Gastrointestinal parasites in an isolated Norwegian population of wild red deer (Cervus elaphus)

Rebecca K Davidson
Susan J Kutz
Knut Madslien
Eric Hoberg
Kjell Handeland
Gastrointestinal parasites in an isolated Norwegian population of wild red deer (Cervus elaphus)
R E S E A R C H Open Access
Background: Thirteen red deer (Cervus elaphus), culled from the isolated population at the Mongstad Oil Refinery, Norway, were investigated for gastrointestinal helminths. These animals, enclosed by the refinery fence, do not have contact with other ruminants and have a high population density considering the available browsing area (1 km 2 ) within the refinery site (3 km 2 ). The population was estimated to be 110-130 at the time of culling. Results: The helminth fauna among these sampled red deer was enumerated and species were identified based on morphology. Ostertagia leptospicularis/O. kolchida was detected in 83% [CI 55 -95%], Spiculopteragia spiculoptera/S. mathevossiani in 92% [CI 65 -99%] and Trichostrongylus axei in 42%, [CI 19 -68%] of the abomasa examined. Characterisation of the intestinal parasite fauna revealed Capillaria bovis, Cooperia oncophora, Oesophagostomum venulosum, Trichuris globulosa and tapeworm fragments (presumed anoplocephalids) in seven individuals. Only one calf had an infection with more than one intestinal helminth (tapeworm fragment and Trichuris globulosa). The remaining six deer had single species intestinal infections. No significant age related trends were seen, with the exception of higher intensity of infection of T. axei in yearlings relative to other age classes. Assessment of abomasal parasite burden and body condition revealed no significant trends. In calves, statistically non-significant correlation was seen between increased parasite burden and decreased slaughter weight, whilst the opposite was seen in adults with the heaviest adults exhibiting the higher burdens. Given the small sample size the trends that were seen need further investigation. The parasite burden was aggregated with three adult red deer harbouring 75% of the total abomasal parasite count.Conclusion: This isolated population was parasitised by a reduced subset of gastrointestinal nematodes typical of this cervid across an extensive geographic range in Eurasia. The intensity and abundance of abomasal nematodes was higher in this isolated population than reported in similar studies of red deer populations across Europe.

Background

Four species of wild cervids are found in Norway: red deer (Cervus elaphus atlanticus), moose (Alces alces), roe deer (Capreolus capreolus) and wild reindeer (Rangifer tarandus tarandus). Populations of red deer are primarily found in coastal areas of West and Central Norway, roe deer in East and Central Norway, whereas moose are common in all parts of the country except for West Norway [1,2]. Wild reindeer live in 23 sub-populations in the alpine regions of southern Norway and constitute one of the last populations of wild free-ranging tundra reindeer in Europe, and, therefore, are of great conservation interest. During the past few decades there has been substantial increase in populations of red deer [1,3] coincidental with geographic expansion to the east-and southwards such that these cervids are now present across all municipalities of South and Central Norway. Red deer are also increasingly seen in the wild reindeer areas during summer.

Generally parasite burdens are predicted to increase with density among deer populations [4] and may negatively influence the health status of the animals [5][6][7]. Increased intensity of parasite infections might, in addition to diminished food resources for hosts, be a contributing factor to the reductions in slaughter weights observed among some of the densely populated red deer areas during the recent years [2]. There is also a concern that the parasite fauna of red deer can be transmitted to sympatric domestic ruminants, such as cattle and sheep as well as other cervid species. There is further concern regarding the potential for parasite transmission from red deer into wild reindeer populations that are also challenged by climate change and environmental constraints. A prerequisite to monitoring the influence of climate change on cervid species and their parasites, as well as detection of host switching events, is development of baseline data on diversity, especially faunal structure for gastrointestinal and abomasal nematodes, among wild red deer from Norway.

Knowledge regarding biodiversity of gastrointestinal nematodes in wild red deer populations from Fennoscandia is lacking. The sole exception is a Norwegian student thesis [8], describing the gastrointestinal fauna in 25 animals taken by hunters from two municipalities in West Norway in 2005. Although the municipalities studied, Suldal and Tingvoll (Figure 1), are important areas for red deer, considerable numbers of sheep and cattle are also grazed during the summer. Thus, parasite transmission from domestic ruminants may have influenced patterns of helminth diversity. In this regard, red deer were commonly infected with species of Ostertagiinae, although identifications were incomplete, in addition to a broader assemblage of helminths known to occur in other wild cervids and domestic ruminants (Table 1). Parasitological surveys of red deer in continental European countries also identify Ostertagiinae as the predominant components of the abomasal fauna, usually including multiple polymorphic species of Ostertagia, Spiculopteragia and possibly Teladorsagia [9][10][11][12][13]. Polymorphism among males of single species (two or exceptionally three discrete male morphotypes) within this group of parasites has resulted in some inconsistency in reports that document diversity of nematode parasites in ungulates [5,14]. Minor morphs have frequently been reported as discrete species in some studies leading to confusion about host associations and geographic range for some species. Consequently, recognition of polymorphic species and correct morphological and taxonomic identification is vital to provide an accurate picture of diversity [12,15]. Establishing baselines including greater knowledge of the gastrointestinal helminth fauna and accurate species identification of abomasal ostertagiines in red deer is needed to address the potential for cross transmission of parasites among freeranging and domestic ungulates and can incorporate parasites into management decisions for wild cervid species in Norway.

The aim of this study was to characterise the gastrointestinal helminth fauna of wild red deer from a dense isolated wild population in an area that for decades has had no other ruminants present, neither domestic nor wild. Also, as a component of diversity, the intensity of infection for helminth parasites was investigated and compared to host body condition, age, and slaughter weight.

