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. 2023 Oct 16;103(1):103197. doi: 10.1016/j.psj.2023.103197

Assessment of fungal contamination and biosecurity risk factors in duck-breeding farms in South Korea

Mina Han 1,1, Munhui Chae 1, Seongtae Han 1
PMCID: PMC10652118  PMID: 37925771

Abstract

Fungi are pathogens that infect all types of poultry and farmers, leading to economic losses in poultry production. Fungi can be isolated from environmental samples and are ubiquitous in the air. This study aimed to evaluate fungal contamination in domestic duck farm environments and analyze biosecurity risk factors associated with fungal infection incidence to assess the vulnerability of the farms to fungal infection.

The average fungal concentration was 203 colony-forming units (CFU)/m3 in the air and 365 × 103 CFU/m2 in the wall surface samples. Sixteen fungal genera were recovered from air and wall surface samples from 19 duck-breeding farms, Aspergillus being the most frequently isolated (air: 43.2%; wall surface: 40%). Eleven additional fungal genera (Acrophialophora, Byssochlamys, Fusarium, Lichtheimia, Paecilomyces, Penicillium, Polycephalomyces, Rhizomucor, Scopulariopsis, Talaromyces, and Thermoascus) were isolated from air samples. Also, 8 additional fungal genera (Chaetomium, Lichtheimia, Penicillium, Petriella, Rhizomucor, Rhizopus, Talaromyces, and Trichosporon) were isolated from wall surface samples. The characteristics of the poultry farms (geographic region, stocking density, breeding house type, affiliate, duck age, and season) and fungal concentrations in the air and wall surface samples were analyzed to evaluate the biosecurity risk of the farms. Fungal infections were significantly affected by high stocking density (>2 ducks/m2), duck age (18–25 wk and >60 wk), and high fungal concentration in the wall surface samples (>300 × 103 CFU/m2).

Key words: breeding farm, duck, fungal contamination, risk factor

INTRODUCTION

Fungi are ubiquitous in the air and can occur when environmental conditions are optimal for their growth (Tell, 2005; Dhama et al., 2013). Poultry are susceptible to fungal infections because of their anatomy (small and nonexpanding lungs and 9 air sacs for air passage) and high body temperature, which accelerate fungal growth (Tell, 2005). Exposure to fungal spores via the internal environment of farms with high humidity, poor ventilation, and moldy chaff bedding and feed can lead to fungal infection in birds (Hadrich et al., 2013), and this is more likely to occur in cases of compromised poultry immune function (Asfaw and Dawit, 2017).

Breeding ducks are egg-laying types bred to produce meat-type ducks. They are constantly exposed to conidia as they lay eggs in confinement until the end of their laying cycle. Moreover, their immune systems can be weakened by stress factors, such as lack of light, crowded housing, poor ventilation, and egg production (Elitok and Bingüler, 2018). These environments render breeding ducks susceptible to fungi, which are important pathogens that must be controlled on farms.

Fungi are always present in the air; thus, preventing and controlling fungal infections is difficult and causes economic losses in poultry production (Wingfield et al., 2021). Poultry infected with fungi exhibit clinical symptoms, such as difficulty breathing, anorexia, polydipsia, emaciation, reduced egg production, growth retardation, and sudden death (Ghori and Edgar, 1979). In South Korea, duck production and consumption have increased sharply since the early 2000s, and as a result, the duck population has increased (Kim et al., 2021). Therefore, the incidence of fungal infections is increasing, and effective prevention and control of this disease are needed (Wingfield et al., 2021).

Contamination by fungi that float in the air or adhere to wall surfaces poses significant health risks to ducks, farmers, and people living near farms (Wingfield et al., 2021). Identification and quantitative analysis of fungi on duck-breeding farms can provide clues regarding their relevance to fungal infections in these hosts. To allow for wider characterization of fungal contamination and a more accurate exposure assessment in the environment, both active and passive sampling methods should be used (Viegas et al., 2019). Active sampling is most commonly used for sampling airborne fungi that directly contact the culture media for a short period of time, and passive sampling uses surface swabs that can determine contamination levels of the environment over long periods of time (Haas et al., 2017; Viegas et al., 2019). Analysis of collected samples uses a culture method that allows for both quantitative and qualitative evaluation and determination of fungal growth (Viegas et al., 2020).

