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Bp:Detection of Hammondia heydorni-like oocysts in feces of a dog with recurrent diarrhea

Martin Steffl and Nadine Nautscher

Institute of Animal Science, Veterinary Practice, University of Hohenheim, Schwerzstr. 15/4, 70599 Stuttgart, Germany


Correspondence to: Dr. Martin Steffl 
Phone: +4971145922450
Fax: +4971145922299
Email:  HYPERLINK "mailto:martin.steffl@uni-hohenheim.de" martin.steffl@uni-hohenheim.de






















Abstract

We report about a male, 15 months-old American Canadian White Shepherd dog suffering from recurrent diarrhea and anorexia. Fecal analysis revealed the detection of coccidian oocysts of small size. Their morphology was similar to those of Hammondia heydorni and Neospora caninum isolates. Measurements revealed a mean length of unsporulated oocysts of 11.8 � 0.96 �m and a mean width of 11.9 � 0.96 �m. H. heydorni infection was suggested based on the larger size compared with N. caninum oocysts. Additionally, realtime polymerase chain reaction analysis for N. caninum from the fecal sample was negative. After a single anti-coccidian treatment accompanied by antibiotic drugs the dog recovered from his disease. H. heydorni-like oocysts were no longer detected in fecal control samples. This case demonstrates that H. heydorni infections may be associated with gastro-intestinal disease in canine species. The role of H. heydorni as single or co-infection remains to be established.



Keywords: diarrhea, dog, Hammondia heydorni, oocysts, treatment

















Introduction

In clinical practice, gastro-intestinal (GI) diseases with signs of soft stool, diarrhea and vomiting are one of the most common diseases of young dogs. Parasitic infections of the GI tract are frequently a cause of illness in young dogs. Recently, it was shown in puppies living in a breeding kennel [1] that the prevalence of parasites is higher than the prevalence of viruses (75% vs 35%). The most prevalent intestinal parasites were Giardia duodenalis (41%) followed by Cryptosporidium parvum (26%), Cystoisospora ohioensis complex (26%) and Toxocara canis (22%). 
Apart from these major parasites there is a group of closely related coccidian parasites (Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi) forming oocysts of 9-14 �m size [2, 3]. Their prevalence in fecal samples of dogs is very low (0.2%) [2]. While T. gondii and N. caninum are widely recognized as infectious pathogens of high importance for human and animal health [4], H. heydorni and H. hammondi infections are regarded to be asymptomatic [2]. Consequentially, there are few clinic reports about infections caused by H. heydorni in dogs (as definitive hosts). Schares and colleagues [2] identified H. heydorni oocyst DNA in fecal samples of 12 dogs. Interestingly, seven of the 12 H. heydorni-shedding dogs had suffered from diarrhea, one dog had anorexia. 
In this case study, we report about a male, 15 months-old American Canadian White Shepherd dog suffering from recurrent diarrhea. Fecal analysis revealed the detection of coccidian oocysts of small size. Their morphology was similar to those of H. heydorni and N. caninum isolates. Finally, H. heydorni infection was suggested based on further investigations. 