Methods

Study population and habitat

Mongstad Oil Refinery, owned by Statoil, is situated in coastal western Norway, about 50 km north of Bergen ( Figure 1). The refinery was established in the early 1970s and harbours a population of free-ranging red deer. Today, the total fenced area at the refinery is about three square kilometres, but roughly one square kilometre of this area is suitable grazing for deer (grassland, bogs or forest, Figure 1). The population size was estimated to be between 110 and 130 individuals in December 2006, giving a minimum estimated population density of 37 -43 red deer/km 2 before culling.

This red deer population is generally considered stationary, due to being enclosed by fencing surrounding the refinery complex. However, single tagged red deer have been registered to leave and return, since there is access to the area via the sea (Figure 1). In 2006, the landowners decided that a cull was necessary to reduce the large population size. Forty-two red deer were culled between February 6 th and February 10 th 2007, comprising of 14 calves, eight sub-adults and 20 adults. Due to logistical limitations, only 13 animals (three females and ten males) were available for examination. The gastrointestinal tract from each animal was removed and ligated at the time of culling. The tracts were subsequently frozen at -20°C until further analysis could be carried out. The age, sex, body condition and slaughter weight of the animal were recorded. The body condition was assessed based on visible fat reserves subcutaneously and around the heart and kidneys, as good, average, or poor [16].

Gastrointestinal investigation

Gastrointestinal tracts were thawed at room temperature and then separated into their component regions: abomasum; small intestine; caecum and large intestine. Each component was placed in its own individual 10 l bucket. The abomasum was opened along the greater curvature, the contents emptied into the bucket and the mucous membrane of the abomasum washed thoroughly with cold tap water (≥2 l). The bucket was allowed to sediment for at least thirty minutes before the supernatant was removed to the 2 l level. The remaining 2 l of fluid and sediment were thoroughly mixed prior to removing two 50 ml subsamples for carrying out parasite counts and identification. Abomasal samples were taken from 12 of the 13 culled animals whilst all 13 had their remaining intestinal tracts investigated. The small intestine was visually divided into thirds and the posterior third was removed and discarded. The intestinal contents of the anterior two thirds were flushed into a bucket. The intestine was clipped open longitudinally and the surface of the mucus membrane stripped by placing a finger and thumb to either side of the intestine and pulling the intestine through. Once again the bucket was allowed to stand for at least thirty minutes to sediment. The supernatant was discarded to the 2 l mark. The remaining 2 l of fluid and sediment were thoroughly mixed prior to removing two 50 ml sub-samples for carrying out parasite counts and identification. A minimum 20 g faecal sample was removed from the rectal end of the large intestine and then the intestinal region containing pelleted faeces was removed and discarded. The remaining large intestine and caecum were emptied into a bucket and flushed thoroughly. Both were clipped open and using a finger and thumb together with cold water the mucus membrane was rinsed. The bucket was allowed to sediment for at least an hour before the supernatant was removed to the 3 l level. The remaining 3 l of fluid and sediment were thoroughly mixed prior to removing one 1 l sub-sample for carrying out parasite counts and identification. All the sub-samples were re-frozen at -20°C until further analysis could be carried out. Abomasal digestion to look for arrested larvae was not carried out.

Nematode count and identification

Parasite counts were done on one 50 ml aliquot from the abomasum (2.5% of abomasal content), one 50 ml aliquot from the small intestine (2.5% of total content) and investigation of 1 l of large intestinal content (33% of total content). The 50 ml fluid was homogenised and a 10 ml subsample transferred to a square line-marked petridish. This was examined under a stereomicroscope at 16x magnification and any nematodes seen were carefully transferred to a sample glass containing 70% ethanol until further analysis could be carried out. This was repeated until the entire 50 ml volume had been examined. The large intestinal contents were first sieved through a 420 μm mesh to remove the largest particles. The fluid was then examined and any parasites seen placed in 70% ethanol in a sample glass. The abomasal and small intestinal nematode counts were multiplied by 40 to obtain a total parasite count. The large intestinal count was multiplied by three to obtain the total count.

Species identification was based on male nematode morphology [14,15,[17][18][19][20] after mounting in polyvinyl lactophenol (Chemi-Teknikk AS, Oslo, Norway) for two to five minutes. Polymorphism in the Ostertagiinae was accounted for with major and minor morphs recorded separately; counts of major and minor morphotypes representing single species were combined for analysis purposes. A few female parasites were also identified to species level, however degradation of specimens during prolonged storage and repeated freezing and thawing meant that the synlophe and other diagnostic attributes [15] could not be reliably examined for this subset of nematodes. Records reported are validated by representative voucher specimens for helminths collected from red deer in the current study that have been deposited in the US National Parasite Collection, USDA, Agricultural Research Service, Beltsville, Maryland, USA.

Statistical analyses

JMP statistical software (SAS institute, version 9.0.0) was used to generate and examine summary statistics in the dataset and a significance level of p < 0.05 was selected. Summary statistics were compared among the age groups, body condition and slaughter weight. The 95% confidence interval (CI) was calculated to compare means. The prevalence of the abomasal nematodes in the study population was calculated as well as the proportion of major and minor morphs of each species in addition to the proportion of males to females. Advanced statistical modelling was not carried out given the small size of the dataset.

Results

The sex of the animals was biased towards males with only three females examined. It was, therefore, not possible to analyse host gender differences in parasitic burden and diversity. The age distribution was five calves, three yearlings and five adults with mean slaughter weight of 22.9 kg, 34.3 kg and 65.3 kg respectively. Assessment of body condition (fat reserves) at slaughter showed that ten animals had average body condition, whilst three had poor body condition: two below average (one calf and one adult) and one emaciated (a yearling).

