 2013). narians participating in the study as commercial food (pellet and seed ASF includes per-acute, acute, sub-acute and chronic mani- mixture), natural diet from the environment (fresh fruit, vegetables and festations that can result in skin erythema, pulmonary oedema, tubers) and homemade food (food scraps and human waste products). splenomegaly, haemorrhagic lymphadenitis, petechial haemorrhages According to the housing conditions, pigs were classified as miniature in lungs, urinary bladder and kidneys. Other clinicals signs are pigs living in natural lands or forests (free-living in the wild), outdoor delayed growth, emaciation, joint swelling and skin ulcers (Yoo et al., concrete soil (urban, semi-urban areas and agricultural land) and out- 2020). door enclosure (animal sanctuaries). CSF produces marked fever, loss of appetite and lethargy. Haem- All wild animals and sanctuary animals in this study were caught orrhage in the kidneys, digestive tract lymph node, urinary bladder using containment techniques such as nets or fencing approved by an and necrosis in the tonsils and spleen is also observed (Sun et al., ethics committee. This study was performed under the supervision and 2011). following the ethics guidelines of the ‘Servei de Prevenció en Salut Ani- AD provokes respiratory, reproductive and neurological disorders in mal’, Departament dt’Agricultura, Ramaderia, Pesca i Alimentació. Gen- pigs and wild boars (Cano-Terriza et al., 2019). eralitat de Catalunya. An informed owner consent was obtained from The rest of the diseases tested in this serological survey were based the director of each sanctuary. on its zoonotic potential including swine influenza, hepatitis E and All the individuals were sedated using a combination of tiletamine- tuberculosis (TB). zolazepam (6 mg/kg, Zoletil, Virbac Salud Animal, Espluges de Llobre- Swine influenza A virus (IAV) is antigenically related to human gat, Spain) and xylazine (3 mg/kg, Xilagesic 20%, Calier Laboratories, influenza virus (Crisci et al., 2013). Typical clinical signs are character- Les Franqueses del Vallés, Spain) administered intramuscularly. Phys- ized by fever of short duration, inappetence, lethargy, coughing, dysp- ical examination included determination of body condition, hydration noea and nasal discharge. status, abdominal palpation, palpation of the lymph nodes and cardiac Hepatitis E virus (HEV) is the most common cause of acute viral and pulmonary auscultation. Fifteen millilitres of whole blood were hepatitis worldwide in humans. The virus is normally apathogenic in obtained using an 18 Ga 1 ½ t’t’ disposable needles (Sterican, Bbraun, pigs but can enhance the pathogenicity of other viruses (Rose et al., Rubí and Spain) and 20 ml syringes (Omnifix, Bbraun, Rubí and Spain) 2011). from the caudal cava vein of each pig. Serum samples were submitted to Tuberculosis: Mycobacterium complex is a multi-host disease that is external laboratories for antibody serology detection. Sera were stored shared among farm animals, wildlife and sporadically humans causing at −20◦ C until analyses. granulomatous lesions mainly in respiratory and gastrointestinal tract TB tests were performed by Centre de Reserca de Sanitat Animal, (Pérez de Val et al., 2017). Bellaterra, Spain (CReSA), and the rest of serologies were sent to Lab- The aim of this study is to perform antibody serology techniques oratori de Sanitat Animal de Catalunya, Lleida, Spain (LaSAC). Serolog- against Brucellosis, IAV, HEV, TB, ASF, CSF and ADV to evaluate the ical details are presented in Table 1. conditions of origin housing and diet to know the minipig health sta- The prevalence of the diseases was estimated from the ratio of pos- tus to prevent zoonotic infections and to demonstrate the existence of itive samples to the total number of samples analyzed, with confidence hybrids of miniature pigs and wild boars in a North-East region of Spain. intervals of 95%. 