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. 2022 Nov 22;11(12):1392. doi: 10.3390/pathogens11121392

The Prevalence and Control of Lungworms of Pastoral Ruminants in Iran

Salman Zafari 1,†, Sina Mohtasebi 2,†, Alireza Sazmand 3,*, Aliasghar Bahari 4, Neil D Sargison 5, Guilherme G Verocai 6,*
Editor: Anastasia Diakou
PMCID: PMC9787811  PMID: 36558726

Abstract

Lungworms of the genera Dictyocaulus, Muellerius, Protostrongylus, and Cystocaulus are common helminths of domestic and wild ruminants with substantial veterinary and economic importance. Several studies have assessed the presence and prevalence of lungworm infections in ruminants in Iran. This report compiles the available scientific information about the occurrence of lungworms in domestic and wild ruminants in Iran between 1931 and June 2022 to give an insight into their epidemiology, and where possible to describe drug treatment efficacy. For this purpose, national and international scientific databases were searched. Overall, 54 publications comprising 33 articles in peer-reviewed journals, 8 conference papers, and 13 dissertations were evaluated regarding prevalence data; and an additional 4 peer-reviewed articles were evaluated regarding drug efficacy. Seven species of lungworms, namely Dictyocaulus filaria, Dictyocaulus viviparus, Dictyocaulus eckerti, Protostrongylus rufescens, Protostrongylus raillietti, Muellerius capillaris, and Cystocaulus ocreatus have been recorded from different ruminant hosts in Iran. Thirty-three studies conducted on small ruminant (sheep and goat) lungworms reported prevalences of lungworm infection of 11.6%, 45.81% and 66.29% using abattoir meat inspection, Baermann technique and fecal flotation, respectively. Eight studies conducted on large ruminants (cattle and water buffalo) reported prevalences of infection of 14.83%, 13.98% and 5% using abattoir meat inspection, the Baermann technique and fecal flotation, respectively. The prevalence of infection in wild ruminants was variable across examined species; 38% in urial, 37% in wild goats, 5% in goitered gazelles and 67% in red deer, in addition to a single case report in roe deer. There are few contemporary studies assessing the efficacy of currently available broad-spectrum anthelmintic compounds against lungworms in Iran. The high prevalence of multiple lungworm species in Iran, combined with a lack of information about drug efficacy, supports the need to improve the understanding of these important nematode parasites and inform the development of sustainable control strategies. The aim of this review and meta-analysis is to provide a baseline for future conventional parasitology and next generation molecular epidemiological studies of lungworm infection in pastoral ruminants in Iran.

Keywords: lungworms, nematoda, verminous pneumonia, protostrongylidae, metastrongyloidea, ruminants, anthelminthics

1. Introduction

Approximately, half of all creatures on earth are parasites [1]. These organisms play important roles in the regulation of host populations, food webs, and interspecific interactions [2]. In addition, they impact the health and welfare of their hosts. Domestic ruminants are widely kept for high quality protein production, but milk and meat production can be reduced as a result of parasitic infections [3,4]. Among these parasites, lungworms can cause significant economic losses, underpinning the importance of correct diagnosis, treatment, and control [5]. Lungworm species within the superfamilies Trichostrongyloidea and Metastrongyloidea are of veterinary importance in domestic ruminants in Iran. Among the Trichostrongyloidea, Dictyocaulus viviparus is of major importance in bovines and Dictyocaulus filaria in small ruminants. Dictyocaulus species lungworms have direct life cycles in which the first-stage larvae (L1) are shed in faces where they develop into infective third-stage larvae (L3) in the environment. L3 are ingested by ruminants while grazing and migrate to the respiratory system, where they mature into dioecious adults within the lumen of bronchi and bronchioles. Females shed eggs, which embryonated in the lungs, and hatch within the gastrointestinal tract, before being shed in feces. Diagnosis can be supported by larvoscopy to identify L1 in feces most often using the Baermann technique [6].

Among the Metastrongyloidea, Muellerius capillaris, Protostrongylus rufescens, and Cystocaulus ocreatus are important in sheep and goats. These lungworms have indirect life cycles, requiring gastropod intermediate hosts for the development of L1 to the infective L3 stage [6,7]. Adult females lay eggs in the terminal bronchioles and alveoli. L1 hatch within the airways, are coughed and swallowed together with respiratory secretions and passed, before invading susceptible terrestrial snail hosts. Development to the infective L3 takes a few weeks to several months, depending on lungworm species, weather conditions and the suitability of the gastropod host species. Small ruminants become infected by inadvertently ingesting snails harboring infective L3 [8]. Additionally, some protostrongylid L3 may actively escape the snails, hence small ruminants can become infected while ingesting free L3 while grazing [9]. Ingested L3 migrate to the respiratory system, maturing to dioecious adults following a prepatent period of 1–3 months. In the absence of effective treatment, patent infections may persist for several years.

Currently, the genus Dictyocaulus contains eight valid species: D. viviparus (Bloch, 1782) in large ruminants (cattle and buffaloes), D. filaria (Rudolphi, 1809) in small ruminants (sheep and goats), Dictyocaulus arnfieldi (Cobbold, 1884) in equids (horses and donkeys, Dictycaulus eckerti (Skrjabin 1941) in cervids, Dictycaulus cameli (Boev, 1951) in camels, Dictycaulus africanus (Gibbons & Khalil, 1988) in African artiodactylids (camels and boars), Dictycaulus capreolus (Gibbons & Höglund, 2002) in roe deers and Dictycaulus cervi (Pyziel et al. 2017) in red deers. Dictyocaulus viviparus infecting cattle and water buffaloes and D. filaria infecting small ruminants are among the most common lungworms around the world, causing economic loss and compromising animal welfare [6,10]. Host responses to infection cause bronchitis and eosinophilic pneumonia, which along with blockage of respiratory bronchioles, can result in dyspnea, coughing, pyrexia, loss of appetite, poor growth rates, and death [4,11,12]. Harsh respiratory sounds are heard on auscultation of the chest. Secondary bacterial infections may add to the pathology arising from infection [5]. Although D. filaria and D. viviparus usually infect ruminants, they have also been reported in camels [13], putatively due to cross-infection from ruminants [14]. Dictyocaulus eckerti (Skrjabin, 1931) is often found in small numbers in adult cervids, namely reindeer, fallow deer, red deer, roe deer, and moose, with no apparent clinical disease [15]. However, farmed deer, especially young animals in their first year of life, are highly susceptible to lungworm infection resulting in loss of productivity and fatality [15]. Cross-species transmission of Dictyocaulus spp. has been demonstrated between wild cervids and bovids [16].

The Protostrongylus genus of metastrongyloid lungworms contains at least thirteen species which P. rufescens (Leuckart, 1865) is the most common species infecting small domestic ruminants worldwide [17]. Although protostrongylosis is widespread, it is not considered highly pathogenic, albeit infected animals may show signs of mucopurulent nasal discharge, dyspnoea, anorexia and weight loss [18]. Nonetheless, pathological changes characterized by chronic eosinophilic granulomatous pneumonia (visible by histopathology) are frequently detected on postmortem examination [19] and are an important cause of offal rejection at meat inspection in many countries.

Muellerius capillaris (Müller, 1889) is present worldwide in small ruminants [20]. The presence of infection is high in goats compared to sheep [21]. Heavy infections can result in interstitial pneumonia, broncho-pneumonia, or fibrinous pleuritis [6], resulting in reduced weight gain, poor reproductive performance, depressed milk production, and increased mortality [22].

Cystocaulus ocreatus (Railliet & Henry, 1907) is present in small ruminants in parts of Asia, Europe, and Africa [17]. Economic losses have been reported due to both adult and developing stages in the alveoli, alveolar ducts, and bronchi [23].

By comparison with gastrointestinal nematodes, lungworms have received little attention from the scientific community of Iran. This review aims to evaluate and unfold the status of lungworm infection in domestic and wild ruminants in Iran.

2. Materials and Methods

International online databases prior to July 2022 (Google Scholar, Pubmed and CAB Direct) and the Iranian national online databases (Irandoc and Civilica) were searched singularly and in combination, using English, Persian and French language keywords: lungworm(s), mammals, domestic, wild, wildlife, ruminant(s), treatment; plus common and scientific names of the hosts and lungworms.

The validity, accuracy, clarity, transparency in the originality, objectivity, sampling method and diagnostic method reported in each document was evaluated by two nematode parasitologists. Validated reports were then sorted for the study area, type of host animal, species diversity and species prevalence, year of study, the number of animals studied and methods used in generating the report.

3. Results

Since the first description of lungworm infection in Iran in 1931, a total of 60 reports were found, of which six sources were excluded in the evaluation of validity and accuracy. The 54 reports included in this review comprise 33 peer-reviewed articles [15 in English, 13 in Persian with English abstract, 5 in Persian], 8 conference papers [4 in English, 4 in Persian], 11 D.V.M. theses by veterinary students [8 in Persian, 2 in Persian with English abstract, 1 in French], and 2 Master’s theses [in Persian with English abstract]. In addition, four peer-reviewed articles [4 in English] were used to assess the efficacy of anthelmintic drugs against lungworms in large and small ruminants. No record of infection of ruminants was found in 13 provinces, in 12 of which, veterinary faculties are not present, i.e., the University of Zabol in Sistan-va-Baloochestan province has a veterinary faculty (Figure 1A).

