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. 2024 Sep 25;10(6):e70021. doi: 10.1002/vms3.70021

Study on fungal contaminants in aborted calves of cattle herds in Iran

Samaneh Eidi 1,✉, Hesam A Seifi 2,3, Soheil Sadr 1, Hamideh Zeinali 3
PMCID: PMC11423906  PMID: 39321209

Abstract

Background/Objective

Abortions in livestock herds are a major contributor to economic losses. The incidence of fungal aetiology has been reported thus far. The purpose of this study is to investigate the prevalence of abortions due to fungi in referred cases to the Center of Excellence in Ruminant Abortion and Neonatal Mortality, Veterinary Hospital of Ferdowsi University of Mashhad, Mashhad, Iran, from different provinces of Iran.

Methods

A total of 200 calves were referred between 2018 and 2022. Samples were taken from the lungs, liver, spleen and abomasum. The fungi present in the cultures were analysed microscopically and morphologically.

Results

There were varying contamination levels in the liver, spleen and lungs, with prevalence ranging from 15% to 17%. Abdomasum had a 1% prevalence rate. Different fungal species, including Cryptococcus neoformans (C. neoformans), Aspergillus spp., Rhodotorula spp., Trichosporon spp., Candida spp., Geotrichum spp., Penicillium spp. and Mucor spp., were identified, indicating a diverse range of pathogens affecting calves. The specificity of fungal contaminants in certain organs, such as C. neoformans, Rhodotorula spp. and Trichosporon spp., highlighted the organ's microenvironment as a potential factor influencing fungal growth.

Conclusion

As fungi are emerging as a significant cause of morbidity and mortality in animals, the growing role of fungi in livestock abortions should be investigated. As clinical signs are not pathognomonic, laboratory help is imperative to confirm fungal abortion diagnosis.

Keywords: cattle, fungal abortion, Iran, prevalence

The challenges presented by foetal abortion and neonatal mortality are imperative in the realm of livestock farming in comparison to other fields, and they seriously hamper the accomplishment of the vast potential of this industry.

Due to the significance and prevalence of foetal abortion among livestock herds, which is caused by both fungal contaminants and the role that fungi play in the occurrence of such abortions, the purpose of the present study is to investigate the prevalence of fungal contaminants in aborted calves of cattle herds in Iran among referred cases to the Center of Excellence in Ruminant Abortion and Neonatal Mortality, Veterinary Hospital of Ferdowsi University of Mashhad, Mashhad, Iran.

Among the 200 calves examined, 21% (42/200) were found to have fungal contamination. Overall, 15% (30/200) of the livers, 17% (34/200) of spleens and 16.5% (33/200) of the lungs exhibited fungal contaminants. However, only 1% (2/200) of the abomasums were contaminated with fungal agents.

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1. INTRODUCTION

Among the numerous challenges faced by cattle and sheep farmers, foetal abortion and neonatal mortality are of major concern (Ali et al., 2019; Clune et al., 2021; Gebretensay et al., 2019). The livestock industry suffers from foetal abortion and neonatal mortality, and scientists must effectively address these issues to harness the full potential of livestock production (Crowe et al., 2018). A foetus may be lost to abortion during the critical period of days 42 through 260 in dairy cows (Keshavarzi et al., 2020; Rafati et al., 2010; Tulu et al., 2018; Wijma et al., 2022). The occurrence of abortions in more than 5% of pregnant sheep or cattle is a warning sign that there is a deeper problem within the herd. As a result, rigorous efforts must be made to identify the aetiology responsible for these abortions (Alemayehu et al., 2021; Zhang et al., 2020). It is especially important to stress that exorbitant economic losses markedly dwarf the costs associated with diagnosing foetal abortion and proactively preventing it (Crilly et al., 2021; Deka et al., 2021). The causes and mechanisms of foetal abortion in herds must be understood and addressed constantly (Mee, 2023).

Infectious and non‐infectious factors play a significant role in foetal abortion (Gojam & Tulu, 2020). An infectious agent, such as a bacteria, virus, fungus or protozoa, constitutes a significant portion of the problem (Hajibemani & Sheikhalislami, 2020; Parthiban et al., 2015; Shaapan, 2016). Approximately 50%–62% of foetal abortions are caused by bacteria, 22%–25% by fungi and 15%–25% by viruses (Pal, 2015). Dairy cows and other livestock suffer foetal abortions as a consequence of these microorganisms (Barkallah et al., 2014; Baumgartner, 2021; Macías‐Rioseco et al., 2020). Additionally, non‐infectious factors, including nutrition, chemicals, drugs, toxins, poisonous plants and hormonal imbalances, significantly impact foetal abortion (Yadav et al., 2021). A comprehensive approach to diagnosis, prevention and mitigation of foetal abortion is therefore needed.