Biosecurity is the management of the risk of harm to animals, humans, and the environment due to the entering, outbreak, and spread of diseases (Robertson, 2020). Farm level biosecurity is a set of management practices that prevent the spread of infectious agents among groups of animals on a farm (Villarroel et al., 2007). Risk factors that pose potential threats to the farm can be demographic, management, and environmental, and the assessment of the association between risk factors and disease can prevent disease (Robertson, 2020). The biosecurity risk factors associated with mycosis should be evaluated to characterize outbreaks of fungal infections in duck breeding farms. Controlling the biosecurity risk factors that increase the prevalence of fungal infections may reduce the incidence.

This study aimed to investigate the fungal communities in the air and on the wall surfaces of duck-breeding farms in South Korea. The biosecurity risk factors of the farms were also evaluated to assess their vulnerability to fungal infections.

MATERIALS AND METHODS

Duck-Breeding Farms

According to statistics on livestock trends for the last quarter of 2020 released by Statistics Korea, 20% of all breeding ducks (>2,000 ducks/farm) are bred in North Chungcheong Province, the second largest of the 9 provinces in the country. Therefore, all 19 duck-breeding farms (Cheongju-si, n = 3; Jincheon-gun, n = 5; Eumseong-gun, n = 4; Yeongdong-gun, n = 1; Chungju-si, n = 1; and Goesan-gun, n = 5) were surveyed in North Chungcheong Province. Data on the locations, stocking densities, breeding house types, and affiliates of the 19 duck-breeding farms were collected.

Fungal Infections of Breeding Ducks

A total of 430 duck carcasses from the 19 duck-breeding farms were presented to the Institute of Chungbuk Provincial Veterinary Service and Research for postmortem examinations. We visited farms to collect carcasses that died from unknown causes that day. The number of sampling times ranged from 1 to 30. As traveling to the farms took approximately 2 h maximum, collected carcasses were placed in biohazard bags and transported directly to the laboratory for further investigation. From April 2019 to December 2020, between 9 and 62 carcasses of various ages (4–85 wk) were collected from each farm. Internal organs showing signs of fungal pneumonia and multifocal-to-coalesced white-to-yellow caseous nodules or white-to-greenish mold growth were collected to be cultured. The cross section of the nodule and the mold growth lesion were picked up with a 1 μL inoculating loop, spread on Sabouraud dextrose agar (SDA) and incubated at 33°C for 4 to 10 d. Cultured fungi were placed in 2 mL cryovials (to which 10% glycerol solution was added) and stored in a deep freezer at −40°C.

Air Sample Collection and Quantitative Analysis

Sampling from the 19 farms was performed using a Microbial Air Sampler PBS-E (Suzhou Norda Cleaning Tech Co., Ltd., Suzhou, China) at 3 locations (close to the entrance, middle of the breeding house, and back of the breeding house) in 3 randomly selected breeding houses in use. The air sampler loaded with SDA plates was placed 1.2 m above the ground (Figure 1A), and the air was collected at a velocity of 100 L/min for 3 min (Wang et al., 2012). The SDA plates were incubated for 4 to 10 d at 33°C. The cultured fungi were then identified (Zarrin et al., 2016), and the concentrations of airborne fungi were measured. Quantitative analysis of the air samples was performed by dividing the total number of fungal colony-forming units by the total volume of collected air (m3) (Yoon et al., 2019).

Figure 1.

Figure 1

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Detection of fungi in (A) air samples using the microbial air sampler and in (B) wall surface samples using the swab method in breeding houses.

