In October 2021, the responsible herd veterinarian of an Austrian piglet producing farm contacted the University Clinic for Swine, University of Veterinary Medicine Vienna, Austria and reported of sows in the gestation area presenting with bloody crusts on the whole skin surface of the body and of bleeding skin lesions. This sarcoptic mange free farm produced piglets in a three-week batch farrowing interval with 105 cross-bred sows (Large White x Landrace). Gilts were obtained from one sarcoptic mange negative gilt supplying farm and were kept in a separate isolation unit before being integrated in the sow herd. Prior to integration gilts were vaccinated against parvovirosis and erysipelas (Parvoruvac®, Merial SAS, Lyon, France) and treated with ivermectine (Ivomec 10 mg/ml, Boehringer Ingelheim Animal Health France SCS, Lyon, France) to prevent introduction of sarcoptic mange and round worms. Sows were dewormed twice a year alternately with fenbendazole (Panacur 4%, Intervet, Vienna, Austria) and flubendazole (Flubenol 50 mg/g, Elanco, Cuxhaven, Germany).
The farmer reported that in July 2021 a general cleaning of the gestation area was performed, when the sows were removed in two steps for cleaning using a high-pressure cold-water washer. Approximately three to four days thereafter a fast growing fly population could be observed in the gestation area. At that time the fly species was not determined, since neither the farmer nor the herd attending veterinarian were able to distinguish stable flies from house flies. The farmer used insecticides in August to control the fly population. From mid-October 2021 onwards, the fly population increased again since liquid manure from the nursery units was directed via a direct connection pipe to the slurry channel of the gestation area to make liquid manure more fluid and to break the crust of the manure cover. However, at that time the farmer and the herd attending veterinarian observed sows suffering from skin lesions that were either covered by bloody crusts or were bleeding. Additionally, the farmer reported of increased return-to-oestrus rates at that time, which were thought being related to a broken climate chamber for semen storage. At this time point the University Clinic for Swine got involved in the diagnostic work up.
Herd inspection and clinical examination of sows
A herd inspection was performed by veterinarians of the University Clinic for Swine. It had to be found out which fly species dominated in the gestation area and if the flies may be related with the skin lesions. All areas of the case farm were inspected starting with the farrowing units and ending at the gestation unit. At the time when the herd inspection was performed, 55 sows and one teaser boar were kept there. 33/55 sows showed moderate to severe skin lesions: bleeding skin parts, bloody crusts and red maculae (Fig. 1A) diffusely distributed over the whole body surface almost always covered by several flies (Fig. 1B). When looking in detail on the flies, 90% of the flies sitting on the skin lesions were individuals of Stomoxys calcitrans. The remaining 10% of the insect population consisted of Musca domestica, Drosophila spp. and species from the family of Psychodidae. Stable flies were not only found on the animals, but the majority was found resting on the walls and the ceiling of the gestation unit, a common behaviour of stable flies after having had blood meals (Supplementary File 1). Sows in the gestation area were evaluated as being stressed and showed permanent avoidance behaviour due to fly bites. Sows were lying and resting for short periods of a few minutes only to stand up again and escape from the stable flies. Some sows gave up standing up and escape from flies and stayed in resting position, but still showed reactions such as repelling flies with their legs or cutaneous reflex (Supplementary File 2). Rectal body temperature of bitten sows was not increased, and no further clinical symptoms could be observed. In the other different compartments of the case herd stable flies could be observed as well, but at much lower numbers. Sows in the farrowing unit similarly presented with reddened skin parts and lesions, but these were in remission and in a healing process, as there were only single stable flies present in the farrowing units. Sows in the farrowing units were subjectively evaluated as relaxed compared to the ones in the gestation unit showing low stress levels, as during inspection none of the sows reacted on our presence and either proceeded in resting in lateral recumbency or in suckling their litter. In the nursery unit, single stable flies could be observed on the walls of the different pens. In general, on a semi-quantitative level the infestation level with stable flies in the farrowing and nursery units was evaluated as low (a maximum of one stable fly sitting on one animal) whereas it was high in the gestation area (more than ten stable flies sitting on one animal). Reproduction data of sows, specifically farrowing rate and return-to-oestrus rate was divided into three parts: the time before the massive growth of fly populations in July 2021, the time from July 2021 until the end of October 2021 when the gestation area was heavily overpopulated with flies or stable flies and the time after October 2021 when rigorously insecticides were used to control flies. Mean values showed that during the time of fly overpopulation, the farrowing rate (83.33%) decreased due to an increased return-to-oestrus rate (16.67%). Once the fly population was almost decreased to a zero level after usage of insecticides the farrowing rate increased again (92.10%), and return-to-oestrus rate decreased to an acceptable level of 7.9% (Fig. 2).