172 SOLER ET AL . FIGURE 1 Hybrids showing morphological characteristics of wild boar and miniature pig TA B L E 1 Serological information according to disease, laboratorial technique and trademark Disease Laboratorial technique Trademark Tuberculosis ELISA Nunc-Maxisorp; Thermo Fisher Scientific, Roslilde, Denmark Influenza A Indirect ELISA INgezim Influenza Porcina Ingenasa Madrid, Spain Blocking ELISA Idexx Influenza A Idexx, Westbrook, Maine, USA Hepatitis E Indirect ELISA PrioCheck HEV Ab porcine Prionics AG, Neuried, Germany Brucellosis Bengal Rose Complement fixation African swine fever Blocking ELISA INgezim PPA Compac Ingenasa, Madrid, Spain Classical swine fever Blocking ELISA Idexx CSFV Ab Idexx, Westbrook, Maine, USA Aujeszky Blocking ELISA Civtest Suis ADV gE Hipra, Gerona, Spain 3 RESULTS miniature pig and wild boar. Serological results are presented in Table 4. The weight of the animals in the study ranged from 4 to 80 kg (26 ± 19.64 kg). Physical examination, including determination of body con- dition, hydration status, abdominal palpation, palpation of the lymph 4 DISCUSSION nodes and cardiac and pulmonary auscultation, was unremarkable, but different relevant clinical findings were recorded. Two animals pre- This study evidences the presence of pet pigs stablished in the wild due sented nail overgrowth, seven animals had scabs (3.31%), 16 females to deliberate or accidental abandonment, resulting in establishments were pregnant and three males were cryptorchid. Geographical distri- in new colonies (Delibes–Mateos & Delibes, 2013). The presence of bution, sex, diet, age and clinically relevant findings are presented in pregnant females, piglets and hybrids in the study demonstrated the Tables 2 and 3. hybridization between miniature pigs and wild boars in Catalonia, since Two hundred and eleven animals were included in the present study. animals of different age, sex and species were found coexisting but not Thirty animals out of two hundred and eleven were hybrids between being castrated. SOLER ET AL . 173 TA B L E 2 Animal distribution according to origin, sex, housing, diet and relevant clinical findings of the animals sampled in the study Relevant clinical Origin Sex Housing Diet findings BCN TAR ♂ ♀ ♂N ♀S A B C COM NAT HOM Yes No Miniature pigs Piglet 5 9 13 1 9 5 9 5 Young adult 39 32 33 20 12 6 37 19 15 17 31 23 21 Adult 57 39 46 37 3 10 52 44 23 50 23 7 Hybrids Piglet Young adult 14 1 6 9 6 2 7 2 3 10 Adult 6 9 11 4 7 8 7 8 Total 121 90 109 71 15 16 102 82 27 58 92 61 28 Note: A, forest; B, outdoor cement; C, outdoor enclosure. Abbreviations: BCN, Barcelona; COM, commercial; HOM, homemade; NAT, natural; TAR, Tarragona. current study, only two animals out of 211 animals (0.94%) presented overgrown nails. In miniature pigs, lameness is often associated with a poor husbandry and soft surfaces that do not allow an adequate hoof wear (Tynes, 1999). This issue can be solved with the use of more abra- sive surfaces and nail trimming (Amalraj et al., 2018; Tynes, 1999). All the animals of the study with nail overgrowth were outdoor concrete soil and outdoor enclosure. Tusk overgrowing is another problem that can occur in miniature pigs, as this grows throughout the life of the ani- mal (Tynes, 1999). This item has not been shown in the study. Influenza A virus (IV) can infect a wide range of species, including human beings, and remains one of the major threats to human health. Pigs are one of the hosts for the virus and play an important role in its epidemiology (Crisci et al., 2013). Pigs are susceptible to IV from avian and human viruses and can act as reservoirs of the disease for humans, stablishing themselves as zoonoses (Crisci et al., 2013). In fact, the ori- F I G U R E 2 Geographical distribution of the animals sampled in gin of several IV pandemics such as the ones that took place in 1957, this study in the provinces of Barcelona and Tarragona, Catalonia, 1968 and 2009 were traced down to pigs (Garten et al., 2009 ). In a Spain. 1: Vallés Oriental. 2: Vallés Occidental. 3: Baix Llobregat. 4: Bages. 5: Tarragonés. 6: Baix Penedés previous study of farm pigs from Spain, the seroprevalence of swine influenza ranged from 23.4% to 87.3%. In the case of the region of Cat- alonia, the virus reached 79.7% (Simon-Grifé et al., 2011) while in wild TA B L E 3 Animal distribution according to municipality and boars it was about 6.4% (Closa-Sebastià et al., 2011). From the results province of the animals sampled in the study of this study, only 5.3% of the animals tested positive for influenza Barcelona Tarragona virus, four animals out of six positives belonged to animal sanctuary, VO VOC BL BA TAR BP increasing the risk of transmission with caretakers of the centre. Two Miniature pigs 33 5 54 9 40 40 animals out of the six positive ones, were free-living animals, enhanc- Hybrids 2 11 7 10 ing the dissemination of this disease