Surface Sample Collection and Quantitative Analysis

Samples were collected from 3 randomly selected breeding houses in use on each farm. Three cement wall surfaces (close to the entrance, middle of the breeding house, and back of the breeding house) at a height of 0.5 m above ground per house were sampled using the swab method, as shown in Figure 1B (Ismaïl et al., 2013). Cotton swab samples were applied to SDA plates and incubated at 33°C for 4 to 10 d for fungal identification. The swabbed samples were placed in 10 mL of distilled water, vortexed, and serially diluted to 10−1, 10−2 for concentration measurements. Next, 1 mL of the diluted samples was inoculated on 3M Petrifilm Yeast and Mold Count Plates and incubated at 33°C for 1 to 2 d for quantitative analysis. The concentration (CFU/m2) was calculated by dividing the number of colony-forming units (CFUs) by the sampled area (0.01 m2).

Identification of Fungal Isolates

Fungal species were identified using macroscopic and microscopic analyses and molecular biology techniques to maximize the distinction between species. Fungi were identified based on colony color (conidia and reverse), texture, and the microscopic characteristics of the spores and hyphae. The observed morphological features were compared with those described in the literature (Wolf et al., 1975; Dugan, 2006).

Regarding molecular biological methods, fungi were identified by sequencing the internal transcribed spacer (ITS) region. Cultured fungal colonies were placed in tissue disruption tubes (IDEXX Laboratories Inc., Westbrook, ME) and tightly capped. The colonies were then ground for 30 s at 6,500 rpm using a homogenizer (Bertin Technologies, Rockville, MD). Nucleic acids from the ground fungal colonies were extracted using the Patho Gene-spin Plus Extraction kit (iNtRON Biotechnology, Gyeonggi-do, South Korea), according to the manufacturer's instructions. Primer sets (ITS1: 5′-TCCGTAGGTGAACCTGCGG-3′ and ITS4: 5′-TCCTCCGCTTATTGATATGC-3′) were used to amplify a DNA fragment (∼600 bp) in the ITS region (Zarrin et al., 2016). This region was amplified using Maxime PCR PreMix (iNtRON Biotechnology). An initial denaturation step for 5 min at 95°C was followed by 30 cycles each of denaturation at 94°C for 40 s, annealing at 58°C for 40 s, extension at 72°C for 40 s, and a final extension at 72°C for 5 min (Zarrin et al., 2016). The amplicons of the ITS region were sequenced, and the nucleotide sequences were compared with reference strains registered in GenBank (NCBI).

Biosecurity Risk Factor Analysis

Data were collected by observing farm characteristics, interviewing farm workers, and using the Korea Animal Health Integrated System program. The collected data were entered into a data file, and 8 categorical variables (geographic region, stocking density of farms, breeding house type, affiliation, duck age, the season of fungal infection, and air and surface fungal concentrations) were analyzed. Statistical analyses were performed to investigate the association between the 8 biosecurity risk factors and the incidence of fungal infections. The data were analyzed using the chi-square, Fisher's exact, and Fisher-Freeman-Halton tests with Benjamini-Hochberg correction (IBM SPSS software, version 21, Armonk, NY). Differences were considered statistically significant at P < 0.05.

RESULTS

Characteristics of Duck-Breeding Farms

The duck-breeding farms are distributed across various regions of North Chungcheong Province in South Korea. The surrounding environment of the duck-breeding farms had specific characteristics for each region: Cheongju-si, wide road and cropfield; Jincheon-gun, rice paddy and cropfield; Eumseong-gun, river and cropfield; Yeongdong-gun, mountain; Chungju-si, orchard; and Goesan-gun, cropfield. Table 1 summarizes the 19 duck-breeding farms from which the samples were collected from 2019 to 2020. Each farm was managed by 1 of the 9 affiliates. The stocking density was 0.47 to 2.48 ducks/m2, with an average of 1.97 ducks/m2. No farm exceeded the legal domestic breeding criteria of 3 ducks/m2 (AWCS, 2016). Most breeding houses were sandwich-panel houses; however, 3 farms used plastic-film houses. Rice husk litter was used in all 19 duck-breeding farms. Three plastic film-type farms were ventilated using only curtain winching systems, 15 sandwich panel-type farms were ventilated using curtain winching systems and ventilation fans, and 1 sandwich panel-type farm (farm H) used ventilation duct systems installed in each house.