Mycotic abortions are a particular concern and are caused by moulds and yeasts (Fatima, 2021; Mostrom & Jacobsen, 2020). Inflammation of the placenta is an important effect of this condition (Borel et al., 2014; Jaiswal et al., 2019). Mycotic abortion has been associated with approximately 35 different fungi spp. (Van Kuijk et al., 2015). Many reports from previous studies emphasize the prominence of certain fungal species in the occurrence of foetal abortion. Approximately 60% of mycotic abortion cases originate from Aspergillus fumigatus, whereas 20% originate from Zygomycetes, such as Absidia, Mucor, Rhizomucor, Geotrichum and Rhizopus (Hajibemani & Sheikhalislami, 2020; Negi et al., 2024; Pal, 2015; Parthiban et al., 2015). Yeasts cause another 20% of cases. The isolation of the organism in fungal abortions should be carried out through the placenta, amniotic fluid, lung and foetal stomach (Elad & Segal, 2018; Reichel et al., 2018). However, the isolation of organisms from other foetal organs remains a relatively rare occurrence.

The challenges presented by foetal abortion and neonatal mortality are imperative in the realm of livestock farming in comparison to other fields, and they seriously hamper the accomplishment of the vast potential of this industry (Redden & Thorne, 2020). Due to the significance and prevalence of foetal abortion among livestock herds, which is caused by both fungal contaminants and the role that fungi play in the occurrence of such abortions, the purpose of the present study is to investigate the prevalence of fungal contaminants in aborted calves of cattle herds in Iran among referred cases to the Center of Excellence in Ruminant Abortion and Neonatal Mortality, Veterinary Hospital of Ferdowsi University of Mashhad, Mashhad, Iran.

2. METHODS AND MATERIALS

2.1. Study design and sampling

The current study was conducted on 200 referred calves between 2018 and 2022. Various farms across different provinces in Iran, mainly in Khorasan, Isfahan, Mazandaran and Tehran, were studied to determine fungal contaminants in aborted calves. There was a collection of samples from the liver, spleen, lungs and abomasum for each calf. Sterile techniques needed to be used in order to ensure that the samples were collected properly during the collection process. Sterile syringes extracted the abomasum contents. Other samples were obtained by dissecting the relevant organs utilizing sterile scalpels to acquire samples. A sterile physiological saline solution was used to preserve these samples to maintain their integrity and prevent future contamination.

2.2. Fungal identification

As soon as these samples were collected, they were referred to the Faculty of Veterinary Medicine's specialized mycology laboratory for analysis. The culture of the samples in a controlled environment was a crucial step in the laboratory. The culture medium was chosen as the Sabouraud dextrose agar medium (Merck Co.) supplemented with chloramphenicol (SC). An incubation period of 7–10 days was conducted in a controlled temperature range of 25–27°C. The incubation period was monitored on a regular basis to ensure that fungal growth was on track. To confirm that the samples contained fungi, fungal colonies had to be developed in order to evaluate their presence. Upon the completion of the growth process, an extensive identification process was initiated so that the fungal organisms could be verified. A morphological and microscopic analysis of the fungi present in the cultures was performed in order to identify them.

3. RESULTS

Among the 200 calves examined, 21% (42/200) were found to have fungal contamination. Overall, 15% (30/200) of the livers, 17% (34/200) of spleens and 16.5% (33/200) of the lungs exhibited fungal contaminants. However, only 1% (2/200) of the abomasums were contaminated with fungal agents.

Within the four cases where only the liver exhibited fungal contamination, Cryptococcus neoformans was identified in two cases: Rhodotorula spp., in one case and Trichosporon spp., in one case. In the six cases where only the lungs were affected, C. neoformans was observed in four cases, Rhodotorula spp., in one case, and Trichosporon spp., in one case. Three cases solely exhibited spleen contamination, whereas the remaining three organs were free from fungal contaminants. Candida spp. was identified in one case, Rhodotorula spp., in one case, and C. neoformans, in one case (Table 1).

TABLE 1.

Within the four cases, only the liver exhibited fungal contamination. In the six cases, only the lungs were contaminated.