Figure 1.

Figure 1

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Map of Iran showing (A) the distribution of reports of lungworms of sheep, goats, cattle and buffaloes, (B) the distribution of reported lungworms of sheep, goats, cattle and buffaloes.

Overall, seven species of lungworms belonging to four genera have been reported in Iran. These are D. filaria, D. viviparus, D. eckerti, P. rufescens, P. raillietti, M. capillaris, and C. ocreatus, reported in domestic sheep, goats, cattle, buffaloes and wild ruminants, namely urial (Ovis orientalis), wild goats (Capra aegagrus), goitered gazelle (Gazella subgutturosa), roe deer (Capreolus capreolus), and red deer (Cervus elaphus) (Figure 1B).

3.1. Sheep and Goat Lungworms

Thirty-three publications reported lungworm infection in sheep and goats in Iran, including 21 peer-reviewed articles, 12 dissertations (11 D.V.M., 1 Master’s), and 6 conference papers. These reports depicted infection in different regions of Iran, including 17 of the 31 provinces. The first record of lungworms is the 1931 report by a French veterinarian who wrote that verminous bronchopneumonia is prevalent in sheep in Iran (Carpentier, 1931). Since then, in total, 28,964 animals were examined for the presence of infection. The majority of animals (80.6%, 23,349) had their respiratory system examined at necropsy, and 19.4% of cases (5615) were diagnosed by microscopy-based fecal diagnostic tests on apparently healthy animals. Prevalence rates of lungworm infection were 11.6%, 45.8% and 66.3% using abattoir meat inspection, Baermann technique, and fecal flotation, respectively (Table 1). One drawback of Iranian reports on small ruminant lungworms is that the plucks of sheep and goats were not inspected separately in abattoirs, because sheep and goats are slaughtered concurrently on the same line, hence lungworm reports for sheep and goats must be considered together.

Table 1.

Lungworms of sheep and goats in Iran according to geographical area, nematode species and diagnostic method.