Abomasal parasites

Total abomasal counts are shown in Table 2. Species of Ostertagia, Spiculopteragia and Trichostrongylus axei were detected. Ostertagiines were detected in 83% [CI 55 -95%] of the deer, all of the positive animals had O. leptospicularis whilst four also had the minor morph O. kolchida. Spiculopteragia spiculoptera (also known as S. boehmi according to Drózdz [14]) was detected in 92% [CI 65 -99%] of the animals and two of the positive animals also had the minor morph S. mathevossiani. T. axei was detected in 42%, [CI 19 -68%] of the deer. Aggregation of the parasites was seen with adult hosts harbouring 86% of the total abomasal parasite burden whilst yearlings harboured 8% and calves 6%. Three adult individuals (two males and a female) harboured 75% of the total abomasal parasite burden estimated in this population. The five adult deer examined had significantly higher infection intensities than the five calves, whilst the two yearlings had a lower mean count than adults, although the confidence interval overlapped with that for both calves and adults.

Comparison of body condition estimate and parasite counts showed that two of the three animals with poor body condition, a calf and a yearling, had abomasal parasite counts of 640 and 4 680 respectively whilst the third, an adult, had a count of 18 360 abomasal nematodes. Comparison of the total abomasal parasite burden and slaughter weight by age showed a statistically nonsignificant trend of decreasing slaughter weight with increasing parasite burden in calves whilst the opposite was true in adults with increasing slaughter weight with increasing parasite burden. However this is based on just five individuals in each age class.

There was a preponderance of female abomasal nematodes compared to male but given that females were not identified we were unable to differentiate counts of the three species detected. The mean ratio of male to female in the complete abomasal parasite count was 1:2.7 (95% CI 1.61 -3.82). The intensity of infection for male abomasal nematodes (S. spiculoptera/S. mathevossiani; O. leptospicularis/O. kolchida), showed no significant differences relative to age of the host with the exception of T. axei which was found at significantly higher intensities in yearlings than in the other two age groups. However with only five of 12 individuals infected with this parasite these findings need further investigation. The relative abundance of the three species of abomasal nematodes varied (Table 3). On the whole, the most abundant species was S. spiculoptera/S. mathevossiani, followed by O. leptospicularis/O. kolchida and the least abundant was T. axei. The proportion of major morphs of both Spiculopteragia and Ostertagia were significantly higher than minor morphs.

Small and large intestinal parasites

Capillaria bovis, Cooperia oncophora, O. venulosum, Trichuris globulosa and tapeworm fragments (presumed anolpocephalids, possibly a species of Moniezia, or Avitellina) were recorded in the small intestine of seven individuals (Table 2). Only one of the deer, a calf, had more than one intestinal parasite species with a co-infection of T. globulosa and tapeworm fragments.

Discussion

Red deer from within the enclosure around the Mongstad oil refinery, in 2007, had significantly higher abomasal parasite burdens than free-ranging red deer examined in 2005 from the regions of Tingvoll and Suldal [8]. Further, intensity and abundance exceeded the values reported in similar studies of other red deer populations from localities across Europe [9][10][11][12]. High levels of infection in this confined Norwegian population are notable, given that the study was carried out in February in contrast to the traditional hunting season in autumn when parasite burdens would in general be predicted to be higher than those observed during mid-winter [13,21].

A significant difference in abomasal parasite burden was seen between the age classes where greater burdens were associated with increasing age of hosts. Andrews [22] suggested that abomasal nematode loads exceeding 8 000 can be pathogenic and the mean abomasal parasite count in adults in the stationary study population (n = 5) exceeded 12 000. Intensity of infection in our study exceeded levels reported from other, more southern, regions of Europe where red deer have been examined for parasites. Additionally, the prevalence of abomasal parasites in these European studies varied depending on the season, the age class of the host and the parasite species investigated; mean prevalence for the population as a whole generally exceeded 90%. A similarly high prevalence level was seen in the present study indicating that Ostertagiinae remain the most commonly observed gastrointestinal helminths in wild cervidae. The increase in mean abomasal parasite intensity in adults compared to yearlings and calves might be an indication that acquired immunity does not develop with some infections involving species of Ostertagiinae, although improved definition of the adults' age by year could reveal a more nuanced picture. The exception was T. axei, which was recorded at highest levels in the yearlings. Further investigation is needed as to what extent this is a reflection of the high infection pressure in a dense isolated population overcoming partial immunity and to what extent it reflects a lack of immunological stimulation by the parasites. Two of the three species of abomasal nematodes identified, S. spiculoptera/S. mathevossiani and O. leptospicularis/O. kolchida, dominated the parasitic picture in the present study with the former being predominant even though both are considered to be characteristic parasites of cervids [12,23]. The more generalist parasite of domestic and wild ruminants, T. axei was found at a much lower prevalence in this study population but highlights the fact that wild cervids can act as reservoirs for parasites of relevance to domestic ruminants. The abomasal parasites in red deer from Suldal and Tingvoll were, for the most part, only identified to family level and not species [8]. Investigation of the small and large intestinal species diversity showed no significant differences between the two studies with the majority of the animals in both populations harbouring single species infections even though a number of animals in the study by Bakka et al. [8] had up to four concurrent species. Neither of the studies was able to address the reasons for differences in species richness although consideration should be given to cross-infection with cattle and sheep since the population described by Bakka et al. [8] shared grazing with domestic ruminants whilst the population in the present study was isolated. For example, this may account for the occurrence of Nematodirus battus, N. filicollis and Teladorsagia circumcincta at Suldal and Tingvoll which are primary helminths of domestic sheep. There were no significant differences in the total parasite count for the small intestine between the two studies although a trend of higher counts was seen in red deer in this study.

Approximately 45 species of gastrointestinal helminths are known in red deer across an extensive range in Eurasia [23]. Diversity reflects the extensive geographic distribution for this cervid in the Palearctic, interactions among sympatric assemblages of freeranging cervids, and other ungulates and local or landscape effects related to climate [5,24]. Helminths identified in the current study and the survey reported by Bakka et al. [8], are a subset of this broader faunal diversity, and there are no new host records documented. In this case, absence of some parasites may indicate environmental limitations on development posed by colder climates characteristic of southern Norway and founder effects on diversity linked to ongoing geographic expansion for red deer, in addition to potential sampling biases. In this regard, and perhaps unexpected, was the complete absence of Nematodirine nematodes at the Mongstad Refinery site, including species of Nematodirus, which otherwise are a prominent component of cervid parasite faunas across the Palearctic [23].