in wildlife populations as seen in previous reports (Closa-Sebastià et al., 2011; Simon-Grifé et al., 2011). Total 35 16 61 9 40 50 This result is lower than in previous reports done in farm pigs and wild Abbreviations: BA, Bages; BP, Baix Penedés; BL, Baix Llobregat; TAR, Tar- boars. The best way to control the disease is surveillance plans. ragonés; VO, Vallés Oriental; VOC, Vallés Occidental. HEV is an infectious disease present in wild boars and domestic pigs (Rose et al., 2011). This disease is considered an emerging zoono- Despite the different kind of diet between free-ranging animals sis in many developing countries. As opposed, in industrialized coun- and animals living in sanctuaries, no signs of obesity or thinness were tries, it occurs sporadically (Pavio et al., 2010). This virus is known to observed, considering all the animals in a proper body condition. be responsible for 20 million of new infections, 3.3 million of acute A low percentage of skin lesions as scabs, scars and papules have hepatitis E and 44,000 deaths from acute liver failure in human beings been found (seven out of 211 animals), despite the fact that pigs can be every year (Sooryanarain & Meng, 2020). It is suggested that zoono- aggressive when sharing small enclosures (Amalraj et al., 2018). In the sis can happen through meat consumption and/or contact with infected 174 SOLER ET AL . TA B L E 4 Results of serologies, affected animals and number of tests performed in the present study Disease Affected animals (%) Number of tests performed Tuberculosis 0% 136 Influenza A 5.30% (four out of six in animal sanctuaries) 113 Hepatitis E 5.35% (five out of six in animal sanctuaries) 112 Brucellosis 7.14% Bengal Rose 210 0% complement fixation 15 African swine fever 0% 211 Classical swine fever 0% 211 Aujeszky 0% 209 wildlife (Rivero-Juarez et al., 2018) or direct contact with infected pigs tive samples for Bengal Rose were negative to complement fixation and (Sooryanarain & Meng, 2020). Pigs are a natural reservoir for the HEV were therefore sorted out as negative. (Salines et al., 2017). It is reported that mingling practices, nursery pro- TB is an infectious disease caused by a range of Mycobacterium cedures and poor hygiene are risk factors that ease the spread of the complex species. It is a multi-host disease which can infect farm ani- disease (Salines et al., 2017). Some experimental studies showed that mals, wildlife and sporadically humans (Pérez de Val et al., 2017). The HEV strains could be transmitted from European wild boars to domes- Eurasian wild boar has been documented as a maintenance host in tic pigs (Jori et al., 2016 ), but further investigation is needed. A previ- the Mediterranean countries (Pérez de Val et al., 2017). In 2004, an ous report in Europe showed that the prevalence of HEV in wild boars outbreak of TB in wild boars was detected in Spain. The outbreak fluctuated between 2% and 68% (Rivero-Juarez et al., 2018). In the was originated in territories where cows and wild boars shared water case of Spain, the prevalence varied from 19.6% (de Deus et al., 2008) and food, which resulted in close contact between these two popula- to 23.2% (Rivero-Juarez et al., 2018). The present study found a preva- tions and facilitated the spreading of the disease (Hermoso de Men- lence of Hepatitis E of 5.35%, where five animals out of the six posi- doza et al., 2006). The prevalence of TB reached 70% in adult wild tives ones were from sanctuary, increasing the risk of zoonosis among boar (Mentaberre et al., 2014), another study in wildlife of the Doñana caretakers, because this disease is asymptomatic in pigs (Rivero-Juarez National Park showed a prevalence of 76.7% in wild boar (Barroso et al., et al., 2018). One animal out of six positive animals was in the free-living 2020). In addition, a previous study in Catalonia revealed a TB preva- group, enhancing the risk of spreading the disease to others, because it lence of 7.6% in wild boar (Ciaravino et al., 2020); however, all the sam- was living in wildlife (Sooryanarain & Meng, 2020; Rivero-Juarez et al., ples tested in this study were negative for Mycobacterium, being a dif- 2018). The best ways to control this disease are wildlife, farm livestock ferent result compared to other parts of Spain. surveillance plans and strict veterinary and sanitary control (Jiménez ASF is a high mortality viral disease. The natural hosts are wild