Organ No. (%) Fungal species (No.)
Liver 4/200 (2%) Cryptococcus neoformans (2)/Rhodotorula spp. (1)/Trichosporon spp. (1)
Lung 6/200 (3%) C. neoformans (4)/Rhodotorula spp. (1)/Trichosporon spp. (1)/Candida spp. (1)
Spleen 3/200 (1.5%) Rhodotorula spp. (1)/C. neoformans (1)
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Note: Three cases solely exhibited spleen contamination, whereas the remaining three organs were free from fungal contamination. The exact pathogen that had been isolated was mentioned in the current table.

In the four cases where both the liver and spleen were simultaneously contaminated, and the lungs and abomasum were not affected, the contaminants were characterized as follows: one case of liver contamination with C. neoformans and spleen contamination with Rhodotorula spp.; one case with simultaneous contaminants in both organs by Rhodotorula spp.; one case with simultaneous contaminants in both organs by Trichosporon spp.; and one case with simultaneous contaminants by C. neoformans in both organs. Two cases demonstrated simultaneous contaminants in the liver and lungs, whereas the spleen and abomasum remained unaffected. Among these, one case was contaminated in both organs by Rhodotorula spp., and the other case exhibited simultaneous contaminants in both organs with Penicillium spp. In the three cases where only the lungs and spleen exhibited fungal contamination, whereas the abomasum and liver remained uncontaminated, one case involved lung contaminants with Rhodotorula spp. and spleen contaminants with Trichosporon spp.; another case demonstrated lung contaminants with C. neoformans and spleen contaminants with Trichosporon spp.; and the third case showed simultaneous contaminants in both organs with C. neoformans (Table 2).

TABLE 2.

In the four cases, both the liver and spleen were simultaneously contaminated.

Co‐contamination No. (%) Fungal species
Liver + spleen 4/200 (2%) Cryptococcus neoformans + Rhodotorula spp.
Rhodotorula spp. + Rhodotorula spp.
Trichosporon spp. + Trichosporon spp.
C. neoformans + C. neoformans
Liver + lung 2/200 (1%) Rhodotorula spp. + Rhodotorula spp.
Penicillium spp. + Penicillium spp.
Lungs + spleen 3/200 (1.5%) Rhodotorula spp. + Trichosporon spp.
C. neoformans + Trichosporon spp.
C. neoformans + C. neoformans
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Note: Two cases demonstrated simultaneous contamination in the liver and lungs. In the three cases, only the lungs and spleen exhibited fungal contamination. The exact pathogen that had been isolated was mentioned in the current table.

In 18 cases, simultaneous liver, lungs and spleen contaminants occurred, whereas the abomasum remained free from fungal contamination. Among these 18 cases, 4 cases exhibited triple organ contaminants with C. neoformans and two cases with Geotrichum spp. A total of two cases with both liver and spleen contaminated with Trichosporon spp. and lungs contaminated with Rhodotorula spp. Moreover, two cases were identified with both liver and lungs contaminated with Trichosporon spp., and spleen was co‐contaminated with Trichosporon spp. and Rhodotorula spp. Furthermore, one case of each of the following forms happened: triple organ contaminants with Candida krusei, triple organ contaminants with Candida albicans; triple organ contaminants with Trichosporon spp.; triple organ co‐contaminants with Trichosporon spp. and Rhodotorula spp.; triple organ contaminants with Rhodotorula spp.; one case with liver contaminated with Trichosporon spp., spleen contaminated with Rhodotorula spp. and lungs contaminated with Trichosporon spp. and Rhodotorula spp.; one case showed liver and spleen contaminated with C. neoformans, and lungs contaminated with C. neoformans and Rhodotorula spp.; in the final case, the liver and spleen were contaminated with Geotrichum spp., and the lungs were contaminated with C. neoformans (Table 3).

TABLE 3.

In 18 instances, simultaneous liver, lungs and spleen contamination occurred, whereas the abomasum remained free from fungal contamination.

Co‐contamination No. (%) Fungal species (liver + lungs + spleen)
Liver + lungs + spleen 4/200 (2%) Cryptococcus neoformans + C. neoformans + C. neoformans
2/200 (1%) Geotrichum spp. + Geotrichum spp. + Geotrichum spp.
2/200 (1%) Rhodotorula spp. + Trichosporon spp. + Trichosporon spp.
2/200 (1%) Trichosporon spp. + Trichosporon spp. + (Trichosporon spp. and Rhodotorula spp.)
1/200 (0.5%) Candida krusei + C. krusei + C. krusei
1/200 (0.5%) Candida albicans + C. albicans + C. albicans
1/200 (0.5%) Trichosporon spp. + Trichosporon spp. + Trichosporon spp.
1/200 (0.5%) (Trichosporon spp. and Rhodotorula spp) + (Trichosporon spp. and Rhodotorula spp) + (Trichosporon spp. and Rhodotorula spp.)
1/200 (0.5%) Rhodotorula spp. + Rhodotorula spp. + Rhodotorula spp.
1/200 (0.5%) Trichosporon spp. + Rhodotorula spp. + (Trichosporon spp. and Rhodotorula spp.)
1/200 (0.5%) C. neoformans + C. neoformans + (C. neoformans and Rhodotorula spp.)
1/200 (0.5%) Geotrichum spp. + C. neoformans + Geotrichum spp.
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Note: The exact pathogen that had been isolated was mentioned in the current table.