Little has been done to explore the gastrointestinal helminth fauna among other wild cervids from Norway, except for one study on abomasal nematodes in wild reindeer [25]. In wild reindeer six different abomasal nematode species were found with Ostertagia gruehneri/ O. arctica being dominant. The only abomasal nematode reported in wild reindeer shared by red deer in the present study was T. axei. However, S. spiculoptera has been identified in captive reindeer co-grazed with elk (Cervus canadensis) in North America and may be a Table 3 The different proportions of the three species of abomasal nematodes identified in the abomasal contents of the red deer (Cervus elaphus) from Mongstad (n = 12), based upon morphological identification of all the male nematodes in each sample significant pathogen in this species [26]. Further studies of mixed cervid populations are needed, to understand if the gastrointestinal parasites found in red deer in the present study may establish (or are already shared) by other cervids species in Norway, and more broadly in Fennoscandia [12]. The need for detailed comparative baselines, linked to archived and identified specimens in museum repositories, is indicated by the effects of accelerating climate change and environmental disruption which are influencing the distributions of cervids and other ungulates as hosts, their parasites, and patterns of disease [27].

Conclusions

The present study was carried out in an isolated wild population of red deer occurring within the core geographic range for this cervid in Norway. Although our sample population was relatively small, results for diversity are expected to be representative for helminth species richness for red deer in this region in the northern extent of the range for Cervus elaphus. The intensity and abundance of abomasal nematodes was higher in this isolated population than reported in similar studies of red deer populations across Europe. The species of gastrointestinal helminths recorded were a reduced subset of gastrointestinal nematodes typical of this cervid across an extensive geographic range in Eurasia.

Figure 1
1Map (a) of the Mongstad area with inset of a map of Norway showing Mongstad (red square) as well as Tingvoll and Suldal (black circles); images (b and c) of the area grazed by the red deer, that is enclosed on three sides by a fence and on the fourth by the sea; red deer post-mortem examination in the field (d), with a backdrop of the industrial complex.

Table 1
1Summary of the results from a gastrointestinal helminth survey in wild red deer (Cervus elaphus) in Norway by Bakka et al.[8] showing the prevalence and parasite counts, including the 95% confidence interval (CI), as well as species identifiedBakka et al. [8]
N
Prevalence [95%CI] Mean counts [95% CI] Min-Max (median) Species detected (No. of individuals
with each parasite species)

Abomasal parasites
25 84% [65-94]
820 [523-1116]
0-2300 (700)
Osteragia sp. (6)*: Ostertagia leptospicularis
(4) and Ostertagia circumcincta (1)

Spiculopteragia sp. (15)

Small intestinal parasites 25 16% [6-35]
21 [-1-42]
0-200 (0)
Nematodirus sp. (4)*: Nematodirus battus
(2) and N. filicollis (1)

Capillaria sp. (1)

Moniezia sp. (3)

Large intestinal parasites 25 72% [52-86]
6 [3-9]
0-20 (3)
Trichuris sp. (5)

Oesphagostomum venulosum (14)

Chabertia sp. (1)

*Not identified beyond family level.

Table 2
2Gastrointestinal helminths in 13 red deer (Cervus elaphus) culled from a stationary population around the Mongstad Oil Refinery, Norway, in February 2007N
Prevalence [95%CI]
Mean counts [95% CI]
Min-Max (median)
Species detected a (No. of individuals
with each parasite species)

Abomasal parasites
12
91.7% [64.6-98.5]
6223 [1262-11185]
0-20480 (1840)
Ostertagia leptospicularis (10)/O.
kolchida (4)

Spiculopteragia spiculoptera (11)/S.
mathevossiani (2)

Trichostrongylus axei (5)

Small intestinal parasites
13
38.5% [17.7-64.4]
40 [-8-88]
0-280 (0)
Capillaria bovis (2)

Tapeworm fragments (1)

Large intestinal parasites
13
30.8% [12.7-57.6]
1 [0-2]
0-6 (0)
Cooperia oncophora (2)

Trichuris globulosa (2)

Oesphagostomum venulosum (2)

a

Voucher specimens for helminths deposited in the US National Parasite Collection, USDA, Agricultural Research Service, Beltsville, Maryland, USA: Trichuris
globulosa USNPC 105314; Anoplocephalidae (unidentified cestodes) USNPC 105315; Spiculopteragia boehmi (syn. S. spiculoptera) USNPC 105316, 105319, 105323;
Ostertagia leptospicularis/O. kolchida USNPC 105317, 105320, 105324; Capillaria bovis USNPC 105318; Trichostrongylus axei USNPC 105321; Cooperia oncophora
USNPC 105322.

Parasite speciesMean proportion of the different species (males only) [95% CI for the mean]Mean proportion of major morphs [95% CI for the mean]The 95% confidence interval (CI) for the mean proportions are shown.Spiculopteragia spiculoptera/mathevossiani
64.5 [43.0-86.0]
93.4 [80.0-100.0]

Ostertagia leptospicularis/kolchida
26.4 [9.3-43.4]
71.9 [45.0-98.9]