Geographical Region Study Area Nematode Species Test # Tested % Prevalence Host Year of Study References
Northern Provinces Single infections
Tehran Dictyocaulus filaria Abattoir meat inspection 192 9.9 Sheep/Goat 1960–1961 [26]
Tehran Dictyocaulus filaria Abattoir meat inspection 33 63.6 Sheep/Goat Not stated [27]
Golestan Dictyocaulus filaria Abattoir meat inspection 60 5.0 Sheep Not stated [28]
Golestan Dictyocaulus filaria Abattoir meat inspection 60 3.3 Goat Not stated [28]
Semnan Dictyocaulus filaria Abattoir meat inspection 380 24.2 Sheep/Goat 2015 [29]
Gilan Dictyocaulus filaria Baermann 140 7.1 Sheep 2017–2018 [30]
Tehran Protostrongylus rufescens Abattoir meat inspection 192 24.5 Sheep/Goat 1960–1961 [26]
Tehran Protostrongylus rufescens Abattoir meat inspection 33 9.1 Sheep/Goat Not stated [27]
Golestan Protostrongylus rufescens Abattoir meat inspection 60 1.7 Goat Not stated [28]
Semnan Protostrongylus rufescens Abattoir meat inspection 380 10.6 Sheep/Goat 2015 [29]
Gilan Protostrongylus rufescens Baermann 140 2.1 Sheep 2017–2018 [30]
Tehran Cystocaulus sp. Abattoir meat inspection 192 19.8 Sheep/Goat 1960–1961 [26]
Tehran Cystocaulus ocreatus Abattoir meat inspection 33 3.0 Sheep/Goat Not stated [27]
Gilan Cystocaulus ocreatus Baermann 140 1.4 Sheep 2017–2018 [30]
Semnan Muellerius capillaris Abattoir meat inspection 380 1.5 Sheep/Goat 2015 [29]
Gilan Muellerius capillaris Baermann 140 0.7 Sheep 2017–2018 [30]
Mixed infections
Tehran Dictyocaulus sp. + Protostrongylus sp. Abattoir meat inspection 192 2.6 Sheep/Goat 1960–1961 [26]
Tehran D. filaria + P. rufescens Abattoir meat inspection 177 31.6 Sheep 1985–1986 [31]
Tehran D. filaria + P. rufescens Abattoir meat inspection 33 9.1 Sheep/Goat Not stated [27]
Tehran D. filaria + C. ocreatus Abattoir meat inspection 33 6.1 Sheep/Goat Not stated [27]
Tehran C. ocreatus + P. rufescens Abattoir meat inspection 33 9.1 Sheep/Goat Not stated [27]
Tehran Lungworms larvae Abattoir meat inspection 1627 3.7 Sheep 1997 [32]
Golestan Verminous pneumonia Abattoir meat inspection 60 7.5 Sheep Not stated [28]
Golestan Verminous pneumonia Abattoir meat inspection 60 7.5 Goat Not stated [28]
Babol Verminous pneumonia Abattoir meat inspection 1000 1.6 Sheep Not stated [33]
Semnan P. rufescens + M. capillaris Abattoir meat inspection 380 1.5 Sheep/Goat 2015 [29]
Semnan D. filaria + P. rufescens Abattoir meat inspection 380 53.0 Sheep/Goat 2015 [29]
Semnan D. filaria + M. capillaris Abattoir meat inspection 380 1.5 Sheep/Goat 2015 [29]
Semnan D. f + P. r + M. c Abattoir meat inspection 380 7.6 Sheep/Goat 2015 [29]
Western Provinces Single infections
Boroujerd Dictyocaulus filaria Abattoir meat inspection 175 12.6 Sheep 2008–2009 [34]
Boroujerd Dictyocaulus filaria Abattoir meat inspection 140 9.3 Goat 2008–2009 [34]
Hamedan Dictyocaulus filaria Abattoir meat inspection 100 9.0 Sheep 2010–2011 [35]
Sanandaj Dictyocaulus filaria Abattoir meat inspection 164 8.5 Sheep 2017 [36]
Sanandaj Dictyocaulus filaria Abattoir meat inspection 45 4.4 Goat 2017 [36]
Boroujerd Protostrongylus rufescens Abattoir meat inspection 175 10.3 Sheep 2008–2009 [34]
Boroujerd Protostrongylus rufescens Abattoir meat inspection 140 8.6 Goat 2008–2009 [34]
Kermanshah Protostrongylus rufescens Abattoir meat inspection 492 0.4 Sheep 2013–2014 [37]
Boroujerd Cystocaulus ocreatus Abattoir meat inspection 175 10.9 Sheep 2008–2009 [34]
Boroujerd Cystocaulus ocreatus Abattoir meat inspection 140 7.9 Goat 2008–2009 [34]
Kermanshah Muellerius capillaris Abattoir meat inspection 492 0.2 Sheep 2013–2014 [37]
Mixed infections
Ilam Lungworms larvae Abattoir meat inspection 17,055 0.3 Sheep 2010–2011 [38]
Kermanshah Verminous pneumonia Abattoir meat inspection 1200 3.4 Sheep 2013–2014 [39]
Eastern Provinces Single infections
Mashhad Dictyocaulus filaria Abattoir meat inspection 2300 4.0 Sheep 2010–2011 [10]
Mashhad Dictyocaulus filaria Baermann 320 7.2 Sheep 2010–2011 [10]
Mashhad Dictyocaulus filaria Abattoir meat inspection 200 0.5 Goat 2010–2011 [10]
Mashhad Dictyocaulus filaria Baermann 30 3.3 Goat 2010–2011 [10]
Mashhad Protostrongylus rufescens Abattoir meat inspection 2300 0.3 Sheep 2010–2011 [10]
Mashhad Protostrongylus rufescens Baermann 320 4.7 Sheep 2010–2011 [10]
Northwestern Provinces Single infections
West Azarbaijan Dictyocaulus sp. Abattoir meat inspection 1325 1.5 Sheep Not stated [40]
Urmia Dictyocaulus filaria Abattoir meat inspection 240 17.1 Sheep 1994–1995 [41]
Urmia Dictyocaulus sp. Fecal flotation 1000 27.4 Sheep 1994–1995 [42]
Urmia Dictyocaulus sp. Fecal flotation 580 24.8 Goat 1995–1996 [43]
Urmia Dictyocaulus filaria Abattoir meat inspection 18,795 8.0 Sheep Not stated [44]
Tabriz Dictyocaulus filaria Abattoir meat inspection 400 34.0 Sheep 2006–2007 [45]
Tabriz Dictyocaulus filaria Baermann 1000 28.9 Sheep 2006–2007 [45]
Shabestar Dictyocaulus filaria Abattoir meat inspection 712 0.7 Sheep 2008 [46]
Tabriz Dictyocaulus filaria Abattoir meat inspection 235 26.8 Sheep Not stated [47]
Salmas Dictyocaulus filaria Abattoir meat inspection 1922 0.1 Sheep Not stated [48]
Zanjan Muellerius sp. Coprolite rehydration 1 Case report Sheep or goat Not stated [24]
Urmia Protostrongylus sp. Fecal flotation 1000 21.9 Sheep 1994–1995 [42]
Urmia Protostrongylus sp. Fecal flotation 580 41.9 Goat 1995–1996 [43]
Urmia Protostrongylus rufescens Abattoir meat inspection 18,795 8.4 Sheep Not stated [44]
Tabriz Protostrongylus rufescens Abattoir meat inspection 400 11.0 Sheep 2006–2007 [45]
Tabriz Protostrongylus rufescens Baermann 1000 12.7 Sheep 2006–2007 [45]
Shabestar Protostrongylus rufescens Abattoir meat inspection 712 0.7 Sheep 2008 [46]
Salmas Protostrongylus rufescens Abattoir meat inspection 1922 0.8 Sheep Not stated [48]
Urmia Cystocaulus ocreatus Abattoir meat inspection 240 36.3 Sheep 1994–1995 [41]
Urmia Cystocaulus sp. Fecal flotation 1000 32.9 Sheep 1994–1995 [42]
Urmia Cystocaulus sp. Fecal flotation 580 38.3 Goat 1995–1996 [43]
Urmia Cystocaulus ocreatus Abattoir meat inspection 18,795 8.6 Sheep Not stated [44]
Tabriz Cystocaulus ocreatus Abattoir meat inspection 400 32.0 Sheep 2006–2007 [45]
Tabriz Cystocaulus ocreatus Baermann 1000 29.4 Sheep 2006–2007 [45]
West Azarbaijan Cystocaulus sp. Fecal flotation 403 0.8 Goat 2007 [49]
Shabestar Cystocaulus ocreatus Abattoir meat inspection 712 3.9 Sheep 2008 [46]
Meshkinshahr Cystocaulus ocreatus Abattoir meat inspection 90 2.2 Sheep 2010 [50]
West Azarbaijan Muellerius sp. Abattoir meat inspection 1325 3.2 Sheep Not stated [40]
Urmia Muellerius sp. Fecal flotation 1000 26.3 Sheep 1994–1995 [42]
Urmia Muellerius sp. Fecal flotation 580 14.0 Goat 1995–1996 [43]
Urmia Muellerius capillaris Abattoir meat inspection 18,795 26.0 Sheep Not stated [44]
Tabriz Muellerius capillaris Baermann 1000 29.0 Sheep 2006–2007 [45]
Mixed infections
Urmia D. filaria + P. rufescens Abattoir meat inspection 240 3.8 Sheep 1994–1995 [41]
Urmia D. filaria + C. ocreatus Abattoir meat inspection 240 12.9 Sheep 1994–1995 [41]
Urmia D. f + P. r + C. o Abattoir meat inspection 240 5.4 Sheep 1994–1995 [41]
Urmia Lungworms larvae Abattoir meat inspection 2014 12.4 Sheep 2009 [51]
Urmia Verminous pneumonia Abattoir meat inspection 626 3.7 Sheep 2011 [52]
Southern Provinces Single infections
Shiraz Dictyocaulus sp. Baermann & abattoir meat inspection 102 21.1 Sheep Not stated [53]
Fars Dictyocaulus sp. Abattoir meat inspection 579 22.6 Sheep 1991 [54]
Shiraz Dictyocaulus filaria Abattoir meat inspection 1804 31.58 Sheep 2001–2005 [55]
Kerman Dictyocaulus filaria Abattoir meat inspection 210 6.2 Sheep 2015–2016 [56]
Shiraz Protostrongylus sp. Baermann & abattoir meat inspection 102 20.5 Sheep Not stated [53]
Fars Protostrongylus sp. Abattoir meat inspection 579 19.3 Sheep 1991 [54]
Shiraz Protostrongylus rufescens Abattoir meat inspection 1804 12.54 Sheep 2001–2005 [55]
Kerman Protostrongylus rufescens Abattoir meat inspection 210 57.8 Sheep 2015–2016 [56]
Fars Cystocaulus sp. Abattoir meat inspection 579 10.3 Sheep 1991 [54]
Shiraz Cystocaulus ocreatus Abattoir meat inspection 1804 4.42 Sheep 2001–2005 [55]
Shiraz Muellerius sp. Baermann & abattoir meat inspection 102 35.7 Sheep Not stated [53]
Fars Muellerius sp. Abattoir meat inspection 579 26.8 Sheep 1991 [54]
Shiraz Muellerius capillaris Abattoir meat inspection 1804 51.46 Sheep 2001–2005 [55]
Southwestern Provinces Single infections
Ahvaz Dictyocaulus filaria Abattoir meat inspection 4592 0.2 Sheep 2008–2009 [57]
Ahvaz Cystocaulus ocreatus Abattoir meat inspection 4592 0.3 Sheep 2008–2009 [57]
Mixed infections
Ahvaz D. filaria + C. ocreatus Abattoir meat inspection 4592 0.1 Sheep 2008–2009 [57]
Shahrekord Verminous pneumonia Abattoir meat inspection 1000 8.5 Sheep Not stated [58]
Ahvaz Verminous pneumonia Abattoir meat inspection 4592 0.5 Sheep 2008–2009 [57]
Samples from different regions Single infections
Dictyocaulus filaria Abattoir meat inspection 30 13.3 Goat Not stated [59]
Dictyocaulus filaria Baermann 30 13.3 Goat Not stated [59]
Dictyocaulus filaria Abattoir meat inspection 135 24.4 Sheep Not stated [60]
Protostrongylus rufescens Baermann 30 20.0 Goat Not stated [59]
Protostrongylus rufescens Abattoir meat inspection 30 13.3 Goat Not stated [59]
Protostrongylus rufescens Abattoir meat inspection 135 22.2 Sheep Not stated [60]
Cystocaulus ocreatus Baermann 30 10.0 Goat Not stated [59]
Cystocaulus ocreatus Abattoir meat inspection 30 13.3 Goat Not stated [59]
Cystocaulus ocreatus Abattoir meat inspection 135 11.1 Sheep Not stated [60]
Muellerius sp. Baermann 30 3.3 Goat Not stated [59]
Muellerius capillaris Abattoir meat inspection 135 25.9 Sheep Not stated [60]
Region not stated Single infections
Dictyocaulus filaria Baermann 1712 41.0 Sheep Not stated [61]
Dictyocaulus filaria Abattoir meat inspection 99 56.0 Sheep Not stated [61]
Dictyocaulus filaria Baermann 297 21.0 Goat Not stated [61]
Dictyocaulus filaria Abattoir meat inspection 19 42.0 Goat Not stated [61]
Protostrongylus sp. Baermann 1712 26.0 Sheep Not stated [61]
Protostrongylus sp. Abattoir meat inspection 99 6.0 Sheep Not stated [61]
Protostrongylus sp. Baermann 297 16.0 Goat Not stated [61]
Protostrongylus sp. Abattoir meat inspection 19 16.0 Goat Not stated [61]
Muellerius sp. Baermann 1712 16.0 Sheep Not stated [61]
Muellerius sp. Abattoir meat inspection 99 9.0 Sheep Not stated [61]
Muellerius sp. Baermann 297 22.0 Goat Not stated [61]
Muellerius sp. Abattoir meat inspection 19 5.0 Goat Not stated [61]
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Dictyocaulus filaria, P. rufescens, C. ocreatus, and M. capillaris were reported in small ruminants in decreasing order (Figure 1B). The variable prevalence rate (0.1 to 63.6%) of lungworm infection in the reviewed studies may be due to numerous factors, including epidemiological influences of temperature, climate, host age and health status, and differences in the biology of different parasite species. The study inevitably revealed many reports of co-infections of D. filaria and P. rufescens and/or C. ocreatus.

In a newly published study, two first-stage larvae of Muellerius sp. were reported from the rehydrated fecal pellet of “sheep or goat” collected in historically rich Chehrabad salt mine in Iran’s northwestern Zanjan province, where several salt men and their personal belongings have been discovered [24]. It is difficult to speciate the animal origin of ancient small ruminant fecal pellets [25] however, this finding shows that this small ruminant lungworm was present in Iran since the era of the Sasanian Empire (500 CE).

3.2. Cattle and Buffalo Lungworms

Seven of 8 studies reporting lungworm infection in cattle and buffaloes were peer-reviewed journal articles, and one was a dissertation. These studies were conducted in the provinces of Mazandaran and Gilan in the north, East Azerbaijan and West Azerbaijan in the northwest, and Fars in the south. Overall, 1416 animals were assessed for the presence of lungworm infection, comprising 1127 cattle and 289 water buffaloes. For the diagnosis in cattle, 50.9% (574) of the cases were examined at abattoir meat inspection, 38.4% (433) were examined using the Baermann technique and 10.6% (120) were examined using fecal flotation. For the diagnosis in buffaloes, 34.6% (100) of the cases were examined at abattoir meat inspection and 65.4% (189) were examined using the Baermann technique. In total, 12.5% (54/433) and 5% (6/120) of tested cattle were found infected by the Baermann technique and fecal flotation, respectively and 17.5% (33/189) water buffaloes were found infected by the Baermann technique (Table 2). In 6 studies, the prevalence of D. viviparus was reported to range from 0.2 to 28.5% in cattle, and from 2.6 to 26.3% in buffalos. Moreover, in two reports, infection of cattle with D. filaria in the Fars and Mazandaran provinces was associated with co-grazing with sheep and goats [62,63] (Figure 1B).

