Hadjelia Truncata Infection Among Quails (Coturnix Coturnix) In Semnan City, Iran

Case History
Hadjelia truncata is a nematode (roundworm) in the order Spirurida, the family Habronematidae. Birds’ digestive tracts, mainly the ventriculus and gizzard, are infected (Anderson, 2000; Senties-Cue et al., 2011; Khordadmehr et al., 2018). H. truncata has an indirect life cycle that has not been completely identified. Eggs are shed in bird feces. When intermediate hosts such as some beetles (Phylan abbreviatus, Asida jurinei, Asida sericea, (Anderson, 2000) and Alphitobius diaperinus (Alborzi & Rahbar, 2012) ingest the eggs, the infective worms or the third-stage larvae (L3) are formed in the hemocoel of the beetles. If birds ingest infected beetles, the life cycle will be completed, and adult worms will be formed in the gastrointestinal tract (Alborzi & Rahbar, 2012).
Quails (Coturnix coturnix, Phasianidae, Galliformes) are grown in different parts of Iran. This report aimed to describe the first quail infection of H. truncata. 
Clinical Presentation
Twenty-five naturally dead male quails’ gastrointestinal tracts were referred from a quail farm in Semnan City to the Parasitology Laboratory, Faculty of Veterinary Medicine, Semnan University, Iran. 

Diagnostic Testing
All referred digestive tracts were inspected, and 18 H. truncata worms were removed and identified from 6 gizzards. Therefore, the infection rate of H. truncata among referred quails was 24%. The average number of worms in each infected quail was 3. All the nematodes were located between the infected gizzards’ submucosal and muscular layers. The direct swabs of the fecal samples were also examined. H. truncata eggs were also observed in the infected quails (Figure 1).

The size of the removed worms and their eggs are presented in Table 1.

Assessments
H. truncata has been reported in pigeons’ (Columba livia domestica) gizzards in Iran (Razmi et al., 2007; Radfar et al., 2011; Alborzi & Rahbar, 2012; Nabavi et al., 2013; Khordadmehr et al., 2018), Iraq (Al-Attar & Abdul-Aziz, 1985), Egypt (Tadros & Iskander, 1975), and Cyprus (Appleby et al., 1995), in gizzard and ventriculus of pigeons in California, US (Senties-Cue et al., 2011; Ochoa & Adaska, 2021). It has also been reported in hoopoe (Upupa epops) in France (Anderson, 2000). 
The sizes of male and female H. truncata have been recorded in several studies as follows: 7-9 and 13-17 mm (Razmi et al., 2007), 7-11 and 15-20 mm (Khordadmehr et al., 2016), and 6.5-9 and 12-16.5 mm (Senties-Cue et al., 2011), respectively. In this study, the size of male worms was 6-9 mm, and that of female worms was 15-18 mm. The mean lengths of long and short spicules were reported in several studies as follows: 1.26 and 0.34 mm (Razmi et al., 2007), 1.27 and 0.35 mm, respectively (Senties-Cue et al., 2011). In our study, it was recorded as 1.44 and 0.35 mm. The egg size was 20-30×43-45 µm in the Khordadmehr et al. (2016) study and was 22-28×44-47 µm in this study. 
The signs of infection are weight loss, weakness, loss of appetite, poor feathering, and diarrhea. However, the disease seems severe and fatal among pigeons (Appleby et al., 1995; Kelly et al., 2013). The histopathologic alterations of previously reported cases of infected pigeons were severe inflammatory cell infiltration with necrosis of mucosal and submucosal layers of the gizzard (Khordadmehr et al., 2018). A polymerase chain reaction technique for detecting H. truncata DNA (deoxyribonucleic acid) has also been described (Kelly et al., 2013). 
This research is the first report of H. truncata infection in quails worldwide. No apparent changes in infected gizzards were grossly observed. It might be because of the low number of worms in each gizzard. The histopathologic sections of gizzards could not be prepared because of postmortem alterations of referred digestive tracts.