De Oya et al., 2011). suids and arthropods, being asymptomatic in the natural swine reser- Brucellosis is a zoonotic infection caused by Brucella suis. This voir hosts. However, in the domestic pig, the infection is lethal (Galindo pathogen affects domestic and feral pigs (Pilo et al., 2015). Porcine bru- & Alonso, 2017). Although the disease was eradicated in Europe in cellosis is a re-emerging disease in South-East Asia and South Amer- the 1990s with the exception of Sardinia (Italy), different outbreaks in ica and a potential arising infection in some countries since B. suis is 2007 and 2014 were observed in eastern countries (Galindo & Alonso, a common finding in wild boar population and its dissemination from 2017). However, Spain is free of this disease. Efficient measures are wild boar to outdoor-reared pigs is reported (Pilo et al., 2015). In case quarantine and biosecurity, animal movement restrictions and slaugh- of humans, this disease is associated with direct contact with infected tering affected and exposed animals (Galindo & Alonso, 2017). In pre- animals, genital secretions and poor hygiene measures (Escobar et al., vious studies of wild boars in Poland, ASF virus was detected, and this 2013). The most effective measures to control the disease are com- fact may contribute to the spread of this disease (Blome et al., 2012). plete separation between wild boars and domestic pig population and The European Commission has recommended procedures for the con- surveillance of brucellosis in wildlife (Pilo et al., 2015). In the study, two trol of ASF in domestic pig and wild boar populations. In the present different laboratory techniques were used for the diagnosis of brucel- study, all the samples tested were negative for ASF, which correlates losis according to the World Organization for Animal Health (OIE). The with the results shown in a previous report in wild boars in Catalonia first technique was the Bengal Rose, which allows an initial screening (Closa-Sebastià et al., 2011). on the field (Farro et al., 2002), 15 animals out of 210 tested positive. CSF is one of the most important viral diseases of domestic pigs and Positive samples were then tested with complement fixation test to wild boars due to its impact on animal health and pig industry world- confirm the presence of Brucella spp. Complement fixation technique wide (Blome et al., 2017). Control measures include stamping out of discriminates non-specific agglutinins better (Farro et al., 2002). This infected herds, delimitation of restriction zones and movement restric- fact could explain the difference obtained from both tests. All 15 posi- tions (Ganges et al., 2020). Another measure described to maintain the SOLER ET AL . 175 disease under control was the vaccination of wild boars because it is Catalunya. An informed owner consent was obtained from the director known that wild boars are an important reservoir of the virus (Sophie of each Sanctuary. Rossi et al., 2015). A previous study in Bama miniature pigs showed that this breed was highly susceptible to a highly virulent CSF virus DATA AVAILABILITY STATEMENT strain (Sun et al., 2011). According to the World Organization for Ani- The authors confirm that the data supporting the findings of this study mal Health (2021), CSF has been currently eradicated from Spain. In are available within the article. this study, all the samples taken for CSF tested negative, which was the expected result. PEER REVIEW AD is a domestic swine disease with significant economic relevance The peer review history for this article is available at https://publons. that causes large losses in the swine industry due to declining produc- com/publon/10.1002/vms3.665 tion and trade restrictions (Boadella et al., 2012; Meier et al., 2015; Vicente-Rubiano et al., 2014). Due to eradication programmes, AD ORCID does not occur in domestic swine (Vicente-Rubiano et al., 2014). The Jaume Martorell https://orcid.org/0000-0001-9031-0042 natural hosts of this disease are Suidae. It is widely recognized that wild boars can act as a reservoir of AD (Boadella et al., 2012), along REFERENCES with wild boar transmission of the virus to the domestic pig (Vicente- Amalraj, A., Matthijs, A., Schoos, A., Neirynck, W., De Coensel, E., Bernaerdt, Rubiano et al., 2014). As a consequence, disease surveillance in wild E., & Maes, D. (2018). 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