Table 2.

Lungworms of cattle and buffaloes in Iran according to geographical area, nematode species and diagnostic method.

Geographical Region Study Area Nematode Species Test # Tested % Prevalence Host Year of Study References
Northern Provinces Single infections
Mazandaran Dictyocaulus filaria Abattoir meat inspection 1 Case report Cattle Not stated [64]
Gilan Dictyocaulus viviparus Baermann 212 22.6 Cattle 2018 [65]
Gilan Dictyocaulus viviparus Abattoir meat inspection 212 2.4 Cattle 2018 [65]
Gilan Dictyocaulus viviparus Baermann 189 26.3 Buffalo 2018 [65]
Gilan Dictyocaulus viviparus Abattoir meat inspection 189 2.6 Buffalo 2018 [65]
Mazandaran Dictyocaulus viviparus Abattoir meat inspection 1 Case report Cattle Not stated [66]
Northwestern Provinces Single infections
Urmia Dictyocaulus viviparus Abattoir meat inspection 470 0.2 Cattle 1996–1997 [67]
Urmia Dictyocaulus viviparus Baermann 221 2.7 Cattle 1996–1997 [67]
Urmia - Abattoir meat inspection 400 0 Buffalo 1996–1997 [67]
Urmia - Baermann 135 0 Buffalo 1996–1997 [67]
Tabriz Dictyocaulus viviparus Fecal flotation 120 5.0 Cattle Not stated [68]
Tabriz Dictyocaulus viviparus Abattoir meat inspection 100 28.5 Cattle 2013 [69]
Tabriz Dictyocaulus viviparus Abattoir meat inspection 100 19.0 Buffalo 2013 [69]
Southern Provinces Single infections
Shiraz Dictyocaulus viviparus Abattoir meat inspection 1 Case report Cattle 1998 [70]
Shiraz Dictyocaulus filaria Abattoir meat inspection 1 Case report Cattle 2003 [62]
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3.3. Wild Ruminant Lungworms

Seven wild ruminant species are present in Iran, namely four species of the family Bovidae (goitered gazelle (G. subgutturosa), chinkara (Gazella bennettii), wild goat (C. aegagrus) and urial (O. orientalis)) and three species of the family Cervidae (Persian fallow deer (Dama mesopotamica), red deer (C. elaphus) and European roe deer (C. capreolus)). These species they are generally under protection in national parks or protected areas, and subject to close monitoring. The parasitic fauna of wild ruminants in Iran is poorly studied. Five peer-reviewed journal articles, one Master’s dissertation, and one conference paper contained information on lungworms of wild ruminants. Overall, 587 wild ruminant individuals belonging to five species were examined with an overall infection of 38.7% (227/587). 38% of urial, 37% of wild goats, 5% of goitered gazelles and 67% of red deer were reported to be infected with lungworms belonging to four genera of Dictyocaulus, Protostrongylus, Cystocaulus and Muellerius. A single case report described Dictyocaulus lungworm infection in a roe deer. 53.1% (312/587), 21.1% (124/587) and 17.2% (101/587) of cases were examined postmortem, by Baermann technique and fecal flotation, respectively. Urial have been studied more than the other wild ruminant species i.e., 367 urial were examined in four studies followed by 133 wild goats in three, 56 goitered gazelles in two, and 30 red deer in one studies. In one case report a single European roe deer was examined (Table 3). The reported prevalence of infection in urial ranged from 1% to 78% in different regions. Interestingly, high prevalences of C. ocreatus (94%), D. filaria (78%), and Muellerius sp. (70%) were reported in a study of Kaboodan Island on Urmia Lake, where animals are living in an isolated area without any external source of infection from domesticated animals [71].

Table 3.

Reports on lungworm infections of wildlife ruminants.

Geographical Region Study Area Nematode Species Test # Tested % Prevalence Host Year of Study References
Northern Provinces Single infection
Amol Dictyocaulus sp. Postmortem 1 Case report Capreolus capreolus 2013 [63]
Northwestern Provinces Single infections
Kabodan island-Urmia Dictyocaulus filaria Postmortem 50 78.0 Ovis orientalis 1994–1995 [72]
Kabodan island-Urmia Protostrongylus rufescens Postmortem 50 38.0 Ovis orientalis 1994–1995 [72]
Kabodan island-Urmia Cystocaulus ocreatus Postmortem 50 94.0 Ovis orientalis 1994–1995 [72]
East Azarbaijan Muellerius capillaris Fecal flotation 30 40.0 Capra aegagrus 2015 [73]
East Azerbaijan Dictyocaulus sp. Fecal flotation 30 66.6 Cervus elaphus 2015 [73]
East Azarbaijan Cystocaulus sp. Baermann 74 36.0 Capra aegagrus 2016 [74]
Mixed infection
Urmia Lungworm larvae Fecal flotation 41 34.1 Ovis orientalis 2002–2003 [71]
National Park & protected regions of Iran Single infections
Not defined Dictyocaulus filaria Postmortem 250 14.4 Ovis orientalis Not stated [75]
Not defined Dictyocaulus eckerti Postmortem 250 1.6 Ovis orientalis Not stated [75]
Not defined Protostrongylus rufescens Postmortem 250 17.6 Ovis orientalis Not stated [75]
Not defined Protostrongylus rufescens Postmortem 29 3.5 Capra aegagrus 2011–2012 [76]
Not defined Protostrongylus rufescens Postmortem 32 3.0 Gazella subgutturosa Not stated [75]
Not defined Protostrongylus raillietti Postmortem 250 4.8 Ovis orientalis Not stated [75]
Not defined Cystocaulus ocreatus Postmortem 32 6.3 Gazella subgutturosa Not stated [75]
Not defined Muellerius sp. Postmortem 250 1.1 Ovis orientalis Not stated [75]
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3.4. Anthelminthic Drug Efficacy

Four studies, including 3 on sheep and goat lungworms and 1 on cattle lungworms have evaluated the efficacy of 9 anthelmintic active compounds (Table 4). Historically, methyridine (200 mg/kg PO), diethylcarbamazine (20 mg/kg IM), tetramisole (15 mg/kg PO), thiabendazole (100 mg/kg PO), and fenbendazole (20 mg/kg) were 100% effective for the treatment of D. filaria in sheep, while cyanacethydrazide (20 mg/kg SC) showed 83% efficacy [77]. The efficacies of thiabendazole (100 mg/kg PO), tetramisole (15 mg/kg PO), emetine hydrochloride (1 mg/kg PO) and fenbendazole (20 mg/kg) against P. rufescens were 97% (goats), 90% (goats), 91% (goats) and 100% (sheep), respectively [77]. The efficacies of thiabendazole (100 mg/kg PO), tetramisole (15 mg/kg PO), diethylcarbamazine (20 mg/kg IM) against Muellerius spp. in sheep were 56%, 26% and 28%, respectively; while the efficacies of thiabendazole (100 mg/kg PO), emetine hydrochloride (1 mg/kg PO) and emetine hydrochloride (3 mg/kg PO) against Muellerius spp. in goats were 46%, 68%, and 99%, respectively [77]. Fenbendazole (20 mg/kg PO) was 100% effective against C. ocreatus in sheep [78]. These anthelmintic drugs, with the exception of fenbendazole, are no longer licensed, or available for use in livestock. A single study evaluated a pour-on ivermectin formulation against D. viviparus in cattle, and reported efficacy of 99% [68].

Table 4.

Anthelminthic efficacy tests on lungworms of ruminants in Iran.

Drug Helminth Species Host Dose and Route of Administration a Efficacy (%) References
Cyanacethydrazide Dictyocaulus filaria Sheep 20 mg/kg SC b 83 [61]
Methyridine Dictyocaulus filaria Sheep 200 mg/kg PO c 100 [61]
Diethylcarbamazine Dictyocaulus filaria Sheep 20 mg/kg IM d 100 [61]
Tetramisole Dictyocaulus filaria Sheep 15 mg/kg PO 100 [61]
Thiabendazole Dictyocaulus filaria Sheep 100 mg/kg PO 100 [77]
Thiabendazole Muellerius sp. Sheep 100 mg/kg PO 56 [77]
Tetramisole Dictyocaulus filaria Sheep 5 mg/kg PO 86 [77]
10 mg/kg PO 100
Tetramisole Muellerius sp. Sheep 15 mg/kg PO 26 [77]
Diethylcarbamazine Muellerius sp. Sheep 20 mg/kg IM 28 [77]
Thiabendazole Protostrongylus rufescens Goat 100 mg/kg PO 97 [77]
Thiabendazole Muellerius sp. Goat 100 mg/kg PO 46 [77]
Tetramisole Protostrongylus rufescens Goat 15 mg/kg PO 90 [77]
Emetine hydrochloride Protostrongylus rufescens Goat 1 mg/kg PO 91 [77]
Emetine hydrochloride Muellerius sp. Goat 1 mg/kg PO 68 [77]
Emetine hydrochloride Muellerius sp. Goat 3 mg/kg PO 99.45 [77]
Fenbendazole e Dictyocaulus filaria Sheep 20 mg/kg 100 [78]
40 mg/kg 100
60 mg/kg 100
80 mg/kg 100
Fenbendazole e Protostrongylus rufescens Sheep 20 mg/kg 100 [78]
40 mg/kg 100
60 mg/kg 100
80 mg/kg 100
Fenbendazole e Cystocaulus ocreatus Sheep 20 mg/kg 100 [78]
40 mg/kg 100
60 mg/kg 100
80 mg/kg 100
Ivermectin pour-on Dictyocaulus viviparus Cattle 0.5 mg/kg 99.21 [68]
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a In publication, b Subcutaneous, c Oral, d Intramuscular, e currently available and labelled for lungworm treatment.