Table 1.

Summary of duck-breeding farms sampled for fungi in this study.

Farms Geographic regions Stocking density of duck (/m2) Age1 (wk) Breeding house types Affiliates
A Cheongju-si 2.48 19–22 Plastic film a
B Cheongju-si 1.96 28–59 Sandwich panel b
C Cheongju-si 1.76 55–59 Sandwich panel b
D Jincheon-gun 1.64 19–24 Sandwich panel c
E Jincheon-gun 2.29 26–55 Plastic film d
F Jincheon-gun 2.08 70–80 Sandwich panel b
G Jincheon-gun 1.89 41–51 Sandwich panel e
H Jincheon-gun 1.54 72–80 Sandwich panel f
I Goesan-gun 2.50 61–85 Sandwich panel b
J Goesan-gun 1.93 20–23 Sandwich panel b
K Goesan-gun 2.34 19–24 Sandwich panel d
L Goesan-gun 2.13 20–24 Sandwich panel d
M Goesan-gun 2.06 20–22 Sandwich panel f
N Eumseong-gun 1.88 4 Sandwich panel f
O Eumseong-gun 2.43 22–25 Sandwich panel b
P Eumseong-gun 1.97 66–74 Sandwich panel g
Q Eumseong-gun 0.47 19–25 Sandwich panel h
R Chungju-si 1.97 14–18 Sandwich panel h
S Yeongdong-gun 2.06 63–75 Plastic film i
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1

Age of breeding ducks during sampling period.

Fungal Species Isolated From Breeding Duck Carcasses

Between April 2019 and December 2020, a total of 430 carcasses from duck-breeding farms were collected for autopsy from which 80 contained fungal lesions. Among these lesions, Aspergillus. fumigatus, A. flavus, and A. terreus were detected in 26, 35, and 19 cases, respectively (Table 2).

Table 2.

Comparison of Aspergillus species isolated from carcasses were taken from 19 duck breeding farms.

Farms Number of carcasses Number of cases with isolated Aspergillus spp.
A. fumigatus A. flavus A. terreus Total
A 21 3 1 1 5
B 32 - - - -
C 16 - 6 - 6
D 20 1 2 - 3
E 43 1 3 1 5
F 19 - 4 1 5
G 10 - - - -
H 17 2 - 1 3
I 62 4 10 7 21
J 11 - - 1 1
K 31 7 1 2 10
L 26 3 2 2 7
M 22 1 1 1 3
N 9 - - - -
O 18 1 1 - 2
P 9 - 1 - 1
Q 21 2 2 2 6
R 10 - - - -
S 33 1 1 - 2
Total 430 26 35 19 80
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Assessment of Fungal Concentrations on Indoor Duck-Breeding Farms

The average fungal concentration in the air was 203 CFU/m3, ranging from 25 to 1,200 CFU/m3. The average fungal concentration on the wall surfaces was 365 × 103 CFU/m2, ranging from 170 to 890 × 103 CFU/m2. The fungal concentration in the air and on the wall surfaces differed significantly between farms (Table 3, Welch's ANOVA, P < 0.05).

Table 3.

Average fungal concentrations in air and wall surface samples from 19 duck-breeding farms.