Trichostrongylus axei
9.2 [-2.8-20.7]
Not applicable

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AcknowledgmentsWe thank Arthur Abrams and Patricia Pilitt at the US National Parasite Collection, USDA, Beltsville, Maryland, for assistance in preparing nematodes for examination and identification. We also thank Bjørnar Ytrehus and Anja Gahr Langangen, at the Norwegian Veterinary Institute, for their respective help with the field work and with the gastrointestinal washes and counting. We would also like to thank Statoil Mongstad for granting us access to this red deer population. This study was financed by the Norwegian Veterinary Institute as part of the Health Surveillance Program for Wild Cervids.Ethical ApprovalThe animals included in this study were part of larger group that were being culled to reduce population levels. Austrheim Municipality authorised this extraordinary cull, at a meeting on 30/11/2006 (Reference number 109/06, Archive number 06/748), because of anticipated animal welfare issues, given the very high red deer population density and limited nutritional resources at the site. Further ethical approval for samplingwas not applied for since the animals were not being culled to participate in the study, rather the researchers took advantage of animals that had been culled to investigate parasitic burdens. The sampling was carried out under the auspices of the Cervid Health Surveillance Program (HOP).Competing interestsThe authors declare that they have no competing interests.Authors' contributions RKD carried out parasite isolation, species identification and performed data analysis, SK helped with parasite identification, KM carried out the field work, EH carried out parasite identification, and KH conceived the study. All authors contributed to drafting the manuscript and have read and approved the final manuscript.Submit your next manuscript to BioMed
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J Drózdz, Polymorphism in the Ostertaginae Lopez-Neyra, 1947 and comments on the systematics of these nematodes. 32Drózdz J: Polymorphism in the Ostertaginae Lopez-Neyra, 1947 and comments on the systematics of these nematodes. Syst Parasitol 1995, 32:91-95.

The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North American: an update and a key to species. J R Lichtenfels, E P Hoberg, Vet Parasitol. 46Lichtenfels JR, Hoberg EP: The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North American: an update and a key to species. Vet Parasitol 1993, 46:33-53.

A field technique for evaluating physical condition of deer. T P Kistner, C E Trainer, N A Hartmann, Wildlife Soc B. 8Kistner TP, Trainer CE, Hartmann NA: A field technique for evaluating physical condition of deer. Wildlife Soc B 1980, 8:11-17.

Two new nematode species for Turkey helmint fauna in roe deer (Capreolus capreolus), Spiculopteragia spiculoptera (Guschanskia, 1931) and minor morph S. (Rinadia) mathevossiani (Ruchliadev, 1948). S Umur, A T Gürler, Y E Beyhan, C S Bölükbaş, M Açici, 17Kafkas Univ Vet Fak DergUmur S, Gürler AT, Beyhan YE, Bölükbaş CS, Açici M: Two new nematode species for Turkey helmint fauna in roe deer (Capreolus capreolus), Spiculopteragia spiculoptera (Guschanskia, 1931) and minor morph S. (Rinadia) mathevossiani (Ruchliadev, 1948). Kafkas Univ Vet Fak Derg 2011, 17:649-654.

Studies on helminths in helminthiases in Cervidae. I. Revision of the subfamily Ostergaiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. J Drózdz, Acta Parasitol Pol. Drózdz J: Studies on helminths in helminthiases in Cervidae. I. Revision of the subfamily Ostergaiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. Acta Parasitol Pol 1965, XII:445-481.

Comparative morphology of Ostertagia mossi and Ostertagia dikmansi (Trichostrongylidae) from Odocoileus virginianus and comments on other Ostertagia spp. from the Cervidae. E P Hoberg, J R Lichtenfels, P A Pilitt, Syst Parasitol. 24Hoberg EP, Lichtenfels JR, Pilitt PA: Comparative morphology of Ostertagia mossi and Ostertagia dikmansi (Trichostrongylidae) from Odocoileus virginianus and comments on other Ostertagia spp. from the Cervidae. Syst Parasitol 1993, 24:111-127.

First report of two polymorphic species of Ostertagia (Nematoda: Trichistrongylidae) in Cervus elaphus in Spain: O. leptospicularis and O. kolchida. J M Ortiz, M Goyen, F Alonso, Res Rev Parasitol. 56Ortiz JM, Goyen M, Alonso F: First report of two polymorphic species of Ostertagia (Nematoda: Trichistrongylidae) in Cervus elaphus in Spain: O. leptospicularis and O. kolchida. Res Rev Parasitol 1996, 56:221-223.

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The arthropod and helminth parasites of red deer (Cervus elaphus L) in New Zealand. Jrh Andrews, Trans R Soc NZ (Zool). 5Andrews JRH: The arthropod and helminth parasites of red deer (Cervus elaphus L) in New Zealand. Trans R Soc NZ (Zool) 1964, 5:97-127.

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Gastrointestinal parasites in an isolated Norwegian population of wild red deer (Cervus elaphus). E P Hoberg, S J Kutz, J A Cook, K Galaktionov, V Haukisalmi, H Henttonen, S Laaksonen, A Makarikov, Dj ; Marcogliese, Davidson, Arctic Biodiversity Assessment: Status and Trends in Arctic Biodiversity. Meltofte H. AkureyiParasites201359Iceland: Conservation of Arctic Flora and FaunaHoberg EP, Kutz SJ, Cook JA, Galaktionov K, Haukisalmi V, Henttonen H, Laaksonen S, Makarikov A, Marcogliese DJ: Parasites. In Arctic Biodiversity Assessment: Status and Trends in Arctic Biodiversity. Edited by Meltofte H. Akureyi, Iceland: Conservation of Arctic Flora and Fauna; 2013:529-557. doi:10.1186/s13028-014-0059-x Cite this article as: Davidson et al.: Gastrointestinal parasites in an isolated Norwegian population of wild red deer (Cervus elaphus). Acta Veterinaria Scandinavica 2014 56:59.