4. Discussion

Around the world, lungworms are important causes of production inefficiency in pastoral livestock systems; albeit there has been a lack of critical evaluation of the impact of and rationale for control strategies in Iran. This study shows a high prevalence of lungworm in those provinces from which diagnostic information is available, consistent with the situation in neighboring countries, with similar climates, environments and pastoral animal management. For instance, in a study in Nangarhar, Afghanistan, 21.8% of 504 sheep examined in an abattoir were infected with lungworms [79], albeit the authors did not define the lungworm species. In Lahore, Pakistan, 31% of sheep and 11% of goats were found harboring lungworms, including D. filaria, P. rufescens, and M. capillaris [80]. Dictyocaulus filaria was also reported in 0.4% and 8.3% of sheep and goats, respectively, in the Chiltan National Park, Balochistan, Pakistan [81]. In Turkey, a relatively higher prevalence was reported in sheep, with 62.5% and 45.1% of animals testing positive in post-mortem and fecal examinations, respectively [79,82]. Regarding bovines, in neighboring Turkey, the prevalence of D. viviparus in cattle ranged between 0.3% and 70% [83], and in Faisalabad, Pakistan, the prevalence of D. viviparus infection in cattle and buffaloes was 4.8% and 5.1%, respectively [84]. Dictyocaulus viviparus lungworms present in Iran can have a major impact on cattle milk yields and growth rates, and cause death [5]. Muellerius and Protostrongylus spp. present in Iran also impact livestock production, in particular through the rejection of plucks at abattoir meat inspection [85]. This study, therefore, identifies a need to determine and implement appropriate, effective, and sustainable control strategies, based on a priori knowledge of the parasites’ life histories and contemporary understanding of the host, management and climatic factors influencing their epidemiology [86] under local Iranian conditions.

This study shows the presence of 7 species of lungworm in Iran, and the high prevalence of D. viviparus in cattle, and D. filaria, Muellerius and Protostrongylus spp. in sheep. The accuracy of species determination, in particular in mixed infections, must be interpreted with caution due to indistinct morphological traits of L1 [87]. The scarcity of published reports on cattle and buffaloes might not represent the true distribution and prevalence of lungworm infection in Iran. These hosts are widely distributed across the country, but due to ongoing droughts, the majority of cattle are housed with relatively good nutrition and limited exposure to infective lungworm L3; possibly accounting for the low prevalence of infection.

The control of lungworm infections in livestock is more challenging than that of gastrointestinal nematodes, not least because Dictyocaulus spp. infective L3 can be introduced by windborne spread, or survive for prolonged periods in the soil, while knowledge concerning the intermediate snail host specificity and distribution is lacking for Protostrongylus and Muellerius spp. The fundamental principal for control of Dictyocaulus spp. is to allow the establishment and maintenance of host immunity, which is rapidly acquired but requires lifelong boosting [88]. This usually requires the judicious use of anthelmintic drugs to reduce pasture contamination and thereby avoid high levels of infective L3 challenge. In some countries, this is complimented by vaccination [89]. However, these strategies are frequently unsuccessful in some regions, lungworms have become the predominant infectious disease causing production loss in cattle; putatively because climate change has extended periods of pasture growth and availability of infectious L3 [90]. In the absence of understanding of the factors influencing the epidemiology of Muellerius and Protostrongylus spp., control strategies are limited to the periodic use of anthelmintic drug treatments. Knowledge of drug efficacy against lungworm species is therefore, needed.

The modern-broad spectrum benzimidazole, imidazothiazole and macrocyclic lactone anthelmintic drugs are effective against L4 and adult stages of Dictyocaulus spp. in sheep and cattle [91]. In most countries, these drugs are not licensed for use in goats. However, there are no data sheet claims of efficacy of these drug groups against Muellerius and Protostrongylus lungworms. Currently, different anthelminthic products in forms of oral solution (levamisole, albendazole, fenbendazole, mebendazole, ivermectin, moxidectin), oral bolus (mebendazole) and injectable solution (ivermectin, doramectin) are labelled for treatment of lungworms in ruminants in Iran. This study included a single recent report of high efficacy of an ivermectin pour-on formulation against D. viviparus in cattle, and a historic report of high efficacy of an oral benzimidazole drug against D. filaria and P. rufescens in sheep. The no longer available, toxic and narrow spectrum anthelmintic drugs showed poor efficacy against Muellerius spp. (Table 4). There is, therefore, a need to demonstrate the efficacies of modern broad-spectrum anthelmintics against the lungworm species that are present in Iran. Drugs with efficacies less than 100%, can still be useful for lungworm control, but their use risks selection for anthelmintic resistance. Poor efficacy against certain parasite species may be due to inherent pharmacological properties of the drugs, which may be stage specific, for example differing between adults and migrating stages in the lymphatics [91].

Poor drug efficacy may indicate anthelmintic resistance; the emergence of which threatens the efficiency of food production from livestock irreversibly [92]. Dictyocaulus viviparus resistance to pour-on macrocyclic lactone drugs has been suggested, but not proven [93]. In Iran, there is growing evidence regarding resistance of trichostrongylid nematodes to common broad-spectrum benzimidazole and imidazothiazole compounds [94,95]. Many Iranian farmers do not adhere to recognized best practices of anthelminthic therapy [95], and resistance in gastrointestinal helminths has been reported [94,96]. There is, therefore, an urgent need to regularly evaluate different drug classes used in the treatment of lungworm infections, using studies designed according to international guidelines, and also respecting withdrawal periods for consumption and commercialization of milk and meat [97]. Strategies such as educating the farmers, combining anthelmintic drug classes, and developing antiparasitic vaccines and novel drugs could ameliorate the problem of anthelmintic resistance [95,98,99].

This study highlights the presence of lungworm infection in wildlife in Iran. It is important as wild species could act as reservoirs of infection for co-managed livestock [16]. While optimum strategies are needed for wild ruminant parasite control according to the diverse conditions of each region in Iran, the ethics and impacts of strategies such as non–intervention, or treatments with broad spectrum-drugs are unknown [100]. Furthermore, although it is known that different species of Varestrongylus and Elaphostrongylus parasitize the respiratory tracts of wild and domestic ungulates within the families Bovidae and Cervidae [101,102] these genera have not been recorded in wild ruminants of Iran. More focused studies with the aid of molecular techniques are first needed to explore lungworm infections in Iranian wildlife and co-managed pastoral livestock.

5. Conclusions

This work provides a framework for the development of effective and sustainable lungworm control strategies, and identifies areas of need for further research. Studies are needed to identify the environmental, climatic and management conditions that play a key role in the epidemiology of lungworm infection in Iran. These studies require the integration of conventional parasitology and molecular diagnostic methods for species level identification of lungworms, to inform cross-host species transmission, and reveal cryptic biodiversity. Large-scale studies should be designed to determine the prevalence of lungworm infection in Iran, to ensure the sustainability of control programs and mitigate against associated economic losses.

Acknowledgments

Authors wish to thank Moosa Tavassoli, Armen Badali, Mahsa Shahbakhsh and Ahmad Nematollahi for their assistance in access to documents in universities of Urmia, Tehran and Tabriz. We are also thankful to Kiavash Hushmandi for his comments on the manuscript.

Author Contributions

Conceptualization, A.S. and S.Z.; methodology, A.S. and S.Z.; investigation, S.Z., A.S. and A.B.; writing—original draft preparation, S.M., S.Z., A.B., A.S., N.D.S. and G.G.V.; writing—review and editing, A.S., N.D.S. and G.G.V.; supervision, A.S.; project administration, A.S. and A.B. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare that they have no competing interest.

