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Communication

Is Chorioptes texanus to Displace Chorioptes bovis? Notes on the Mites Causing Bovine Chorioptic Mange in Central Europe

by
Steffen Rehbein
* and
Martin Visser
Boehringer Ingelheim Vetmedica GmbH, Kathrinenhof Research Center, Walchenseestr. 8-12, 83101 Rohrdorf, Germany
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(4), 199; https://doi.org/10.3390/d16040199
Submission received: 8 March 2024 / Revised: 21 March 2024 / Accepted: 23 March 2024 / Published: 26 March 2024
(This article belongs to the Special Issue Diversity and Ecology of the Acari)
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Abstract

:
Chorioptic mange is the most common type of bovine mange in central Europe, affecting mainly housed dairy cattle. Until 1976, when Chorioptes texanus were described for the first time from mangy cattle in Brazil, bovine chorioptic mange was thought to be caused only by C. bovis mites. In Europe, C. texanus parasitism in cattle was for the first time reported in Germany in 1998. Following the repeated diagnosis of C. texanus mites in skin scrapings from local cattle in recent years, scrapings from cattle that were clinically suspicious for chorioptic mange were requested and provided during the years from 2019 to 2022 from Austria, France, Germany, and Switzerland (from 6, 17, 28, and 7 farms, respectively) and from dairy cows of 1 farm in Canada. Mites were isolated from the scrapings, cleared, and microscopically identified based on their morphology. Examination of scrapings revealed the presence of C. texanus in the cattle from 2 farms in Austria, 13 farms in France, 7 farms in Germany, 1 farm in Switzerland, and in the specimens from Canada. Chorioptes bovis mites were recovered only in scrapings from 5 farms in Germany and Psoroptes ovis mites in scrapings of cattle from 2 farms in France. The scrapings did not reveal co-infestations of C. bovis and C. texanus or of Chorioptes species and P. ovis. The records of C. texanus from Austria, France, Switzerland, and Canada constitute the first descriptions of this mite species in these countries. Although this investigation was based on an opportunistic collection of the material and was of small extent, the results suggest a widespread occurrence of C. texanus in central Europe and may emphasize the need for studies to closely investigate the nature of the causative agents of chorioptic mange in cattle and other hosts.

1. Introduction

Chorioptes mites (Acari, Psoroptidae) are obligatory, permanent ectoparasites of a wide range of domesticated and wild ungulates, but also of carnivores (ursids and stink badgers). Chorioptes species are non-burrowing mites causing chorioptic mange [1].
In cattle, chorioptic mange constitutes the most prevalent form of mange in the majority of countries in temperate regions. In contrast to bovine mange caused by infestation with Sarcoptes and Psoroptes mites, chorioptic mange is generally considered to be a less pathogenic, milder dermatitis of superficial character. The lesions are usually restricted in size and associated with the root of the tail (tail head) and the grooves on either side (caudal folds); however, they may spread towards the perineum, escutcheon, thighs, and lower legs (Figure 1), and even cases of generalization have been reported. Irritation and itching are present and may become intense, especially on palpation of the lesions. Chorioptic mange is mainly observed in milking-age cows and, although potentially present year-round under indoor-housing management systems, the condition is generally highly seasonal and most prevalent during the winter housing period. There are different opinions about the impact of chorioptic mange on cattle given the high variability in the clinical presentation and the difficulties to quantify negative effects on performance in adult animals. However, a generally higher level of restlessness, especially during the milking process, or an increase in activities to relieve pruritus associated with mange, constitute long-term stressors which reduce the well-being of the animals and can contribute to productivity losses [2,3,4,5,6,7].
The taxonomy of the genus Chorioptes has been repeatedly a matter of debate in the recent past [8,9,10]. The most recent revision concluded that there are six valid species including C. bovis (Hering, 1845) and C. texanus Hirst, 1924 which are the causative agents of chorioptic mange in bovines and other ungulates [1]. Until 1976, when C. texanus were described for the first time from mangy cattle in Brazil [11], bovine chorioptic mange was thought to be caused exclusively by C. bovis mites. In Europe, C. texanus mite parasitism on cattle was for the first time reported in 1998 from Germany [12] and later again by [10]. No other records of C. texanus from cattle have been published from Europe apart from a notice in a paper from Iceland which mentioned the observation of C. texanus on cattle from Norway [13].
Following the repeated diagnosis of C. texanus mites in scrapings from cattle kept in farms in the vicinity of our laboratory in recent years, we were interested in getting a better understanding of the nature of the agents causing bovine chorioptic mange and examined scrapings from cattle with lesions suspicious for mange collected in Germany and neighboring countries.