A man with an infected finger: a case report

Pieter J Gathier
Titus Ja Schönberger
A man with an infected finger: a case report
10.1186/s13256-015-0589-5C A S E R E P O R T Open Access
Introduction: Whitlow is an infection of a finger or around the fingernails, generally caused by bacterium. However, in rare cases, it may also be caused by the herpes simplex virus. As herpetic whitlow is not seen often, it may go under-recognised or be mistaken for a different kind of infection of the finger. Delayed recognition and/or treatment puts patients at risk of complications ranging from superinfection to herpetic encephalitis. Case presentation: A 23-year-old Caucasian man with no medical history was referred by his primary care physician because of erythema and swelling of the little finger of his left hand. The primary care physician had already treated him with the oral antibiotic Augmentin® (amoxicillin-clavulanic acid) and incision of the finger, but this had not resolved his complaints. He had multiple vesicles on the finger, which led to the diagnosis of herpetic whitlow, which we confirmed by polymerase chain reaction testing. All cutaneous abnormalities disappeared after treatment. Conclusions: Whitlow is rarely caused by the herpes simplex virus, but this disease requires a swift recognition and treatment to prevent complications. This case serves to emphasise that not all whitlow is caused by a bacterial infection, and that it is important to differentiate between herpetic and bacterial whitlow, as these diseases require a different treatment.

Introduction

Herpetic whitlow is an infrequently seen cause of infection of a finger. It is estimated to affect 2.5 per 100,000 people each year. It is caused by the herpes simplex virus type 1 (60%) or type 2 (40%). When it is seen, it is generally in patients with occupational hazards such as medical workers, dental workers, hairdressers or thumb-sucking children. As herpetic whitlow is rare, it may go underrecognised or be mistaken for a different kind of infection of the finger. Delayed recognition and/or treatment puts patients at risk of complications ranging from superinfection to herpetic encephalitis [1,2]. In patients with specific occupational hazards or those with an atypical whitlow, physicians should be aware of herpetic whitlow.

Case presentation

A 23-year-old Caucasian man with no medical history was referred to our emergency department by his primary care physician because of swelling and erythema of the little finger of his left hand for ten days prior to presentation. He had been prescribed the antibiotic Augmentin® (amoxicillin-clavulanic acid), and the primary care physician had already incised the finger releasing clear liquid (no pus). Despite this therapy, his complaints persisted. He had no fever or itching, and had never had these complaints before (Figures 1 and 2).

We confirmed the erythema and swelling of the distal phalanx of his left little finger, with vesicles with a yellow translucent colour. From these vesicles, a clear fluid spontaneously discharged. There was no pus, bony tenderness or pain over his flexor tendons. The motion of his finger was unlimited, and he had no fever (Figures 3  and 4).

On the basis of the clinical appearance we considered herpetic whitlow with superinfection. When asked, he confirmed he had also observed vesicles on his genitals. He denied ever having sexual intercourse or contact with infected individuals. A polymerase chain reaction on herpes simplex virus type 1 was positive on both the material from his genital vesicles and on material from his finger. We referred him to a dermatologist for further treatment. Because of spontaneous subsidence of his complaints, Fucidine® (fusidic acid) cream was chosen as primary treatment. In other cases, in which subsidence does not occur spontaneously, antiviral agents such as acyclovir or valacyclovir may also be used.

The herpes simplex virus causes two types of infections: primary and recurrent. Usually, a break in the skin barrier (for example a wound) allows the virus to enter the tissue and establish an infection. Appearing several days after a person's first exposure, the sores of a primary infection last approximately 1 to 3 weeks. They heal completely, rarely leaving scars. Nevertheless, after the primary infection, the virus remains in the body, hibernating in nerve cells. Certain triggers can cause the hibernating (latent) virus to become active and travel back to the skin. Recurrent infections tend to be milder than primary infections, and generally occur in the same location as the primary infection [3,4].

Conclusions

Whitlow is rarely caused by the herpes simplex virus, but this disease requires swift recognition and treatment to prevent complications. As this treatment differs from that of a traditional whitlow, physicians should be aware of herpetic whitlow.

Consent

Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Figure 1
1Patient's finger, dorsal view. Dorsal and radial side of the patient's little finger, showing yellowish vesicles and erythema.

Figure 2
2Patient's finger, dorsal view (Figure 1) zoomed in.

Figure 3
3Patient's finger, radial view. Radial side of the patient's little finger, showing yellowish vesicles and erythema.

Figure 4
4Patient's finger, palmar view. Palmar side of the patient's little finger, showing two yellowish vesicles.
AcknowledgementsSusanne Veeken revised the manuscript critically for important intellectual content.Received: 5 November 2014 Accepted: 8 April 2015Competing interestsThe authors declare that they have no competing interests.Authors' contributions PG drafted the manuscript. TS revised it critically for important intellectual content. Both authors read and approved the final manuscript.
Herpetic whitlow. I B Wu, R A Schwartz, Cutis. 793Wu IB, Schwartz RA. Herpetic whitlow. Cutis. 2007;79(3):193-6.

Herpetic whitlow: an occupational hazard. R W Klotz, AANA J. 581Klotz RW. Herpetic whitlow: an occupational hazard. AANA J. 1990;58(1):8-13.

Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution. Freedberg Irwin MMcGraw-Hill1317New YorkFitzpatrick's Dermatology in General Medicine. Submit your manuscript at www.biomedcentral.com/submitFreedberg Irwin M, editor. Fitzpatrick's Dermatology in General Medicine. 6th ed. New York: McGraw-Hill; 2003. p. 1317, 2063, 2068. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit


Successful treatment of a T4 lung tumor with vertebral body invasion using fiducial markers in the thoracic spine for image-guided radiation therapy: A case report