Funding Statement

This research received no external funding.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Poulin R., Morand S. Parasite Biodiversity. Smithsonian Institution; Washington, DC, USA: 2005. [Google Scholar]
  • 2.Jephcott T.G., Sime-Ngando T., Gleason F.H., Macarthur D.J. Host–parasite interactions in food webs: Diversity, stability, and coevolution. Food Webs. 2016;6:1–8. doi: 10.1016/j.fooweb.2015.12.001. [DOI] [Google Scholar]
  • 3.Barger I. Population regulation in trichostrongylids of ruminants. Int. J. Parasitol. 1987;17:531–540. doi: 10.1016/0020-7519(87)90129-9. [DOI] [PubMed] [Google Scholar]
  • 4.Holzhauer M., Van Schaik G., Saatkamp H., Ploeger H. Lungworm outbreaks in adult dairy cows: Estimating economic losses and lessons to be learned. Vet. Rec. 2011;169:494. doi: 10.1136/vr.d4736. [DOI] [PubMed] [Google Scholar]
  • 5.Sargison N. The unpredictable epidemiology of Dictyocaulus viviparus lungworm infection of cattle. Vet. Irel. J. 2016;6:387–391. [Google Scholar]
  • 6.Panuska C. Lungworms of ruminants. Vet. Clin. Food Anim. Pract. 2006;22:583–593. doi: 10.1016/j.cvfa.2006.06.002. [DOI] [PubMed] [Google Scholar]
  • 7.Gerichter C.B. Studies on the lung nematodes of sheep and goats in the Levant. Parasitology. 1951;41:166–183. doi: 10.1017/S0031182000084018. [DOI] [PubMed] [Google Scholar]
  • 8.Lesage C., Jouet D., Patrelle C., Guitton J.S., Decors A., Ferté H. Protostrongylus pulmonalis (Frölich, 1802) and P. oryctolagi Baboš, 1955 (Nematoda: Protostrongylidae), parasites of the lungs of European hare (Lepus europaeus L.) in France: Morphological and molecular approaches. Parasitol. Res. 2014;113:2103–2111. doi: 10.1007/s00436-014-3860-6. [DOI] [PubMed] [Google Scholar]
  • 9.Kuchboev A., Krücken J., Karimova R., Ruziev B., Pazilov A. Infection levels of protostrongylid nematodes in definitive caprine and intermediate gastropod hosts from Uzbekistan. J. Helminthol. 2017;91:236–243. doi: 10.1017/S0022149X16000171. [DOI] [PubMed] [Google Scholar]
  • 10.Borji H., Azizzadeh M., Ebrahimi M., Asadpour M. Study on small ruminant lungworms and associated risk factors in northeastern Iran. Asian Pac. J. Trop. Med. 2012;5:853–856. doi: 10.1016/S1995-7645(12)60159-X. [DOI] [PubMed] [Google Scholar]
  • 11.Forbes A. Lungworm in cattle: Epidemiology, pathology and immunobiology. Livest. 2018;23:59–66. doi: 10.12968/live.2018.23.2.59. [DOI] [Google Scholar]
  • 12.Jørgensen R.J. Bovine dictyocaulosis. Acta Vet. Scand. 1980;21:658–676. doi: 10.1186/BF03546853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Wernery U., Kinne J., Schuster R.K. Camelid Infectious Disorders. OIE (World Organisation for Animal Health); Paris, France: 2014. [Google Scholar]
  • 14.Sazmand A., Joachim A. Parasitic diseases of camels in Iran (1931–2017)—A literature review. Parasite. 2017;24:21. doi: 10.1051/parasite/2017024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Johnson M., Mackintosh C., Labes R., Taylor M., Wharton D. Dictyocaulus species: Cross infection between cattle and red deer. N. Z. Vet. J. 2003;51:93–98. doi: 10.1080/00480169.2003.36346. [DOI] [PubMed] [Google Scholar]
  • 16.Walker J.G., Morgan E.R. Generalists at the interface: Nematode transmission between wild and domestic ungulates. Int. J. Parasitol. Parasite Wildl. 2014;3:242–250. doi: 10.1016/j.ijppaw.2014.08.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Anderson R. Nematode Parasites of Vertebrates: Their Development and Transmission, the Superfamily Metastrongyloidea. CABI; Wallingford, UK: 2000. [Google Scholar]
  • 18.Mansfield L., Gamble H., Baker J., Lichtenfels J. Lungworm infection in a sheep flock in Maryland. J. Am. Vet. Med. Assoc. 1993;202:601–606. [PubMed] [Google Scholar]
  • 19.Panayotova-Pencheva M.S., Alexandrov M.T. Some pathological features of lungs from domestic and wild ruminants with single and mixed protostrongylid infections. Vet. Med. Int. 2010;2010:741062. doi: 10.4061/2010/741062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Rose J. Observations on the larval stages of Muellerius capillaris within the intermediate hosts Agriolimax agrestis and A. reticulatus. J. Helminthol. 1957;31:741062. doi: 10.1017/S0022149X00033241. [DOI] [PubMed] [Google Scholar]
  • 21.Sauerländer R. Experimental infection of sheep and goats with Muellerius capillaris (Protostrongylidae, Nematoda) J. Vet. Med. B. 1988;35:525–548. doi: 10.1111/j.1439-0450.1988.tb00527.x. [DOI] [PubMed] [Google Scholar]
  • 22.Geurden T., Vercruysse J. Field efficacy of eprinomectin against a natural Muellerius capillaris infection in dairy goats. Vet. Parasitol. 2007;147:190–193. doi: 10.1016/j.vetpar.2007.04.003. [DOI] [PubMed] [Google Scholar]
  • 23.Yildiz K., Karahan S., Cavusoglu K. The fine structures of Cystocaulus ocreatus (Nematoda: Protostrongylidae) and the related lung pathology. Helminthologia. 2006;43:208–212. doi: 10.2478/s11687-006-0039-4. [DOI] [Google Scholar]
  • 24.Wu T.K., Heidari Z., Makki M.S., Yazdi B., Aali A., Stöllner T., Boenke N., Bowman D.D., Mowlavi G. First paleoparasitological evidence of Muellerius sp. in sheep or goat dated to the Sasanian Empire (500 CE) in ancient Iran. Vet. Parasitol. Reg. Stud. Rep. 2022;34:100758. doi: 10.1016/j.vprsr.2022.100758. [DOI] [PubMed] [Google Scholar]
  • 25.Sazmand A. Paleoparasitology and archaeoparasitology in Iran: A retrospective in differential diagnosis. Int. J. Paleopathol. 2021;32:50–60. doi: 10.1016/j.ijpp.2020.11.005. [DOI] [PubMed] [Google Scholar]
  • 26.Azaryanyazdi K. D.V.M. Thesis. University of Tehran; Tehran, Iran: 1961. Study on Sheep and Goat Lungworms in Tehran Slaughterhouse. (In Persian) [Google Scholar]
  • 27.Taher A.A. D.V.M. Thesis. University of Tehran; Tehran, Iran: 1996. Pathological Examination of Sheep and Goat Pneumonia in Tehran Slaughterhouse. (In Persian) [Google Scholar]
  • 28.Ranjbar-Bahadori S., Eslami A., Agha-Ebrahimi-Samani R. Study on parasitic infection of domestic ruminants in Golestan province. J. Fac. Vet. Med. Univ. Tehran. 2007;62:303–305. (In Persian with English abstract) [Google Scholar]
  • 29.Orouei M. D.V.M. Thesis. University of Semnan; Semnan, Iran: 2016. Prevalence of Lungworm Infestation in Sheep and Goat in Semnan. (In Persian with English abstract) [Google Scholar]
  • 30.Aghazadeh F., Yakhchali M. Study on parasitic helminths infection in gastrointestinal tract and respiratory system of sheep in Gilan Province, Northern Iran. Vet. Res. Biol. Prod. 2020;33:26–32. doi: 10.22092/vj.2019.125386.1559. (In Persian with English abstract) [DOI] [Google Scholar]
  • 31.Tabatabayi A.H., Gharagozlou M.J., Ghader-Sohi A. A survey of Mycoplasma arginini and other agents from subacute and chronic ovine pneumonia in Iran. Prev. Vet. Med. 1992;12:153–158. doi: 10.1016/0167-5877(92)90077-S. [DOI] [Google Scholar]
  • 32.Bokaei S., Rokni N., Hoseini S., HoseiniNasab Z. Prevalence of recorded lesions of sheeps sent to Lavasan slaughterhouse J. Fac. Vet. Med. Univ. Tehran. 1999;54:19–23. (In Persian with English abstract) [Google Scholar]
  • 33.Sedaghat R., Ranjbar-Bahadori S., Lotfollah-Zahed S., Hassanpour M. Macroscopic and microscopic study on pulmonary lesions in slaughtered sheep from Babol. Vet. Microbiol. 2007;1:41–45. (In Persian with English abstract) [Google Scholar]
  • 34.Hashemi S., Eslami A., Vosogh H., Kakekhani S. Study on the prevalence of lungworm infection in the sheep and goats in Boroujerd slaughterhouse. Vet. Clin. Res. J. 2011;5:61–66. (In Persian) [Google Scholar]
  • 35.Gharekhani J., Gerami-Sadeghian A., Yousefi M.R. Parasitic helminth infections in native sheep (Mehraban) in Hamedan, Iran. J. Adv. Vet. Anim. Res. 2015;2:115–119. doi: 10.5455/javar.2015.b59. [DOI] [Google Scholar]
  • 36.Sadeghi-Dehkordi Z., Partoandazanpour A., Abdolmaleki N., Sari A.A., Sadeghi-Nasab A. Survey on zoonotic parasites in Sanandaj slaughterhouse, 1396. Iran. J. Clin. Infect. Dis. 2019;23:25–36. (In Persian) [Google Scholar]