In two cases, all four organs exhibited fungal contamination, with one case contaminated with Trichosporon spp. and another contaminated with Mucor spp.

Simultaneous contaminants with two fungi occurred three times in the spleen, with two cases involving both Rhodotorula spp. and Trichosporon spp. and one case with simultaneous contaminants of Aspergillus spp. and Rhodotorula spp. Simultaneous contaminants with two fungi also occurred three times in the lungs, with one case involving both Trichosporon spp. and Rhodotorula spp., one case with Aspergillus spp. and Rhodotorula spp. and one case with both C. neoformans and Rhodotorula spp. Simultaneous contaminants with two fungi occurred once in the liver, involving Aspergillus spp. and Rhodotorula spp. (Table 4).

TABLE 4.

Simultaneous contamination with two fungi occurred three times in the spleen, three times in the lungs and once in the liver.

Organ No. of cases Fungi involved (No.)
Spleen 3 Rhodotorula spp. and Trichosporon spp. (2)
Aspergillus spp. and Rhodotorula spp. (1)
Lungs 3 Trichosporon spp. and Rhodotorula spp. (1)
Aspergillus spp. and Rhodotorula spp. (1)
Cryptococcus neoformans and Rhodotorula spp. (1)
Liver 1 Aspergillus spp. and Rhodotorula spp. (1)
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Note: The numbers in parentheses indicate the frequency of occurrence for each combination of fungi in the specified organ.

4. DISCUSSION

Various types of microorganisms cause infectious abortions, which are among the most serious public health problems and are of great economic significance (Clothier & Anderson, 2016; Vidal et al., 2017). Worldwide, dairy cattle suffer from the problem of mycotic abortion, which is one of the most common reproductive problems (Yoo, 2010). Australia, India, New Zealand and the USA are some countries where the disease has been reported (Fatima, 2021). As a result of the presence of various types of fungi in the environment, the disease is transmitted by a wide range of fungi. Most abortion cases are caused by A. fumigatus, followed by Zygomycetes, the most prevalent fungi (Atwa & Rady, 2007; Seyedmousavi et al., 2015). Generally, a fungal abortion has been recorded to occur between the sixth and eighth months of gestation in cattle (Wolf‐Jäckel et al., 2020). A retained placenta is the most common cause of suffering in aborted animals (Givens & Marley, 2008). In addition, animals kept in humid, hot, unclean, old and unhygienic conditions are predisposed to mycotic abortions due to mouldy feed or hay. Disease transmission and epidemiology are still inadequately studied. The mainstay of fungal contaminants diagnosis is direct microscopy and culture isolation from clinical specimens. At present, there is no effective treatment available for mycotic abortions as of yet (Ali & Khan, 2006). Keeping pregnant animals in hygienic sheds and avoiding mouldy feed reduces disease risk.

To the best of our knowledge, few studies have investigated fungal foetal contamination or evaluated fungal foetal abortion in Iran and worldwide. According to the first report of bovine abortion by A. fumigatus in Japan (Matsui et al., 1977), 6 bovine abortion cases, among 19 of those brought in for the pathological examination from 1961 to 1974, were diagnosed histologically as mycotic infectious abortion. Fungi were isolated from the cutaneous lesion, foetal membrane and abomasal content.

Additionally, a recent study was aimed to characterize the pathological and etiological findings in foetuses aborted due to secondary bacterial and fungal infections submitted for post‐mortem examination between 2004 and 2019 in the State of Rio Grande do Sul, Brazil and five cases of fungal aetiology were assessed (Henker et al., 2022). Aspergillus spp. was the main fungal agent identified, and cases of mycotic abortion were characterized by placentitis, dermatitis and pneumonia.

Recently, it has been recognized that mycotic infections play a significant role in the causes of bovine abortion. According to the report, histology, cytology, culture and molecular assays demonstrated the presence of Aspergillus nidulans, Aspergillus luchuensis and Lichtheimia spp. in the abortion of a Chianina cow (Pesca et al., 2020). It is rare to demonstrate a mixed infection with more than one fungus in abortion.