Farms Air samples (CFU/m3) Surface samples (×103 CFU/m2)
A 172 ± 19 606 ± 97
B 163 ± 92 247 ± 47
C 349 ± 18 378 ± 109
D 300 ± 100 206 ± 15
E 49 ± 31 381 ± 91
F 700 ± 30 431 ± 116
G 142 ± 25 277 ± 51
H 40 ± 10 301 ± 94
I 85 ± 5 789 ± 101
J 87 ± 6 305 ± 24
K 224 ± 39 608 ± 115
L 1122 ± 107 405 ± 168
M 148 ± 38 312 ± 54
N 85 ± 9 219 ± 48
O 66 ± 7 229 ± 61
P 167 ± 10 301 ± 19
Q 31 ± 3 371 ± 71
R 75 ± 21 216 ± 9
S 40 ± 19 338 ± 107
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Assessment of Fungal Species Diversity on Indoor Duck-Breeding Farms

Sixteen genera of fungi were recovered from the air and from wall surfaces. Figure 2 provides information on the fungi isolated from the duck-breeding farms. Aspergillus spp. was the most frequently isolated fungus (air, 43.2%; wall surfaces, 40%) and was detected in air samples from all 19 farms and wall surface samples from 12 farms. Additionally, Lichtheimia (20.5%) and Penicillium (9.1%) were frequently isolated from air samples, whereas Trichosporon (20%), Talaromyces (10%), and Lichtheimia (10%) were frequently isolated from wall surface samples.

Figure 2.

Figure 2

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Frequency of fungal genera isolation from the air and wall surface samples. Sixteen fungal genera were recovered from air and wall surface samples, with Aspergillus being the most frequently isolated.

Analysis of Biosecurity Risk Factors for Fungal Infection

The results of the biosecurity risk factor analysis reflected the correlation between the 8 categorical variables and fungal infection-positive farms (Table 4). When fungi were isolated from suspicious lesions, the corresponding farm was designated as positive. The fungal species were excluded from the analysis.

Table 4.

Biosecurity risk factor analysis for fungal infection in the duck-breeding farms.

Variables No. of farms No. of positive farms (%)
Overall 19 15
Geographic region3
 Cheongju 3 2 (66.7%)
 Jincheon 5 4 (80.0%)
 Goesan 5 5 (100%)
 Eumseong 4 3 (75.0%)
 Chungju 1 0 (0.0%)
 Yeongdon 1 1 (100%)
 P value 0.340
 Adjusted P value4 0.544
Stocking density of duck farm1
 ≦2/m2 10 6 (60.0%)
 >2/m2 9 9 (100%)
 P value 0.036*
 Adjusted P value4 0.045*
Breeding house type2
 Constructed with plastic film 3 3 (100%)
 Constructed with sandwich panel 16 12 (75.0%)
 P value 0.470
 Adjusted P value4 0.617
Affiliate3
 a 1 1 (100%)
 b 6 5 (83.3%)
 c 1 1 (100%)
 d 3 3 (100%)
 e 1 0 (0.0%)
 f 3 2 (66.7%)
 g 1 1 (100%)
 h 2 1 (50.0%)
 i 1 1 (100%)
 P value 0.540
 Adjusted P value4 0.617
Duck age3
 ≦4 wk 1 0 (0.0%)
 4–18 wk 1 0 (0.0%)
 18–25 wk 8 8 (100%)
 25–60 wk 4 2 (50.0%)
 >60 wk 5 5 (100%)
 P value 0.005*
 Adjusted P value4 0.020*
Season3
 Spring 1 1 (100%)
 Summer 1 1 (100%)
 Fall 2 2 (100%)
 Winter 15 11 (73.3%)
 P value 1.000
 Adjusted P value4 1.000
Concentration of fungi_air (CFU/m3)3
 ≦50 4 4 (100%)
 50–100 5 3 (60.0%)
 100–150 2 1 (50.0%)
 150–200 3 2 (66.7%)
 >200 5 5 (100%)
 P value 0.313
 Adjusted P value4 0.544
Concentration of fungi_surface (×103 CFU/m2)3
 200–250 5 2 (40.0%)
 250–300 1 0 (0.0%)
 >300 13 13 (100%)
 P value 0.004*
 Adjusted P value4 0.020*
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Italicface indicates statistical significance.