  • 37.Hashemnia M., Chalechale A., Malmir E. Pulmonary lesions in slaughtered sheep in Western Iran: Gross and histopathological findings. Vet. Ital. 2019;55:47–56. doi: 10.12834/VetIt.785.3795.3. [DOI] [PubMed] [Google Scholar]
  • 38.Seyd-Yousefi S., Karampour R. A study on prevalence of parasitic infections in lung and liver of sheeps and goats slaughtered in Ilam slaughterhouse; Proceedings of the 17th Iranian Veterinary Congress; Tehran, Iran. 28–30 April 2012; (In Persian) [Google Scholar]
  • 39.Malmir E. D.V.M. Thesis. University of Razi; Kermanshah, Iran: 2015. A Study on the Prevalence of Sheep Lung Lesions in Kermanshah Slaughter House: Pathological and Parasitological Study. (In Persian with English abstract) [Google Scholar]
  • 40.Yazdi-Shahreza M.R. D.V.M. Thesis. University of Urmia; Urmia, Iran: 1991. Histopathological Study of Sheep Lung Lesions in West Azerbaijan Province and Their Statistical Estimation. (In Persian) [Google Scholar]
  • 41.Eisaleva-Asl M. D.V.M. Thesis. University of Urmia; Urmia, Iran: 1995. Investigation of Sheep Pulmonary Nematodes in Urmia Slaughterhouse. (In Persian) [Google Scholar]
  • 42.Tavassoli M., Kiani N. A survey on annual infestation of sheep to respiratory nematodes in Urmia based on fecal test. Vet. Res. Biol. Prod. 1999;11:169–171. (In Persian with English abstract) [Google Scholar]
  • 43.Tavassoli M., Mokhtari M. Investigation of contamination of Urmia goats with respiratory nematodes. Vet. Res. Biol. Prod. 2000;13:141. (In Persian) [Google Scholar]
  • 44.Yakhchali M., Lotfi A. Investigation of lungworm contamination in buffalo and sheep in industrial slaughterhouse of Urmia. Vet. Res. Biol. Prod. 2003;16:101–102. (In Persian) [Google Scholar]
  • 45.Nematollahi A., Moghaddam G.A. A survey on annual infestation of sheep with lung worms based on fecal test and slaughter house study in Tabriz. J. Vet. Res. 2009;64:339–342. (In Persian with English abstract) [Google Scholar]
  • 46.Sadeghian M., Eshrat-khah B., Moharar E. Prevalence of respiratory parasites in sheep in Shabestar slaughterhouse; Proceedings of the First National Congress of Veterinary Laboratory Sciences; Tehran, Iran. 1–2 December 2009; (In Persian) [Google Scholar]
  • 47.Nematollahi A. Survey on infestation to Dictyocaulus fillaria in slaughtered sheep in Tabriz (Northwest of Iran); Proceedings of the XVth International Congress of the International Society for Animal Hygiene; Vienna, Austria. 3–7 July 2011. [Google Scholar]
  • 48.Rezaeian A., Ghasemi A., Rasouli S. Prevalence of lungworms in sheep in Salmas slaughterhouse; Proceedings of the 17th Iranian Veterinary Congress; Tehran, Iran. 28–30 April 2012; (In Persian) [Google Scholar]
  • 49.Tavassoli M., Dalir-Naghadeh B., Sahandi A. Study on gastrointestinal and external parasites of goats in West Azerbaijan, Iran. J. Fac. Vet. Med. Univ. Tehran. 2011;66:77–79. (In Persian with English abstract) [Google Scholar]
  • 50.Heidari Z., Mobedi I., Mirhendi S., Mikaeaili F., Zarei Z., Beigom E. Coexistence of adult worms, larvae, and eggs of Cystocaulus ocreatus with hydatid cysts protoscolices in sheep lungs; Proceedings of the 9th National Congress of Parasitology and Parasitic Diseases of Iran; Guilan, Iran. 20–22 May 2015. [Google Scholar]
  • 51.Bahrami M., Emami J., Rezaei F., Bahrami R. prevalence of recorded lesions of sheep sent to the industrial slaughterhouse of Urmia city; Proceedings of the 16th Iranian Veterinary Congress; Tehran, Iran. 27–29 April 2010; (In Persian) [Google Scholar]
  • 52.Araghi-Sore A., Hoseinzad-Nazlu M., Nassiri M. Study on the prevalence of pulmonary lesions of slaughtered sheep at Urmia abattoir. Vet. Clin. Pathol. 2013;7:229–238. (In Persian with English abstract) [Google Scholar]
  • 53.Ebrahimi M. D.V.M. Thesis. University of Shiraz; Shiraz, Iran: 1990. Evaluation of Lung Parasitic Infection of Slaughter Sheep in Shiraz Slaughterhouses in Summer and Its Pathological Effects. (In Persian) [Google Scholar]
  • 54.Sadeghi-Faridi J. D.V.M. Thesis. University of Shiraz; Shiraz, Iran: 1992. Investigation of Seasonal Prevalence of Pulmonary Worms in Slaughtered Sheep in Fars Meat Complex. (In Persian) [Google Scholar]
  • 55.Moghaddar N., Shekarforoush S., Afrahi A. Seasonal dynamics in lungworm infections in sheep. J. Parasit. Dis. 2008;32:42–46. [Google Scholar]
  • 56.Heydari-moghadam M. Master’s Thesis. Shahid Bahonar University; Kerman, Iran: 2017. Parasitological and Pathological Study of Lungworms of Sheep Slaughtered in Kerman Slaughterhouse in 2015. (In Persian with English abstract) [Google Scholar]
  • 57.Esmaeilzadeh S., Sabagh A., Mohammadian B., Alborzi A., Ghorbanpoor M., Pourmehdi-Borujeni M. Frequency of ovine pulmonary lesions in Ahvaz slaughterhouse: Pathological, bacteriological and parasitological study. Iran. Vet. J. 2014;9:14–24. (In Persian with English abstract) [Google Scholar]
  • 58.Karimi I., Mohammadnia A. An abattoir survey of pulmonary lesions of sheep in Shar-e-Kord region. Anim. Sci. J. 2003;6:78–81. (In Persian with English abstract) [Google Scholar]
  • 59.Feyzi A. D.V.M. Thesis. University of Tehran; Tehran, Iran: 1975. A Study on Gastrointestinal Tract and Respiratory Parasites in Tehran Slaughterhouse. (In Persian) [Google Scholar]
  • 60.Farshian M. D.V.M. Thesis. University of Tehran; Iran: 1976. A Study on Lungworms in Sheep in Iran. (In Persian) [Google Scholar]
  • 61.Skerman K.D., Shahlapour A.A., Eslami A.H., Eliazian M. Anthelmintics for Dictyocaulus filaria in sheep. Arch. Razi Inst. 1970;22:177–185. [Google Scholar]
  • 62.Moazeni M., Khodakaram-Tafti A. Verminous pneumonia in a calf caused by Dictyocaulus filaria. Vet. Rec. 2007;160:380. doi: 10.1136/vr.160.11.380. [DOI] [PubMed] [Google Scholar]
  • 63.Vahedi-Nouri N., Gholampour M., Torabizadeh Z., Foroghi H., Golchin M. A case of severe infection of mountain goats (Capreulus capreulus) with Dictyocaolus spp. in Mazandaran (Amol city); Proceedings of the 9th National Congress of Parasitology and Parasitic Diseases of Iran; Guilan, Iran. 20–22 May 2015. [Google Scholar]
  • 64.Beheshti B., Yousefi M. First report of Dictyocaolus filaria from caw lung in Mazandaran province; Proceedings of the First National Congress of Parasitic Disease and Zoonotic Parasites; Tehran, Iran. 14–15 November 2018. [Google Scholar]
  • 65.Jamshidi K., Zahedi A., Seidavi A., Poorghasemi M.R. Slaughterhouse study on the prevalence and pathological lesions caused by Dictyocaulus viviparus infection in cattle and water buffaloes. Iran. J. Med. Microbiol. 2020;14:584–595. doi: 10.30699/ijmm.14.6.584. [DOI] [Google Scholar]
  • 66.Vahedi-Noori N., Salehi A. Verminous pneumonia in a calf from a dairy farm unit. Anim. Husb. Dairy Vet. Sci. 2019;3:35–36. doi: 10.15761/AHDVS.1000152. [DOI] [Google Scholar]
  • 67.Tavassoli M., Shafipour R., Akbari G. Study of Dictyocaolus viviparus infection in cattle and buffalo in Urmia. J. Fac. Vet. Med. Univ. Tehran. 2000;55:69–70. (In Persian with English abstract) [Google Scholar]
  • 68.Garedaghi Y., Khayatnouri M., Safarmashaei S. The effect of ivermectin pour-on administration against natural Dictyocoulus viviparous infestations and prevalence rate of that in cattle. J. Anim. Vet. Adv. 2011;10:2546–2549. doi: 10.3923/javaa.2011.2546.2549. [DOI] [Google Scholar]
  • 69.Alipourazar M., Garedaghi Y., Hashemzadefarhang H. Prevalence of cattle and buffalo lungworm infestation in Tabriz city, Iran. Biol. Forum Int. J. 2015;7:195–198. [Google Scholar]
  • 70.Moazeni M., Shekarforoush S.S., Hadipour M.M. The first report of cattle infection with Dictyocaulus viviparus in Fars province. J. Fac. Vet. Med. Univ. Tehran. 2000;55:5–6. (In Persian with English abstract) [Google Scholar]