Case presentation

The 15 months-old, male American Canadian White Shepherd dog was presented for clinical examination because of recurrent diarrhea. During the last three days, the feces was continuously watery and the dog developed anorexia. In the past, there was a disease history of giardiasis but this could not be verified. 
The clinical examination was largely unremarkable. Rectal temperature (38.5�C), respiratory and heart rate were within reference limits. The dog was not dehydrated but showed discomfort during abdominal palpation. 
A fecal sample was collected and examined immediately by different methods. First, a FASTest� GIARDIA Strip test-kit (Megacor, Austria) was used for the detection of Giardia duodenalis antigens in feces. The test result was negative. Then, some drops of feces were mixed with few drops of distilled water on a slide, covered, and examined directly under a light microscope. In parallel, the fecal sample was treated by a conventional flotation method using saturated magnesium sulphate solution (FASOL, Kruuse, Denmark). Helminthic parasites were not detected with both methods. However, round oocysts of small size were observed at higher magnification (figure 1). 
Light microscopic measurements were performed using the fecal sample treated with flotation solution according to the recommendations of other authors [2]. Morphology of coccidian parasites was analysed under a light microscope (Leica DM 2000 LED, Leica Microsystems, Wetzlar, Germany) connected to a camera (Leica ICC 50, Leica Microsystems) and coupled to a PC. Image processing was performed with integrated image processing software (Leica Application Suite, Version 4.4.0, Leica Microsystems). The length und width of oocysts (n = 20) was measured at three different locations und results are expressed as mean � standard deviation of the mean, minimal and maximal values. The measurements revealed a mean length of unsporulated oocysts of 11.8 � 0.96 �m (range of 9.8 to 13.4 �m). The mean width of oocysts was 11.9 � 0.96 �m (range of 10 to 13.8 �m). The mean length-width ratio was 0.99 � 0.05 �m (range of 0.91 to 1.08 �m).
Additionally, developmental biology of oocysts was studied in the native sample stored in a humid chamber at room temperature (21�C) for several days. Specific observations were made on days 1, 4, 5, 6, and 7 after defecation. 100 oocysts were counted daily at a magnification of 400. Sporulation was first observed at day 4 after defecation (note: sample was not examined at days 2 and 3). Approximately one third to one quarter of oocysts remained unsporulated during the observation period (table 1).
In summary, H. heydorni or N. caninum infection was suggested based on the oocyst morphology. As N. caninum oocysts are shorter (d" 10.7 �m, [2]) compared with oocysts described herein, we favorite H. heydorni species as the causative agent. Realtime polymerase chain reaction (PCR) analysis for N. caninum from the fecal sample was then performed in an accredited veterinary laboratory (Laboklin, Bad Kissingen, Germany) to further differentiate these species. PCR analysis for the detection of N. caninum revealed a negative test result.

Therapy and outcome

The dog with 31 kg body weight was treated orally with Procox� (Bayer, Leverkusen, Germany) and received a single dose of 0.45 mg emodepside + 9 mg toltrazuril per kg body weight. Additionally, antibiotics were prescribed (Amoxitab� 500 mg, cp-pharma, Burgdorf, Germany, 375 mg amoxicillin twice daily for 6 days), because secondary infection with bacteria could not be excluded. 
One week later, the owner of the dog was contacted by phone and he reported that the consistency of the feces returned to normal within two days. Additionally, the dog started to eat only one day after treatment with Procox�. Eleven days after initial examination a serial stool sample (one fecal sample every day for three days) of the dog was analyzed using the same methods described above. Coccidian parasites were not detected.

Discussion

Infectious agents including bacteria, viruses and parasites often cause GI tract disorders of younger dogs. In this case, we focused on parasitic infections because the clinical examination gave no evidence for other probabilities. Specifically, clinical signs like fever, dehydration, sepsis, and bloody stool were not present. Additionally, the dog was vaccinated completely according to the official German guideline for vaccination (StIKO Vet.). 
The fecal analysis revealed unsporulated oocysts of 11.8 � 0.96 �m size. In the past, it was postulated that the light microscopic structures of N. caninum oocysts are similar and indistinguishable to those of H. heydorni oocysts in dog feces [5]. Meanwhile, it was shown that oocysts of N. caninum are shorter (d" 10.7 �m) compared with oocysts of H. heydorni species when analysed in flotation media [2]. These authors also found out that Neospora caninum oocysts have a smaller length-width ratio (d" 1.06 �m) compared with H. heydorni oocysts. In our study the mean length-width ratio of oocysts was 0.99 � 0.05 �m. One reason for this discrepancy may be the small number (20) of oocyst measurements in our study. For comparison, Schares and colleagues [2] characterized oocysts of 29 fecal samples and generated morphological descriptions that are obviously more precise. Nevertheless, Schares and colleagues [2] postulated that it may be possible to identify N. caninum (or H. heydorni) in dog feces based on oocyst morphology. 
Molecular biology methods are actually used to differentiate these species. As a PCR method was not available to detect H. heydorni, we performed the same method in a commercial laboratory to detect N. caninum. The result was negative. We conclude therefore that oocysts found in our case can be regarded as H. heydorni isolates due to two important facts: First, morphologically similar N. caninum oocysts are shorter compared with oocysts described herein. Second, PCR result was negative for N. caninum. 
On the other side, it was shown that morphologically similar structures like T. gondii and H. hammondi oocysts could be present in dog feces, even if the cat is thought to be the definitive host [2]. The latter �ndings suggest that coprophagia of the dog with a subsequent intestinal passage might play a role in the dissemination of coccidian parasites. Based on the morphological descriptions of Schares and colleagues [2], we excluded largely that coccidian parasites as T. gondii and H. hammondi could play a causative role in this case.
Our observations in this case do not exclude that other microbial agents may be principally involved. There are several studies showing the simultaneous presence of multiple enteropathogens in dogs with diarrhea [6, 7]. For example, Duijvestijn and colleagues [7] detected one or more pathogens in 86.5% of diarrhoeic puppies. They found significant positive associations e.g. between canine Parvovirus and Cystoisospora spp.. In our study, the occurrence of bacteria and viruses was not further investigated, because there was no clinical evidence for their involvement. In this context, Duijvestijn and colleagues [7] postulated that routine screening for specific viruses (canine Parvovirus and canine Coronavirus) and bacteria (�-hemolytic Escherichia coli) is only recommended in puppies if they are under three months of age and originate from high-volume dog breeders. Moreover, Gizzi and colleagues [6] demonstrated that co-infection was more prevalent among the 0-1-year-old dogs (58.1%) and occurred less often in 1-8-year-old dogs (13.8%) or in dogs that are >8 years old (12%).
Nevertheless, it is imaginable that H. heydorni oocysts act as predisposing factors to produce an environment conducive to an increase in the abundance of e.g. Clostridium perfringens or Escherichia coli strains. Such interactions between coccidia and bacteria were already shown in animal experiments with other species [8]. A more complete understanding of the effects of predisposing factors and mechanisms of interaction with gut microbiota may help in the future to give better treatment recommendations.
In conclusion, we showed in this case the detection of H. heydorni-like oocysts in feces of a dog with GI symptoms (diarrhea, anorexia). After a single anti-coccidian treatment accompanied by antibiotic drugs the dog recovered from his disease. It is actually not possible to distinguish if the dog recovered due to the anti-coccidian or antibiotic treatment. Both drugs appeared to be indicated because of the high possibility that there may be secondary bacterial infection [9].