P values based on the

1

Chi-square test.

2

Fisher's exact test.

3

Fisher-Freeman-Halton test.

4

Benjamini-Hochberg correction.

⁎

P < 0.05.

Fungal infections were significantly affected by the farm's stocking density (P = 0.036), duck age (P = 0.005), and fungal concentration on wall surfaces (P = 0.004). This suggests that farms that raised ≤2 ducks/m2 had a lower prevalence than that of farms that raised >2 ducks/m2. Infections were predominant in ducks aged 18 to 25 wk, corresponding to the start of reproductive maturity, and in older ducks (>60 wk), which are susceptible to fungal infection. Fungi on wall surfaces were found to easily infect ducks when the concentration was >300 × 103 CFU/m2. However, the breeding house type, season, and fungal concentration in the air did not significantly affect fungal infections.

DISCUSSION

The extent and presence of fungi in the air and on wall surfaces were investigated from April 2019 to December 2020 in 19 duck farms selected for this study. In addition, the biosecurity risk factors of the farms were evaluated to assess their vulnerability to fungal infections. An examination of the characteristics of the poultry farms revealed that 17 of the 19 farms were distributed in Cheongju-si, Jincheon-gun, Eumseong-gun, and Goesan-gun and were regionally concentrated. Only 3 farms used plastic film-type houses, whereas the remaining 16 employed sandwich panel-type houses. According to a report by the Korea Duck Association (2019), 76.3% of duck-breeding houses are plastic film-type houses, and breeding ducks are raised in better facilities than meat-type ducks are raised in. Plastic film-type houses use only natural ventilation; thus, an influx of external substances will likely occur. Thus, sandwich panel-type houses are preferred for duck-breeding farms that need to raise ducks over long periods. The farms had different stocking densities, but none of the 19 farms exceeded 3 ducks/m2 (the appropriate number of ducks per unit area) (AWCS, 2016). Duck-breeding farms maintain low stocking densities because high densities reduce egg production performance (Xiong et al., 2020). Affiliates control the duck-breeding farms because they sell ducklings to the affiliated duck farms. The affiliates consult the farms about their production techniques and farm management and provide them with feed and bedding.

According to previous studies, the fungal concentration in air samples from other poultry farms was 2.5 × 101 to 1.1 × 108 CFU/m3 in Europe and Asia (Radon et al., 2002; Wang et al., 2007; Popescu et al., 2013; Wingfield et al., 2021). There are no data on surface samples from poultry farms, but the fungal concentrations on wall surfaces in nonpoultry farms are reported to be 3.0 × 104 to 3.4 × 106 CFU/m2 (Fan et al., 2021; Tseng et al., 2021). Moreover, because indoor fungal contamination exacerbates environmental diseases such as asthma and atopic dermatitis, mold levels should be kept below 500 CFU/m3, following the recommended standard for indoor air quality in public facilities for humans (Lee et al., 2020). In this study, the concentration of fungi from duck-breeding farms was 2.5 × 101 to 1.2 × 103 CFU/m3 and 1.70 × 105 to 8.9 × 105 CFU/m2 in air and wall surface samples, respectively, showing different fungal concentrations between farms and between sampling sites. Except for 2 farms (F and L), the fungal concentration in the air from the duck-breeding farms did not exceed the recommended standard (500 CFU/m3). Although there are no established criteria for wall surface fungal concentrations, the fungal concentrations on wall surfaces from the duck-breeding farms in this study were similar to those reported in previous studies.