Anudh K Jain
John Handal
Lawrence J Solin
Successful treatment of a T4 lung tumor with vertebral body invasion using fiducial markers in the thoracic spine for image-guided radiation therapy: A case report
C A S E R E P O R T Open Access
Introduction: Paravertebral and paraspinal tumors pose a significant challenge in radiation therapy because of the radiation sensitivity of the spinal cord and the need for maximum treatment accuracy. Implantation of fiducial markers into vertebral bodies has been described as a method of increasing the accuracy of radiation treatment for single-dose stereotactic radiosurgery for spinal and paraspinal primary tumors and metastases. However, utilization of this technique has not been described for conventionally fractionated radiation therapy. This report is the first of its kind in the literature and describes successful treatment of a T4 primary lung tumor with vertebral body invasion with conventionally fractionated, image-guided radiotherapy using fiducial markers implanted in the thoracic spine. Case presentation: Our patient was a 47-year-old African-American man who presented to our hospital with a history of several months of increasing left arm pain, chest pain, dyspnea on exertion, occasional dry cough, and weight loss. He was found to have stage IIIA T4, N0, M0 lung cancer with vertebral body invasion. He had fiducial markers placed in the thoracic spine for image-guided radiation treatment set-up. The patient received 74 Gy radiation therapy with concurrent chemotherapy, and daily matching of the fiducial markers on the treatment machine allowed for treatment of the tumor while sparing the dose to the adjacent spinal cord. With one year of clinical follow-up, the patient has had regression of the tumor with only asymmetric soft-tissue thickening seen on a computed tomographic scan and grade 1 dyspnea on exertion as the only side effects of the treatment. Conclusion: Fiducial marker placement is a safe and effective technique for maximizing the accuracy and reproducibility for radiation treatment of lesions near the spinal cord. This technique may be used in conventionally fractionated radiation treatment regimens, such as those employed to treat a lung tumor with vertebral body invasion, to potentially improve clinical outcomes for patients.

Introduction

The radiation tolerance of the spinal cord has traditionally been a dose-limiting factor in the treatment of spinal and paraspinal lesions. Intensity-modulated radiation therapy (IMRT) planning has the ability to achieve concave dose distributions that provide spinal cord sparing even if the target lesion is only millimeters away [1]. However, these treatment plans have very steep dose gradients, so a very high degree of precision is needed during radiation delivery. Even very slight set-up errors may result in significant deviation of delivery of the planned dose [2].

Fiducial marker matching is a method of image-guided radiation therapy (IGRT) used to maximize set-up accuracy. Radiopaque markers are implanted in or near the tumor site and can be imaged on the treatment machine and matched to the digitally reconstructed radiograph (DRR) from the planning computed tomography (CT) scan. The majority of published data regarding fiducial markers in the spine have pertained to methods used in stereotactic radiosurgery [3][4][5]. Our case report describes the application of this technique for conventionally fractionated radiation treatment of a lung tumor. The application of IGRT using fiducial markers in the spine in our patient allowed for radiation treatment of primary lung cancer with vertebral body invasion while limiting the radiation dose to the adjacent spinal cord.

Case presentation

Our patient was a 47-year-old man who presented to our hospital with a history of several months of increasing left arm pain, chest pain, dyspnea on exertion, occasional dry cough, and a 2.3 kg weight loss over the course of the preceding three months. A physical examination showed 4 of 5 weakness of the left upper extremity but no other abnormalities.

He underwent CT of the chest, which showed a large left upper lobe mass measuring 6.4 cm × 3.3 cm, encasing the great vessels, and invading the T3 vertebral body ( Figure 1). A video-assisted thoracoscopic biopsy of the left upper lobe mass was positive for non-small-cell carcinoma. Multiple mediastinal lymph nodes, including stations L2, L4, L5, and L7, sampled negative for tumor. A positron emission tomography (PET) scan showed hypermetabolic uptake in the mass but no mediastinal or distant metastases.

The patient was diagnosed with stage IIIA T4, N0, M0 lung cancer on the basis of the AJCC Cancer Staging Manual, Seventh Edition, staging system criteria [6]. He was offered enrollment in Radiation Therapy Oncology Group (RTOG) protocol 0617, and he consented. He was randomized to receive 74 Gy of radiation therapy using conventional daily fractions of 2 Gy with concurrent carboplatin and paclitaxel, followed by consolidation carboplatin and paclitaxel.

He was evaluated by an orthopedic surgeon (JH) for implantation of fiducial markers for IGRT because of the proximity of the tumor to the spinal cord. Markers were placed in the operating room with fluoroscopic guidance. A commercially available fiducial marker kit (CIVCO Medical Solutions, Kalona, IA, USA) was used, with 1.2 mm × 3 mm gold markers pre-loaded in 17gauge sterile placement needles. The patient was sedated using general anesthesia. A 13-gauge Jamshidi bone marrow biopsy needle (CareFusion Corp., San Diego, CA, USA) Verified. was inserted into the pedicle of the T2 vertebral body. The pre-loaded needle containing the fiducial marker was inserted through the vertebroplasty trochar, and the gold marker was deployed into the bone (Figures 2 and 3). Bone wax was used to secure the markers in place. This procedure was repeated for the T3 and T4 vertebral bodies. The patient was then discharged to home. The only side effect he reported from the procedure was mild pain at the surgical sites, which lasted for three days and was controlled with over-the-counter pain medications.

The patient underwent CT simulation for radiation therapy planning with the use of a custom Alpha Cradle foam mold and wingboard (Smithers Medical Products, Inc., North Canton, OH, USA) Verified for immobilization. CT scans of the patient were taken during inspiration, expiration, and free breathing. CT simulation images were fused with PET images to aid in target delineation. Gross tumor volume was outlined during inspiration, expiration, and free breathing scanning and  fused to form an integrated target volume. A margin of expansion of 5 mm was used to create a clinical target volume (CTV). An additional expansion of 5 mm was used to create a planning target volume (PTV). The CTV and PTV margins were decreased in the areas of bone to limit microscopic disease extension and organ motion in this area. A five-beam IMRT treatment plan was devised to provide 95% coverage of the PTV with the prescription dose of 74 Gy delivered at 2 Gy per fraction. The maximum spinal cord dose was 48.54 Gy, with a concave dose distribution and tight dose fall-off in the area of vertebral body invasion. Figure 4 demonstrates the sharp fall-off from the treatment dose of 74 Gy (red) to the approximate spinal cord tolerance dose of 50 Gy (purple). The volume of lung receiving 20 Gy was 17%. The treatment plan, including lung, heart, and esophagus dose parameters, was within the specifications of the RTOG 0617 protocol.