To find out risk factors contributing to the huge stable fly population, the whole internal environment of the case herd was inspected with special focus on finding decomposing organic plant material, as this is known to be the main substrate for stable fly maggots to effectively develop [4,5,6]. In the gestation area and in the farrowing unit no relevant sources of decomposing organic matter could be found. However, a completely different situation was seen in the nursery unit where huge amounts of piglet feed were found below the slatted floors on the slurry starting to build a manure cover (Fig. 3). As the farmer reported of the transfer of liquid manure from the nursery unit to the gestation area to increase liquidity of the slurry and to break the manure cover there, the slurry channel of the gestation area was checked again for spots of decomposing organic matter. In some areas it was possible to find accumulation of decomposing feed on the manure cover in the gestation area together with typically long shaped pupae most probably of stable flies.
Swab samples of the skin lesions from four representative sows and stable fly specimen (4 pooled samples containing 10 individuals each) were collected for microbiological analysis. In all four swab samples high grade methicillin-resistant Staphylococcus (S.) aureus (MRSA) and S. hyicus (SH) could be found. In three samples high grade of Streptococcus dysgalactiae subsp. equisimilis (SDSE) and in one high grade S. microti was detected. All bacterial species were identified to the species level by matrix-assisted laser desorption ionization-time-of-flight mass spectrometry (MALDI-TOF MS) (Bruker Daltonik, Bremen, Germany) and further characterized by susceptibility testing and in case of MRSA the isolate of the swab of Sow 1 and Sow 4 exemplarily genotyped for all MRSA isolates by spa-, dru-typing and DNA based microarray . A summary of the results of microbiological investigations can be found in Supplementary File 3. Genes coding for exfoliative toxins of S. hyicus were analysed as previously described . MRSA isolates belonged to spa type t034, dru type dt6j, SCCmec type V/VT and clonal complex (CC) 398. Genetic resistance matched the phenotypic resistances of the respective isolates. The mecA, blaZ, tet(K) and tet(M) were observed. Full hybridisation results for MRSA isolates examined in this study can be found in Supplementary File 4. The PCR characterization of S. hyicus exfoliative toxin genes revealed that all isolates did not harbour any of examined genes. The preparation of stable flies was as previously described . For selective isolation of Staphylococcus sp., 200 µl of suspension containing bacteria from the fly surface were preincubated at 37 °C overnight in buffered peptone water (BPW) (Merck, Germany), wherefrom 200 µL were cultured at 37 °C in trypticase soy broth (TSB) (Becton Dickinson (BD), Heidelberg, Germany) with 6.5% (w/v) NaCl overnight and subsequently streaked onto a BBL CHROMagar MRSA II (Becton Dickinson, Heidelberg, Germany(BD)) and on Columbia CNA Improved II Agar with 5% (v/v) sheep blood (BD). All isolates showing typical staphylococcal colony appearance were identified by MALDI-ToF-MS revealing the presence of S. hyicus and S. simulans in each of the four stable fly suspensions. The susceptibility testing and the PCR characterization of S. hyicus exfoliative genes did not differ from the porcine isolates.
Recommendations to the farmer and further outcome
Veterinarians from the University Clinic for Swine together with the herd attending veterinarian and the farmer analysed the fly control program of the case farm for weak points that may be improved in future for prevention of any insect overpopulation. A major point for improvement was the time point of starting with insect control. The farmer reported that after cleaning the gestation area in July 2021 it took approximately two weeks until a massive fly population was recognized. Furthermore, the second increase of the fly population occurred at the beginning of October 2021 when liquid manure from the nursery unit was directed in the slurry channel of the gestation area. As plenty of wasted feed was observed on the manure cover of the nursery unit, it was hypothesized that once directed into the slurry channel of the gestation area the decomposing process started and may have established an important source for stable fly reproduction in the gestation area. The farmer was advised to regularly empty slurry channels of all different compartments directly into the slurry tanks to prohibit the transfer of wasted nursery feed. Additionally, he was advised to install fully non-slatted plates around the feeding troughs to reduce the spill over of feed directly into the slurry channel.
Since the high population density of stable flies in the gestation unit needed fast intervention to improve animal welfare and health of sows quickly, we recommended the use of adulticides together with larvicides to quickly and sustainably reduce the relative abundance of the stable flies close to zero.
We recommended to the farmer, whenever the relative abundance of stable flies increases in any of the different compartments of the case herd, control measures have to be applied immediately to stop further reproduction and spread within the farm. Waiting too long with starting fly control measures can have substantial impact on the reproduction rate of the stable fly population, as one female may produce a maximum of 820 eggs . Control measures referred to removal and reduction of reproduction niches of stable flies to break the development of maggots .
Regarding the skin lesions of sows, we recommended local treatment using zinc or silver sprays. In any case constitution of sows suffering from skin lesions should get worse, antimicrobial treatment of skin lesions with a thiamphenicol spray together with nonsteroidal antiphlogistic drugs was recommended.
According to the farmer, skin wounds healed without any therapeutic intervention once the adult and larval stable fly population was reduced and controlled. The farmer also reported that it took approximately four weeks until skin lesions healed, and reproductive performance reached again acceptable levels. One year after the massive outbreak of stable flies in the gestation unit, just single specimens of Stomoxys calcitrans were reported by the farmer, assuming that controlling reproduction of stable flies was successful. Since October 2021 no further massive occurrence of stable flies was observed in the case herd.