2. Material and Methods

2.1. Source of Material

Local practitioners, veterinarians of animal health services, veterinary parasitologists, and the Boehringer Ingelheim technical services group were asked for the submission of skin scrapings from cattle with lesions clinically suspicious for chorioptic mange (one scraping per animal, scrapings of up to five animals per farm) accompanied by information on the locations of the farms and the breeds of the cattle. In addition, the authors of a recently published paper on the behavior of cows with chorioptic mange on a dairy farm in British Columbia, Canada [5], provided skin scrapings for the speciation of the mites.

2.2. Examination of Skin Scrapings for Ectoparasites

The skin specimens were examined for ectoparasites with the standard methodology. Native examination of the material was followed by maceration in a gently heated (~70 °C) 10% potassium hydroxide solution. A dissection microscope (Leica M205C; Leica Microsystems GmbH, Wetzlar, Germany) was used for both the examination of the native scraping material and the digest and the recovery of the ectoparasites.
Identification of the isolated ectoparasites (lice and mites), including Chorioptes mites to genus, was made according to Sweatman [14] and Hiepe and Ribbeck [15]. Differentiation of the Chorioptes mites to species was based on the examination of the opisthosomal setae (setae length ratios and shape) associated with the opisthosomal lobes of adult male mites (Figure 2) using a binocular light microscope (Leica DM2500; Leica Microsystems GmbH, Wetzlar, Germany) which are the primary morphological characters used to identify Chorioptes species from ungulates [10].

3. Results

During the years from 2019 to 2022, a total of 246 skin scrapings from cattle from 58 farms in Austria, France, Germany, and Switzerland, and one scraping each from three cows from the farm in Canada, were received and examined.
The examination of the skin specimens yielded the following results:
Austria: 33 scrapings from 6 farms (3 to 5 scrapings per farm): C. texanus, 2 farms; Bovicola bovis, 2 farms; Haematopinus eurysternus, 2 farms.
France: 80 scrapings from 17 farms (2 to 5 scrapings per farm): C. texanus, 13 farms; Chorioptes spp. (no male mites isolated), 1 farm; Psoroptes ovis, 2 farms; B. bovis, 5 farms; H. eurysternus, 2 farms; Linognathus vituli, 1 farm.
Germany: 114 scrapings from 28 farms (1 to 5 scrapings per farm): C. texanus, 7 farms; C. bovis, 5 farms; B. bovis, 2 farms; H. eurysternus, 3 farms; L. vituli, 2 farms.
Switzerland: 19 scrapings from 7 farms (1 to 5 scrapings per farm): C. texanus, 1 farm.
Canada: 3 scrapings from 1 farm: C. texanus.
The examination of the scrapings did not reveal co-infestations of C. bovis and C. texanus or of Chorioptes species mites and P. ovis, or the concurrent presence of the two Chorioptes species on one and the same farm; however, lice were occasionally observed in scrapings with Chorioptes mites.
Figure 3 shows the geographic localization of the farms with C. texanus and C. bovis records in Europe. Chorioptes texanus-positive cattle were recorded on farms in Austria in the federal state of Upper Austria; in Germany in the federal states of Bavaria, North Rhine-Westphalia, Saxony, and Thuringia; in France in the regions Bretagne, Normandy, and Pays de la Loire; and in Switzerland in the Canton of Friborg.
The breeds of cattle diagnosed as C. texanus-positive in this investigation are included in Table 1 which provides a listing of the records of C. texanus in cattle worldwide.

