Abstract

Introduction

Parasitic mastitis causing some degree of inflammation and fibrosis in the mammary tissue has been described in free-ranging odontocete and mysticete cetaceans.^1,2,4 This report describes the diagnosis of parasitic mastitis, by ultrasonography and by demonstration of the presence of parasite eggs in milk samples, in a group of three female bottlenose dolphins (Tursiops aduncus) and the attempts at treatment.

Case Report

Three bottlenose dolphins (Tursiops aduncus) were housed together in pools that were part of a complex of concrete pools containing a total of 4.5 million L of chlorinated, natural seawater. Origin, reproductive status, age, and time in captivity for each female are presented in Table 1.

Table 1. Description of the three bottlenose dolphins (Tursiops aduncus)

In January 2001, enlargement of the mammary glands was first noted in dolphin E upon visual inspection. Later, similar enlargement was seen in dolphin A and H. No clinical signs were observed in dolphin A and H. Dolphin E presented with a brief period of anorexia, which was diagnosed as being due to hepatic disease, and it resolved with supportive treatment and antibiotics.

Female dolphins at this facility are monitored weekly by ultrasound to assess ovarian activity or fetal development. As soon as enlargement was noted, mammary glands were scanned weekly to objectively assess gland size and appearance in detail. A single lesion within the muscle overlying the left mammary gland had been detected on ultrasound in dolphin E in February 2000. In dolphin H, smaller lesions in the muscle adjacent to the left mammary gland and within left mammary tissue were seen in November 2001. On 23 January 2002, the presence of a helminth was confirmed in the central lactiferous canal of the left mammary gland of dolphin E. The diameter of the parasite was 1.4 mm; its length was estimated at 6–10 cm. Ultrasound images from dolphin A and H were suggestive of the presence of a similar parasite.

Milk collection was performed on each dolphin, using a breast pump connected to a size 2 human infant inflatable anesthetic facemask (King Systems, Noblesville, IN, USA). Eggs were present in milk samples from all three females (dolphins A and E from 1 February 2002, dolphin H from 13 March 2002). Eggs were elliptical, measuring 25–30 µm x 27.5 µm, and were detected on fresh smears and by sedimentation.

The affected females were kept physically separated from the rest of the animals in that complex of pools, although they were held in the same water system. Treatment was initiated with ivermectin orally at a dose rate of 0.2 mg/kg three times at 2-week intervals. The mammary glands were monitored weekly by ultrasound for the presence of parasites, and milk samples were obtained every 2 weeks to evaluate for the presence of eggs. The presence of the parasite was confirmed again on ultrasound 2 weeks after the last dose of ivermectin. Eggs continued to be present in milk samples.

Discussion

The elongated, oval mammary glands are located just below the blubber along each side of the genital slit. The slits, which house the nipples, are just lateral to the larger, longer, mid-ventral genital slit. The nipples protrude quite noticeably during the period of suckling, but otherwise are drawn within the general contour of the body.⁵ Mammary glands are in the same portion of the body as the ovaries and are visible at each ultrasound scan where ovarian function is being assessed.

Differential diagnoses for increased mammary size include lactation (postpartum or via hormonal stimulation, such as lactation induced by the presence of a calf), bacterial mastitis, parasitic mastitis,⁴ environmental pollutants, and neoplasia.⁷

Ultrasonography proved to be a useful technique to objectively measure the size of the glands, as well as demonstrate the presence of intra-mammary parasites. The presence of milk in the main lactiferous duct allows delineation of the parasite and increases likelihood of diagnosis. Images pre- and post-milk sampling demonstrated this, as the parasite was much more difficult to visualize when the ducts were empty. It is not known whether the presence of the parasite stimulates production of milk. The lesions within muscle adjacent to the mammary tissue in two of the three females appeared similar to the description of lesions caused by Crassicauda grampicola in Atlantic white-sided dolphins (Lagenorhynchus acutus). In that report, nodules, thin-walled and containing dissolving nematodes, or in one case, containing a verminous coil within the musculature overlying the gland were observed.⁴ Acoustic shadowing, visible on ultrasonography in dolphins A and H, indicated the presence of mineralization, which could suggest the presence of a nonviable parasite. There appeared to be, in all three female dolphins in this case, a degree of hyperplasia or fibrosis of the lactiferous ducts, visible on ultrasound.

The size and shape of the eggs and of the parasite in dolphin E were consistent with a parasite belonging to the class Nematoda, but it has not been identified. Parasites causing mastitis in cetaceans have been reported to belong to two genera: Crassicauda and Placentonema.^1,2,6 Here, treatment was initiated with ivermectin since this agent has been suggested for treatment of Crassicauda sp.-infested cetaceans.³ Failure of ivermectin to eliminate the parasite could be related to the small percentage of the drug being excreted in milk.

As the parasite has not been identified and its life cycle is not known, it appears prudent to consider that this parasite may be transmitted by the following routes: ingestion of eggs from the environment, pre-natal infection, post-natal infection through nursing, or infection by ingestion of an intermediate host such as an invertebrate or a fish species. As in Toxocara canis, all four modes of transmission could occur concurrently for this parasite.

Possible implications for the collection if treatment proves to be unsuccessful include permanent infestation of these three females. The impairment of future lactation in females is a concern. As described in Atlantic white-sided dolphins (Lagenorhynchus acutus), replacement of normal mammary tissue by non-secretory tissue may occur. Additionally, the presence of firm fibrous replacement tissue might impair milk output. In cetaceans, milk output depends on forcible abdominal muscular compression of a normally pliable gland in order to extrude milk.⁴ There is also a possibility of transmission to offspring and to other dolphins held in the same complex of pools. Members of the genus Crassicauda are commonly observed in mammary tissue, around the genitalia, as well as in kidneys. Although there is no evidence of this in other animals in this collection, the unidentified parasite in this case could potentially affect the males as well as females if the pathogenic effects are not limited to the mammary tissue.

Conclusion

To date, we believe that this is the first report of a case of parasitic mastitis diagnosed with the help of ultrasonography. Identity of the parasite has not been established, and treatment with ivermectin has been unsuccessful. Routine ultrasonographic examination of the mammary glands and collection of milk samples in lactating cetaceans or females presenting with enlarged mammary glands are encouraged. Gross and microscopic examinations of the mammary tissue from necropsies are recommended. These may allow further determination of the incidence of parasitic mastitis in captive bottlenose dolphins, as well as aid in the identification of the parasite involved.

Acknowledgments

The authors wish to thank Ocean Park’s marine mammal trainers, veterinary technician and laboratory staff and manager for their help, as well as Andrew Routh for the review of this abstract.

Literature Cited

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