  • 71.Tavassoli M., Khoshvaghti H. Helminthes and coccidia infection of wild sheep (Ovis ammon Orintalis) in Kabodan island of National Park of Urmia Lake, Iran. Vet. Res. Forum. 2010;1:26–29. [Google Scholar]
  • 72.Tavassoli M., Jalil-Jamshidi R. Lung and liver helminths of wild sheep (Ovis ammon orintalis) from Kabodan island, national park of Urmia Lake (North west of Iran) J. Vet. Parasitol. 2001;15:71–72. [Google Scholar]
  • 73.Norouzi R., Ouzbandi A. Survey of gastrointestinal parasite in wild boar (Sus scrofa), wild goat (Capra aegagrus) and red deer (Cervus elaphus) in the Aynaloo protected area, East Azerbaijan. Vet. Clin. Pathol. 2017;11:107–117. (In Persian with English abstract) [Google Scholar]
  • 74.Mardomi H. Master’s Thesis. University of Tabriz; Tabriz, Iran: 2017. Prevalence of infection with internal parasites in wild goats (Capra aegagrus) Arasbaran National Park. (In Persian with English abstract) [Google Scholar]
  • 75.Eslami A., Nikbin S., Rahbari S. Lugworm infection of wild sheep (Ovis ammon orientalis) and gazelle (Gazella subgutturosa) in Iran. J. Fac. Vet. Med. Univ. Tehran. 1980;35:11–16. (In Persian) [Google Scholar]
  • 76.Modabbernia G., Meshgi B., Eslami A. Diversity and burden of helminthiasis in wild ruminants in Iran. J. Parasit. Dis. 2021;45:394–399. doi: 10.1007/s12639-020-01314-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Shahlapour A., Eslami A., Eliazian H. Comparative anthelmintic tests in sheep and goats infected with gastro-intestinal nematodes and lungworms in Iran. Trop. Anim. Health Prod. 1970;2:223–234. doi: 10.1007/BF02356443. [DOI] [Google Scholar]
  • 78.Eslami A., Anwar M. Activity of fenbendazole against lung worms in naturally infected sheep. Vet. Rec. 1976;99:129. doi: 10.1136/vr.99.7.129. [DOI] [PubMed] [Google Scholar]
  • 79.Samadi A., Faizi N., Abi A.J., Irshad A.R., Hailat N. Prevalence and pathological features of ovine lungworm infection in slaughtered animals in Nangarhar Province of Afghanistan. Comp. Clin. Pathol. 2019;28:1667–1673. doi: 10.1007/s00580-019-02996-x. [DOI] [Google Scholar]
  • 80.Iqbal Z. A critical analysis of parasitic research on some domesticated animals of Pakistan. J. App. Emerg. Sci. 2004;1:1–14. doi: 10.36785/jaes.1174. [DOI] [Google Scholar]
  • 81.Ahmed S. Parasites of markhor, urial and Chiltan wild goat in Pakistan. Ann. Parasitol. 2020;66:3–12. doi: 10.17420/ap6601.232. [DOI] [PubMed] [Google Scholar]
  • 82.Girisgin O., Senlik B., Girisgin A.O., Akyol V. Studies on sheep lungworms in Bursa province of Turkey: Determination of prevalence and relationships between larval output and parasite burden in the lungs. Pak. J. Zool. 2008;40:365–369. [Google Scholar]
  • 83.Yildiz K. Prevalence of lungworm infection in sheep and cattle in the Kirikkale province. Parazitol. Derg. 2006;30:190–193. [PubMed] [Google Scholar]
  • 84.Mahmood F., Khan A., Hussain R., Anjum M. Prevalence and pathology of Dictyocaulus viviparus infection in cattle and buffaloes. J. Anim. Plant Sci. 2014;24:743–748. [Google Scholar]
  • 85.Hanks J.E., Campbell A.J., Larsen J.W. Severity and prevalence of small lungworm infection on three South Australian farms and associations with sheep carcass characteristics. Vet. Parasitol. 2021;296:109503. doi: 10.1016/j.vetpar.2021.109503. [DOI] [PubMed] [Google Scholar]
  • 86.McCarthy C., Vineer H.R., Morgan E., van Dijk J. Predicting the unpredictable? a climate-based model of the timing of peak pasture infectivity for Dictyocaulus viviparus. Vet. Parasitol. 2022;309:109770. doi: 10.1016/j.vetpar.2022.109770. [DOI] [PubMed] [Google Scholar]
  • 87.Verocai G.G., Chaudhry U.N., Lejeune M. Diagnostic methods for detecting internal parasites of livestock. Vet. Clin. N. Am. 2020;36:125–143. doi: 10.1016/j.cvfa.2019.12.003. [DOI] [PubMed] [Google Scholar]
  • 88.Ploeger H.W. Dictyocaulus viviparus: Re-emerging or never been away? Trends Parasitol. 2002;18:329–332. doi: 10.1016/S1471-4922(02)02317-6. [DOI] [PubMed] [Google Scholar]
  • 89.Claerebout E., Geldhof P. Helminth vaccines in ruminants: From development to application. Vet. Clin. N. Am. 2020;36:159–171. doi: 10.1016/j.cvfa.2019.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.McCarthy C., van Dijk J. Spatiotemporal trends in cattle lungworm disease (Dictyocaulus viviparus) in Great Britain from 1975 to 2014. Vet. Rec. 2020;186:642-642. doi: 10.1136/vr.105509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91.Forbes A. Lungworm in cattle: Treatment and control. Livest. 2018;23:102–106. doi: 10.12968/live.2018.23.3.102. [DOI] [Google Scholar]
  • 92.Charlier J., Bartley D., Sotiraki S., Martinez-Valladares M., Claerebout E., von Samson-Himmelstjerna G., Thamsborg S., Hoste H., Morgan E., Rinaldi L. Anthelmintic resistance in ruminants: Challenges and solutions. Adv. Parasitol. 2022;115:171–227. doi: 10.1016/bs.apar.2021.12.002. [DOI] [PubMed] [Google Scholar]
  • 93.Jewell N., Jones J., Mitchell S., Marsman A. Treatment failure of lungworm in cattle. Vet. Rec. 2019;185:379. doi: 10.1136/vr.l5686. [DOI] [PubMed] [Google Scholar]
  • 94.Nemati R., Bahari A., Mahmoodi P., Sazmand A. Molecular study of benzimidazole resistance in Teladorsagia circumcincta isolated from sheep in North of Iran. Iran. J. Parasitol. 2019;14:646. doi: 10.18502/ijpa.v14i4.2108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95.Sazmand A., Alipoor G., Zafari S., Zolhavarieh S.M., Alanazi A.D., Sargison N.D. Assessment of knowledge, attitudes and practices relating to parasitic diseases and anthelmintic resistance among livestock farmers in Hamedan, Iran. Front. Vet. Sci. 2020;7:584323. doi: 10.3389/fvets.2020.584323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96.Borji H. Prevalence and anthelmintic resistance in gastrointestinal nematodes of sheep in Iran: A systematic review and how overcome it; Proceedings of the 4th International and 11th National Congress in Parasitology and Parasitic Disease of Iran; Urmia, Iran. 8–10 October 2019. [Google Scholar]
  • 97.Geurden T., Smith E.R., Vercruysse J., Yazwinski T., Settje T., Nielsen M.K. World association for the advancement of veterinary parasitology (WAAVP) guideline for the evaluation of the efficacy of anthelmintics in food-producing and companion animals: General guidelines. Vet. Parasitol. 2022;304:109698. doi: 10.1016/j.vetpar.2022.109698. [DOI] [PubMed] [Google Scholar]
  • 98.Shalaby H.A. Anthelmintics resistance; how to overcome it? Iran. J. Parasitol. 2013;8:18. [PMC free article] [PubMed] [Google Scholar]
  • 99.Vercruysse J., Charlier J., Van Dijk J., Morgan E.R., Geary T., von Samson-Himmelstjerna G., Claerebout E. Control of helminth ruminant infections by 2030. Parasitology. 2018;145:1655–1664. doi: 10.1017/S003118201700227X. [DOI] [PubMed] [Google Scholar]
  • 100.Moroni B., Granados Torres J.E., López-Olvera J.R., Espinosa Cerrato J., Ráez Bravo A., Mentaberre G., Fandos P., Pazzi M., Romagnoli M., Gardini G. Ivermectin plasma concentration in Iberian ibex (Capra pyrenaica) following oral administration: A pilot study. Front. Vet. Sci. 2022;9:830157. doi: 10.3389/fvets.2022.830157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Alberti E., Gioia G., Sironi G., Zanzani S., Riccaboni P., Magrini M., Manfredi M. Elaphostrongylus cervi in a population of red deer (Cervus elaphus) and evidence of cerebrospinal nematodiasis in small ruminants in the province of Varese, Italy. J. Helminthol. 2011;85:313–318. doi: 10.1017/S0022149X10000647. [DOI] [PubMed] [Google Scholar]
  • 102.Verocai G.G. Ph.D. Thesis. University of Calgary; Calgary, Canada: 2015. Contributions to the Biodiversity and Biogeography of the Genus Varestrongylus Bhalerao, 1932 (Nematoda: Protostrongylidae), Lungworms of Ungulates, with Emphasis on a New Nearctic Species. [Google Scholar]

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