4. Discussion

The question of which species of mites of the genus Chorioptes are the causative agents of bovine chorioptic mange in a region is of importance to help make a correct diagnosis of the parasites and to understand the epidemiology of this parasitic condition. In addition, it may have implications for the potential for cross-transmission between different host species and for the implementation of control measures.
Any interpretation of the results of the present investigation needs to consider the type of sampling and the rather limited extent, such that no conclusion can be made on the prevalence of C. texanus and C. bovis in cattle in central Europe. However, the findings indicate that C. texanus may currently be a common agent of chorioptic mange in cattle in central Europe beside C. bovis. It is not clear for how long C. texanus have been present and infesting cattle in Europe. When discussing the unexpected finding of exclusively C. texanus mites in the scrapings collected from cattle in Germany for their study, Essig et al. [8] expressed the opinion that many chorioptic mite isolates may previously have simply (“… stereotypically …”) been designated to C. bovis because no other species of Chorioptes was expected to infest cattle and to cause chorioptic mange and the mites were thus not thoroughly examined. This assumption may be kept in mind at least for more recent reports on bovine C. bovis mange which did not mention a species-level identification based on microscopy of adult male mites or did not take C. texanus as a parasite of cattle into account.
Based on records from 7 of the 16 federal states in Germany—Essig et al. [8]: Baden-Württemberg, Bavaria, Brandenburg, and Schleswig-Holstein; present study: Bavaria, North Rhine-Westphalia, Saxony, and Thuringia—a wide geographic distribution of C. texanus in the cattle population of the country can be assumed. Conversely to the work of Essig et al. [8], this investigation confirmed the presence of C. bovis in cattle in Germany with records from the federal states of Hesse, Saxony, Saxony-Anhalt, and Thuringia.
To the knowledge of the authors, the findings of C. texanus on cattle from Austria, France, Switzerland, and Canada constitute the first descriptions of this species in these countries and add to the number of countries with records of C. texanus as a causative agent of bovine chorioptic mange (Table 1). Although expected to occur on cattle in the UK [37], there are no surveys which have confirmed the presence of C. texanus in the UK (R. Wall, in litt., 15 February 2021).
The examination of skin scrapings in the present investigation did not identify cases of mixed infestation with C. texanus and C. bovis on the same animal. However, co-infestation with both species of mites in cattle has been reported several times from Japan [29,30,31,32].
The range of breeds of cattle from which C. texanus were isolated indicates that various cattle breeds are susceptible to the infestation (Table 1). The apparent predominance of Holstein-Friesian cattle likely reflects that this breed represents the most important dairy breed worldwide and that Holstein-Friesian cattle are subject to extensive international trade.
Chorioptes texanus, which was described in 1924 based on mites collected from a domestic goat in Texas, USA, were recognized on cattle for the first time in a brief report from Brazil in 1976 [11]. However, mites collected from cattle in Israel and Japan in 1960 and 1972, respectively, and originally assigned to be C. bovis, were identified as C. texanus upon re-examination [25,38]. Since the report of C. texanus on cattle in Brazil from 1976, C. texanus have been reported as the causative agent of bovine chorioptic mange several times in various countries in Asia, Europe, and the Americas (Table 1). Based on unpublished observations by the US Department of Agriculture, it was assumed that “C. texanus may now be the prevalent Chorioptes species on cattle in the USA” [36]. In Japan, where C. texanus on cattle were first reported in 1991 [26,39], studies conducted since then have shown that, although both C. bovis and C. texanus are present in the cattle population, infestation with C. texanus is more frequently observed in the more recent studies [31].
No difference in the clinical consequence of the infestation of cattle with C. bovis or C. texanus is expected [37]. In addition, controlled studies conducted worldwide to evaluate the efficacy of the pour-on administration of ivermectin and eprinomectin products in cattle with chorioptic mange consistently demonstrated a high efficacy of the products and did not indicate any difference in the response to the treatments between C. bovis and C. texanus [2,4,29,34,40,41,42].
Apart from causing mange in cattle, C. texanus mites have been identified as parasites of goats in Texas, USA [43,44], Java, Indonesia [45]; putatively, as per Hirst [44] and von Maydell [46]), Malaysia [47], and India [48]; of sheep in Brazil [49]; and of Formosan serows (Capricornis swinhoei) from Taiwan [50]. Interestingly, all records of C. texanus in non-bovine hosts were exclusively made in warmer climate regions while C. texanus infestation of cattle was reported from both regions with warmer climate (Brazil; Israel; southern China; South Korea; southern prefectures of Japan) and temperate regions (British Columbia, Canada; Wisconsin, USA; Austria; France; Germany; Switzerland; Norway; Moscow region, Russia; Hokkaido and Yamagata prefectures, Japan) (Table 1).
In Canada, mites isolated from the ears of semi-domesticated reindeer (Rangifer tarandus) have been described as C. texanus in the past [14]. However, recently conducted studies of mites collected from the outer ear canal of moose (Alces alces) from Scandinavia and Russia concluded that the mites described as C. texanus by Sweatman [14] were most likely mites of the newly described species C. sweatmani Bochkov, Klimov, Hestvik and Saveljev, 2014, which is closely related to C. texanus [1,10,51]. In this context, it is worth mentioning that, similarly, mites isolated from the body surface of clinically unsuspicious wild cervids (moose; fallow deer [Dama dama]; sika deer [Cervus nippon]) in Poland and described as C. texanus [52,53,54,55,56] were discussed as potentially representing C. sweatmani [1].
Although conducted on an opportunistic basis and of small extent, the work presented here provides the most up-to-date information on C. texanus and C. bovis occurrence in Germany and reports the first records of the species C. texanus in cattle from Austria, Canada, France, and Switzerland. The results of this work suggest a widespread occurrence of C. texanus in central Europe and put the role of C. bovis, which was thought to be the prevalent agent of bovine chorioptic mange in the past, in question. Further studies on the causative agents of bovine chorioptic mange in Europe, on the potential role of C. texanus as a parasite of sheep and goats, as well as on the host specificity of the species, are desired.

Author Contributions

Conceptualization, resources, supervision, writing, S.R.; Investigation, formal analysis, writing—review, M.V. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Ethics approval not applicable.