The frequency of isolation and fungal genera in the air and on the wall surfaces of duck-breeding farms varied. A total of 16 fungal genera were isolated, of which 5 (Aspergillus, Lichtheimia, Penicillium, Rhizomucor, and Talaromyces) were found in the air and wall surface samples. The most common fungal genera in the air samples (accounting for 72.8%) were Aspergillus, Lichtheimia, and Penicillium in descending order, and the most common fungal genera in the wall surface samples (accounting for 80%) were Aspergillus, Trichosporon, Talaromyces, and Lichtheimia in descending order. Some of the fungi detected in the air and wall surface samples are opportunistic human and animal pathogens. Although present in the environment, Aspergillus and Penicillium can cause many health problems in humans and animals. There have been cases of infection with Lichtheimia species in trauma patients with soil-contaminated wounds and burn patients with fungi-contaminated dressings (Thielen et al., 2019). Trichosporon, which can be isolated from soil and water, infects immunocompromised patients, and Talaromyces contains several species that infect humans (Supparatpinyo et al., 1994; Horré et al., 2001; Limper et al., 2014; Montoya Mendoza and González, 2014; Guevara-Suarez et al., 2017). Aspergillus species (A. fumigatus, A. flavus, A. terreus) were the most frequently detected fungi in the air and wall surface samples and the most frequently isolated fungi in the clinical lesions of breeding ducks. Avian aspergillosis is the most common opportunistic mycotic infection wherever environmental conditions are optimal for fungal growth (Tell, 2005).

Biosecurity risk factors were analyzed to control the incidence of fungal infection in breeding ducks. The results showed that geographic region and season were not associated with aspergillosis (P > 0.05). This suggests that changes in external temperature and humidity, and differences in the surrounding environment of the farms did not affect fungal infections among breeding ducks reared in confined houses. The breeding house type did not have a statistically significant effect on fungal infections (P > 0.05). The 2 types of houses differed in terms of building materials, but all the duck-breeding farms except 1 farm used natural ventilation. Hence, there was no difference in fungal infection by house type due to the uniform ventilation method. Affiliates did not have a statistically significant effect on the occurrence of fungal infections (P > 0.05). This is because all affiliates used practices from the same duck breeding management guide book (Valley, 2017); hence, there were no differences in breeding methods or management. The incidence of fungal infections was associated with the duck age and stocking density (P < 0.05). Specifically, when ducks were of egg-laying age and the stocking density was high, the prevalence of fungal infections increased. This suggests that the breeding ducks were easily infected with fungi when under considerable stress (Jenkins, 1991). Breeding ducks older than 60 wk also had a high rate of fungal infections. This suggests that ducks become more susceptible to fungal infections as their immunity declines with age (Vanderheyden, 1993), or that the hygiene in the house notably deteriorates by the end of the laying cycle, because of the large amount of feces in the house.

The fungal concentration in the air samples did not have a statistically significant effect on fungal infection (P > 0.05). However, the fungal concentration in the wall surface samples was related to the presence of fungal infections (P < 0.05). Fungi attached to the walls could not be removed, because it is difficult to clean the walls of the house with breeding ducks present. The respiratory systems of breeding ducks living on the ground with litter rather than cages are highly likely to become infected, as the ducks separate the fungi attached to the walls when they flap their wings and move. Fungal infections were found in all 13 farms with fungal concentrations in wall surface samples greater than 300 × 103 CFU/m2; thereby deeming this as an important determining factor for fungal infection in duck-breeding farms.

The present study demonstrated the state of fungal infections in duck-breeding farms, and the biosecurity risk factors for fungal infections. Biosecurity risk factors that increase the prevalence of fungal infection in breeding ducks include: a stocking density of more than 2 ducks/m2; the 18 to 25 wk period when egg laying begins, a period of >60 wk when immunity is reduced and houses are contaminated with feces for a long time; and when the concentration of wall surface fungi is >300 × 103 CFU/m2. These results suggest that control of biosecurity risk factors affecting fungal infections is essential for breeding ducks raised in confined houses for long periods.

ACKNOWLEDGMENTS

We thank the Institute of Chungbuk Provincial Veterinary Service and Research for providing the environment for this study.

Funding: This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

Ethical Approval: The present study did not require ethical approval as we collected fungal samples only from normal functioning farms and did not alter their routine.

DISCLOSURES

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in the present study.

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