References

1. Grellet A, Chastant-Maillard S, Robin C, Feugier A, Boogaerts C, et al. (2014) Risk factors of weaning diarrhea in puppies housed in breeding kennels. Prev Vet Med 117: 260-265.
2. Schares G, Pantchev N, Barutzki D, Heydorn AO, Bauer C, et al. (2005) Oocysts of Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi in faeces collected from dogs in Germany. Int J Parasitol 35: 1525-1537.
3. Jie HJ, Yu M, Fen YY, Mei GY, Yan Y, et al. (2013) First isolation of Hammondia heydorni from dogs in China. Vet Parasitol 197: 43-49.
4. Goodswen SJ, Kennedy PJ, Ellis JT (2013) A review of the infection, genetics, and evolution of Neospora caninum: From the past to the present. Infect Genet Evol 13: 133-150.
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$dh�a$gd�L�$dh�a$gdC(2014) Presence of infectious agents and co-infections in diarrheic dogs determined with a real-time polymerase chain reaction-based panel. BMC Vet Res 10: 23.
7. Duijvestijn M, Mughini-Gras L, Schuurman N, Schijf W, Wagenaar JA, et al. (2016) Enteropathogen infections in canine puppies: (Co-)occurrence, clinical relevance and risk factors. Vet Microbiol 195: 115-122.
8. Moore RJ (2016) Necrotic enteritis predisposing factors in broiler chickens. Avian Pathol 45: 275-281.
9. Turk J, Maddox C, Fales W, Ostlund E, Miller M, et al. (1998) Examination for heat-labile, heat-stable, and Shiga-like toxins and for the eaeA gene in Escherichia coli isolates obtained from dogs dying with diarrhea: 122 cases (1992-1996). J Am Vet Med Assoc 212: 1735-1736. 











Figure legends

Figure 1: Detection of Hammondia heydorni-like oocysts in feces of a 15 months-old dog. Unsporulated oocysts (a) and sporulated oocysts containing two sporocysts (b). Scale bar represents 50 �m. Magnification 40x.





























Tables

Table 1: Number of sporulated and unsporulated oocysts (in %) in a native fecal specimen of an American Canadian White Shepherd dog analyzed at different time points after defecation (100 oocysts counted daily at 40x magnification)

Day 0Day 1Day 4Day 5Day 6Day 7sporulated oocysts (%)0068787565unsporulated oocysts (%)10010032222535
Note: day 0 = day of defecation.














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