Treatment was delivered on a Trilogy™ machine (Varian Medical Systems, Inc., Palo Alto, CA, USA) using daily kilovoltage (KV) imaging, which helped us to clearly visualize the fiducial markers ( Figure 5). The position of the fiducial markers was marked on the DRR and superimposed on the KV image taken on the treatment machine, and appropriate shifts were made (Figures 6 and 7). Corrections were made in the vertical, longitudinal, and latitudinal directions as indicated. The range, median, and mean values of shifts are reported in Table 1. Migration of fiducial markers was not noted during the patient's treatment.

The patient developed improvement in left arm pain and strength three weeks into radiation treatment. He developed grade 2 esophagitis toward the end of radiation treatment, which was controlled with diet modification and sucralfate as needed. His esophagitis resolved four weeks after treatment was completed.

A CT scan of the chest and abdomen obtained 10 months after radiation treatment showed stable soft-tissue asymmetry in the mediastinum, with no evidence of recurrent or metastatic disease (Figure 8). At his oneyear follow-up visit, the patient reported grade 1 dyspnea on exertion but was otherwise asymptomatic.

Discussion

IGRT has emerged as a method of improving radiation treatment accuracy for tumors near the spinal cord. Three forms of IGRT for this purpose have been described in the literature: cone-beam CT (CBCT), KV X-ray imaging, and fiducial marker matching.   CBCT involves use of a CT scan that can be taken on the treatment machine. The tumor volume or normal structures on the CBCT scan are then matched with the treatment-planning CT scan, and appropriate shifts can be made. Kim et al. [7] used CBCT to set up single-fraction stereotactic body radiotherapy for spinal treatments and found that it provided precise target localization with accuracy within 2 mm. KV X-ray imaging involves the use of orthogonal Xray images that can be taken in the treatment room. These images have a higher resolution than traditionally used megavoltage (MV) images and allow for matching of patient anatomy to bony landmarks on a DRR. Yin et al. [8] at Henry Ford Hospital have used KV X-ray imaging with anatomy matching to vertebral bodies for intensity-modulated spinal radiosurgery and found that patient motion could be reduced to within 3 mm when coupled with good immobilization.

Fiducial markers have been used successfully in spinal radiosurgery at a number of institutions, including the University of Pittsburgh [3] and Stanford University [4]. The implantation of markers involves an invasive procedure with associated risk. Gerstzen et al. [5] reported a series of spinal radiosurgery procedures where fiducial tracking was used in 30 cases, and they reported one durotomy secondary to the marker implant procedure. Movement, or migration of markers, can also interfere with the use of fiducial markers for accurate treatment set-up. Shirato et al. [9] reported marker migration in one of three patients who underwent transcutaneous insertion of spinal markers for radiotherapy.

However, there are data suggesting that there may be increased accuracy of fiducial markers with the use of other forms of IGRT. Watchman et al. [10] compared KV X-ray imaging and fiducial marker matching for the set-up of 18 treatment fractions of stereotactic spinal radiotherapy. They found that matching to implanted markers was consistently more accurate, by   approximately 0.5 mm, which also led to significant sparing of the spinal cord dose. Fiducial markers carry several practical advantages. The markers can be clearly visualized on MV imaging ( Figure 9). Some centers that may not have newer modalities such as KV imaging or CBCT available can still use MV imaging for the daily set-up to fiducial markers. The daily matching process takes only a few minutes for each patient, so it can be implemented in busy clinical departments with minimal impact on staffing needs and machine time. The use of spinal markers also limits the possibility of human error during the matching process, such as matching to the wrong vertebral body, which can occur when using other forms of IGRT.

The case of our patient shows an extension of this technique from stereotactic radiosurgery to conventionally fractionated radiation therapy. Patients who have spinal or paraspinal tumors who are not candidates for radiosurgery because of tumor factors such as large tumor size or other clinical reasons (such as indications for concurrent chemotherapy) may benefit from the use of spinal fiducial markers for conventionally fractionated radiation therapy.

Conclusions

Fiducial marker placement is a safe and effective technique for maximizing the accuracy and reproducibility of radiation treatment to lesions near the spinal cord. The procedure can be performed on an out-patient basis and with little discomfort to the patient. This technique can be used in combination with IMRT in conventionally fractionated radiation therapy to potentially improve clinical outcomes for patients.

Consent

Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Figure 1
1Pre-treatment computed tomographic scan.

Figure 2
2Anteroposterior view of fiducial marker placement.

Figure 3
3Lateral view of fiducial marker placement.

Figure 4
4Radiation dose distribution.

Figure 5
5Kilovoltage image of fiducial markers (blue arrows) (anteroposterior view).

Figure 6
6Matching of digital reconstructed radiograph to kilovoltage image using fiducial markers (anteroposterior view).

Figure 7
7Matching of digital reconstructed radiograph to kilovoltage image (lateral view).

this article as: Jain et al.: Successful treatment of a T4 lung tumor with vertebral body invasion using fiducial markers in the thoracic spine for image-guided radiation therapy: A case report. Journal of Medical Case Reports 2011 5:470.

Figure 9
9Megavoltage image of fiducial markers (blue arrows) (anteroposterior view).

Table 1
1Daily shifts at treatment set-up (in centimeters)Direction
Range
Mean
Median

Vertical
0 to 0.7
0.2
0.2

Longitudinal
0.4 to 1.3
0.9
0.8

Latitudinal
0.3 to 1.0
0.6
0.5

© 2011 Jain et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Jain et al. Journal of Medical Case Reports 2011, 5:470 http://www.jmedicalcasereports.com/content/5/1/470 Page 2 of 5
Authors' contributions AKJ supervised all aspects of radiation treatment planning and delivery, analyzed and interpreted the patient data, and performed literature review. JH performed the implantation of the fiducial markers. LJS analyzed and interpreted the patient data and conducted the literature review. All authors read and approved the final manuscript.Competing interestsThe authors declare that they have no competing interests.
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