Moreover, in 2022, Aspergillus terreus was identified immunohistochemically, morphologically and molecularly in bovine placentas and aborted foetuses (Sato et al., 2022). Histopathological examination of the placenta and foetus revealed severe necrotic placentitis associated with numerous irregular degenerative fungi and inflammatory cells. Additionally, the presence of regular filamentous fungi was also found in the digestive and respiratory systems of the foetus without causing inflammation.

Moreover, a total of 120 samples of aborted foeti, vaginal discharge and Placenta were collected from 70 aborted ewes and 50 aborted she‐goats from Menoufiea Governorate for mycological examination (Atwa & Rady, 2007). Mycological examination of aborted foeti, vaginal discharge and Placenta of aborted sheep revealed the isolation of A. fumigatus, Aspergillus niger, Aspergillus flavus, C. albicans, C. krusei and Mucor spp. Abisidia spp. and Rhodotrula spp. with incidence of 12.9%, 5.7%, 2.9%, 8.6%, 2.9%, 4.3%, 2.9% and 1.4%, respectively. However, the fungi isolated from aborted she‐goats were A. fumigatus, A. niger, A. flavus, Candida tropicalis, C. albicans, Mucor spp., Rhizopus spp., Penicillium pp. and Fusarium spp. with the incidence of 14%, 6%, 2%, 10%, 8%, 6%, 4%, 2% and 2%, respectively.

It is critical to note that conventional culture may not detect fungal organisms that may be responsible for bovine abortion. It has been proposed that the gold standard workflow to diagnose a mycotic abortion involves the microscopic observation of fungal hyphae or elements, along with gross lesions that match the fungal hyphae (Vidal et al., 2018). It is also suggested that fungi or fungal DNA can be detected in the abortion material using culture or molecular methods. Abortion diagnostic workflow should always include other abortifacients and histopathological analyses. This will enable us to diagnose based on the three criteria. The organism is present in large numbers in the foetal abomasum and/or other tissues and in pure or almost pure culture. Second, foetal tissues and/or membranes are associated with inflammation. Finally, tests exclude other common abortion agents.

The current study imposes several constraints that are recommended for future consideration. The age of the dam, especially in cases where her calf has been aborted, is crucial and warrants thorough examination. Additionally, it is imperative to investigate the dam's stage of pregnancy. Factors, such as season, weather conditions and geographic information system data, play pivotal roles in understanding the overall context. The age of the dam also emerges as a significant factor that necessitates attention.

5. CONCLUSION

In conclusion, the high prevalence of fungal contaminations in the examined calves, along with the diversity of fungal species and organ‐specific patterns, underscores the need for a comprehensive investigation into the underlying factors contributing to these infections. Understanding these factors is essential for developing effective preventive measures and treatment strategies to safeguard animal health. Additionally, addressing fungal contaminants in livestock is crucial for protecting human health, especially when these animals are part of the food supply chain. Enhanced biosecurity protocols, regular monitoring and targeted interventions will be vital in mitigating the impact of fungal pathogens in livestock populations.

AUTHOR CONTRIBUTIONS

Samaneh Eidi: Conceptualization; investigation; supervision; methodology; performing experiments; project administration; validation; visualization; data curation; formal analysis; writing‐review and editing. Hesam A. Seifi: Methodology; data curation; investigation; formal analysis. Soheil Sadr: Methodology; formal analysis; data curation; writing – original draft preparation; writing – review and editing. Hamideh Zeinali: Methodology; performing experiments; formal analysis. All authors checked and approved the final version of the manuscript for publication in the present journal.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

FUNDING INFORMATION

Ferdowsi University of Mashhad, Grant No: 2/38428).

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.70021.

ETHICAL STATEMENT

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. The study procedure has been approved by the ethical committee of the Animal Welfare Committee at the Ferdowsi University of Mashhad. IR.UM.REC.1402.191.

ACKNOWLEDGEMENTS

We thank the research deputy of the Ferdowsi University of Mashhad and Veterinary Faculty for supporting us. Furthermore, we want to thank Fetal Abortion and Neonatal Mortality Research Center at the School of Veterinary Medicine, Ferdowsi University of Mashhad for giving us samples.

Eidi, S. , Seifi, H. A. , Sadr, S. , & Zeinali, H. (2024). Study on fungal contaminants in aborted calves of cattle herds in Iran. Veterinary Medicine and Science, 10, e70021. 10.1002/vms3.70021

DATA AVAILABILITY STATEMENT

The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.

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