Ethical Considerations

Compliance with ethical guidelines
There were no ethical considerations to be considered in this research.

Funding
This research received no specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Authors' contributions
Sample preparation and data collection: Abbas Oliya Ardekani and Hassan Moazzezi; Species diagnosis and writing: Maryam Rassouli.

Conflict of interest
The authors declared no conflict of interest.

Acknowledgments
The authors are grateful to Rezaeian and Khodadi for their help. 

References

Al-Attar, M. A., & Abdul-Aziz, T. A. (1985). Hadjelia truncata in pigeons. The Veterinary Record, 117(20), 535. [DOI:10.1136/vr.117.20.535-b] [PMID]

Alborzi, A., & Rahbar, A. (2012). Introducing alphitobius diaperinus, (insecta: Tenebrionidae) as a new intermediate host of Hadjelia truncata (nematoda). Iranian Journal of Parasitology, 7(2), 92–98. [PMID] [PMCID]

Anderson, R. C. (2000). Nematode parasites of vertebrates; their development and transmission. Wallingford: CABI Publishing. [DOI:10.1079/9780851994215.0000]

Appleby, E. C., Gibbons, L. M., & Georgiou, K. (1995). Distortion of the gizzard in cyprus pigeons (columba livia) associated with Hadjelia truncata infestation. The Veterinary Record, 136(22), 561–564. [DOI:10.1136/vr.136.22.561] [PMID]

Kelly, J. M., Senties-Cue, C. G., Charlton, B. R., Gerhold, R. W., Santoro, T. J. & Bland, M. C. Treatment, diagnostic trials, and construction of species-specific PCR primers of Hadjelia truncata in pigeons (Columba livia). Journal of Applied Poultry Research, 22(3), 559-564. [DOI:10.3382/japr.2012-00645]

Khordadmehr, M., Ranjbar, V. R., Shahbazi, P., & Zeinoddini, M. (2018). Co-infection of Sarcocystis sp. and Hadjelia truncata in fantail pigeons (Columba livia domestica). Bulgarian Journal of Veterinary Medicine, 21(1), 115-121. [DOI:10.15547/bjvm.995]

Nabavi, R., Khedri, J. & Jahantigh, M. (2013). High clinical disturbance and mortality in pigeon flocks caused by Hadjelia truncata infection in Sistan, Iran. Turkish Journal of Veterinary and Animal Sciences, 37(3), 355-357. [DOI:10.3906/vet-1112-20]

Ochoa, J. N. & Adaska, J. M. (2021). Multifocal ulcerative ventriculitis a pigeon by Hadjelia truncate. Brazilian Journal of Veterinary Pathology, 14(3), 210-212. [DOI:10.24070/bjvp.1983-0246.v14i3p210-212]

Radfar, M. H., Fathi, S., Asl, E. A., Dehaghi, M. M., & Seghinsara, H. R. (2011). A survey of parasites of domestic pigeons (Columba liva domestica) in South Khorasan, Iran. Veterinary Research, 4(1), 18-23. [Link]

Razmi, G. R., Kalidari, G. A., & Maleki, M. (2007). [First report of the Hadjelia truncata infestation in pigeons of Iran (Persian)]. Iranian Journal of Veterinary Research, 8(2), 175-177. [DOI:10.22099/IJVR.2007.2693]

Sentíes-Cué, C. G., Charlton, B. R., Anthenill, L., Naem, S., McDougald, L., & Bland, M. (2011). Parasitic ventriculitis caused by Hadjelia truncata in California rock pigeons (Columba livia). Journal of Veterinary Diagnostic Investigation, 23(6), 1243–1246. [DOI:10.1177/1040638711425575] [PMID]

Tadros, G. & Iskander, A. R. (1975). Hadjelia truncata, a new parasite of pigeons in Egypt and its pathogenicity. Journal of the Egyptian Veterinary Medicine Association, 35(3), 283-301. [Link]