Data Availability Statement

All relevant data are presented in the paper.

Acknowledgments

The authors acknowledge the support of A. Ahrens, Thüringer Tierseuchenkasse, Jena, Germany; A. Brune and G. Sabatini, Boehringer Ingelheim Vetmedica GmbH, Ingelheim, Germany; P. Kukla, Boehringer Ingelheim RCV GmbH&Co KG, Animal Health, Vienna, Austria; J.-M. Le Mer, Boehringer Ingelheim Animal Health, Lyon, France; K. Pfister, Bern, Switzerland; M.G. Wagener, University of Veterinary Medicine Hannover, Germany; and A.C. Moncada, J. Lee, and D. Weary, University of British Columbia, Vancouver, Canada, during the collection of skin scrapings, and S. Mayr in the examination of the samples. The authors thank B.K. Gjerde for the information on the finding of C. texanus in Norway and M. Heddergott for creating Figure 1. Special thanks are due to T. Nagata, G. Kinoshita, and A. Kusanagi for their help in accessing publications from Japan and their translation.

Conflicts of Interest

Authors S.R. and M.V. were employed by the company Boehringer Ingelheim Vetmedica GmbH. The research reported here was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Figure 1. Chorioptic mange lesions associated with the grooves (caudal folds) on the sides of the root of the tail (left picture) or the escutcheon and thighs (right picture) of dairy cows.
Figure 1. Chorioptic mange lesions associated with the grooves (caudal folds) on the sides of the root of the tail (left picture) or the escutcheon and thighs (right picture) of dairy cows.
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Figure 2. Chorioptes bovis (left picture) and C. texanus (right picture) male mites (ventral view).
Figure 2. Chorioptes bovis (left picture) and C. texanus (right picture) male mites (ventral view).
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Figure 3. Localization of the farms with cattle testing positive for Chorioptes texanus (red dots) and C. bovis (yellow dots) in Austria, France, Germany, and Switzerland.
Figure 3. Localization of the farms with cattle testing positive for Chorioptes texanus (red dots) and C. bovis (yellow dots) in Austria, France, Germany, and Switzerland.
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Table 1. Countries of record and breeds of cattle infested with Chorioptes texanus.
Table 1. Countries of record and breeds of cattle infested with Chorioptes texanus.
CountryBreeds of Cattle Diagnosed
Chorioptes texanus-Infested		Reference(s)
AustriaHolstein-Friesian 1, (Austrian) SimmentalThis study
FranceHolstein-Friesian, NormandeThis study
GermanyNo information provided[8,10,12]
Holstein-Friesian, (German) SimmentalThis study
NorwayNorwegian Red[13], B.K. Gjerde (in litt., 07 and 24 January 2022) 2
RussiaHolstein-Friesian[16]
SwitzerlandBrown SwissThis study
ChinaHolstein-Friesian, Montbeliarde, Simmental, Chinese native cattle[17,18]
No information provided[19,20]
IsraelHolstein-Friesian, Charolais[21,22,23,24,25]
JapanHolstein-Friesian, Japanese black[4,26,27,28,29,30,31,32]
South KoreaHolstein-Friesian[33,34]
BrazilHolstein-Friesian, Zebu cattle[11,35]
CanadaHolstein-FriesianThis study
USANo information provided[1,8,12,36]
1 ‘Holstein-Friesian’ refers to the most widespread breed type of dairy cattle in the world, often referred to as Holstein or Friesian only or ‘Black-pied’. 2 Chorioptes texanus were identified in Norway in 2001 from “in all likelihood … dairy cows of the Norwegian Red breed”; identification was based on the morphology of adult male mites (opisthosomal lobes and setae).
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Rehbein, S.; Visser, M. Is Chorioptes texanus to Displace Chorioptes bovis? Notes on the Mites Causing Bovine Chorioptic Mange in Central Europe. Diversity 2024, 16, 199. https://doi.org/10.3390/d16040199

AMA Style

Rehbein S, Visser M. Is Chorioptes texanus to Displace Chorioptes bovis? Notes on the Mites Causing Bovine Chorioptic Mange in Central Europe. Diversity. 2024; 16(4):199. https://doi.org/10.3390/d16040199

Chicago/Turabian Style

Rehbein, Steffen, and Martin Visser. 2024. "Is Chorioptes texanus to Displace Chorioptes bovis? Notes on the Mites Causing Bovine Chorioptic Mange in Central Europe" Diversity 16, no. 4: 199. https://doi.org/10.3390/d16040199

APA Style

Rehbein, S., & Visser, M. (2024). Is Chorioptes texanus to Displace Chorioptes bovis? Notes on the Mites Causing Bovine Chorioptic Mange in Central Europe. Diversity, 16(4), 199. https://doi.org/10.3390/d16040199

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