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Parasites in fine needle breast aspirates—assessment of host tissue response
  1. K Sahai,
  2. K Kapila,
  3. K Verma
  1. Cytopathology Laboratory, Department of Pathology, All India Institute of Medical Sciences, New Delhi, India
  1. Correspondence to:
 Dr Kusum Kapila, Cytopathology Laboratory, Department of Pathology, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India

Abstract

Parasites in the human breast are uncommon but not rare. Cysticercus and filariasis in fine needle breast aspirates have been documented and their cytomorphology is well characterised. However, the host tissue response to these parasites and the factors responsible for their initiation are not clear. Over a 21 year period, 28 cases of breast parasites (16 cases of cysticercus and 12 of filariasis), diagnosed by fine needle aspiration cytology, were reviewed to assess the host tissue response.

  • parasites
  • fine needle breast aspirates
  • host tissue reaction

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Cytomorphological diagnosis of parasitic lesions in various parts of the body is well established.1,2 The diagnostic morphological criteria of Cysticercus cellulosae, microfilarial larvae, and adult forms of Wuchereria bancrofti are well documented.3–6 Parasitic infection of the breast, though uncommon, is not rare. Presence of cysticercosis, filarial worms, and schistosomiasis have been reported.4,7,8 Since these parasites present as lumps in the breast they are a cause for concern as they are often clinically suspected to be malignant. It is known that parasites can remain in human tissues for varying periods of time without invoking any adverse host inflammatory response. All the factors responsible for initiation of the host inflammatory response are not clear,9 but it is this host response that brings on the symptoms and signs of the parasites' presence. This study was therefore undertaken to study the cytomorphology of parasites in breast lumps and document the host tissue response in fine needle aspirates.

METHODS

Over a 21 year period (1980–2000) 28 breast aspirates, in which parasitic infections had been diagnosed, were retrieved and reviewed from the case files of the cytopathology laboratory of the All India Institute of Medical Sciences. In all 28 cases the chief complaint was a mass in the breast, clinically thought to be a tumour. Eleven cases were suspected to have a carcinoma. In all the cases smears stained with both alcohol fixed Papanicolaou and air dried May-Grünwald-Giemsa were reviewed. Histology was available in three cases.

RESULTS

All 28 patients were females with ages ranging from 14 to 65 years. Of the 28 cases, 16 showed features of cysticercus while 12 showed features of filariasis, and a gravid adult worm was identified in four of them. The age of the patient, size and duration of the lump, and the cytomorphological findings are shown in tables 1 and 2.

Table 1

Cytomorphological findings in patients with breast cysticercosis

Table 2

Cytomorphological findings in patients with filariasis of the breast

Of the 16 cases of Cysticercus cellulosae, larval bladder wall fragments of varying sizes were seen in 15 cases. In all these cases clear fluid or fluid admixed with necrotic material was aspirated. The cases having large larval fragments showed the ciliated wall of the larva thrown into several rounded folds. The parenchymal reticulin of thin fibrils could be seen with ovoid nuclei having characteristic prominent chromatin condensation. Three of the 15 cases showed bits of degenerating parasite. The remaining case yielded 2 ml of clear acellular fluid and the parasite was detected on histology. All the 15 cases that showed fragments of cysticercus were associated with varying degrees of inflammatory response ranging from the presence of a few eosinophils to marked acute and chronic inflammatory cell infiltrate (fig 1). Palisading histiocytes were seen in 12 of the 15 cases (fig 2). The three cases that showed pieces of degenerating parasite were associated with a dense acute inflammatory cell reaction, and numerous polymorphs could be seen infiltrating the degenerating fragments. Calcareous corpuscles were seen in only one case.

Figure 1

Acute and chronic inflammatory cells with foreign body giant cells (Papanicolaou stain × 200).

Figure 2

Cysticercus cellulosae showing parenchymal reticulin with cluster of palisading histiocytes (May-Grünwald Giemsa stain × 100).

In four of the 12 cases that showed evidence of filarial infection an adult worm was identified. Three were gravid containing microfilariae (fig 3) in various stages of development while in one case the empty cuticle of the adult filarial worm was seen. In two cases the breast aspirates showed an eosinophilic infiltrate only and microfilariae were seen in the aspirates from the ipsilateral lymph nodes. In six aspirates numerous sheathed microfilariae were seen. Aspirates from all the cases showed an inflammatory response comprising eosinophils and polymorphs. Three of the cases showed epithelioid cell granulomas with palisading histiocytes (fig 4).

Figure 3

Gravid adult filarial worms with elongated and coiled forms of larvae along with benign ductal cells and inflammatory cells (Papanicolaou stain × 100).

Figure 4

Microfilarial larva with an epithelioid cell granuloma (Papanicolaou stain × 200).

DISCUSSION

Parasitic infections of the breast, though uncommon, have been described by many authors. The majority of the cases described are those of filariasis.10Anderson's Pathology states that the lymphatic vessels of the mammary gland are commonly involved after those of lower extremities, retroperitoneal tissues, and the scrotum.11 The other parasites described are cysticercosis,4 schistosomiasis,7 and dirofilariasis.8

The host tissue response to the parasites is extremely variable and ranges from an insignificant response to marked inflammatory cell infiltration with histiocytes and formation of epithelioid cell granulomas. The tissue response to cysticercus has been divided into five stages.9 The initial response is patchy and comprises macrophages and lymphocytes. After this a well formed layer of palisading histiocytes is seen and is believed to be derived from circulating macrophages. As the inflammatory response achieves chronicity, eosinophils appear. Later the necrotising parasite is invaded by polymorphs. However, most of these parasites often do not invoke any host tissue response as the parasites produce taeniaestatin and other poorly defined molecules which interfere with the cellular immune response.12 The factors responsible for the parasite degeneration are not known. The appearance of various HLA molecules on the surface of the parasite are believed to be one of the reasons.13 Certain physical factors such as the firm non-expansile nature of the host tissue may contribute in limiting the growth of the parasite and initiating the host inflammatory response.

In this study it was not possible to find a correlation between the duration of the breast lump, its size, and the intensity of the host immune reaction. However, palisading histiocytes and eosinophils were consistent features in these aspirates emphasising the fact that the host inflammatory response does indeed occur in stages.9 Probably the initial response showing lymphocytes is too short lived and therefore was not picked up on cytology. An acute inflammatory exudate was also seen in a number of cases and it is this that is probably responsible for the signs and symptoms of the breast lump. The three cases that showed the degenerating parasite had numerous polymorphs infiltrating the parasite fragments. Calcareous corpuscles were seen in only one case and it is now believed that these corpuscles serve as nidus for focal deposition of exceeding amounts of calcium protecting the larvae against calcification.14

In cases of filariasis also the tissue immune response is variable, with intact worms provoking only minimal reaction. The degenerating parasite is associated with inflammatory cell infiltration particularly eosinophils. Filarial granulomas have been commonly described.10 In this study epithelioid cell granulomas were seen in three cases. It should be mentioned that the presence of granulomas should not lead to a mistaken diagnosis of tuberculosis as the necrosis associated with filariasis is never as complete as that of tuberculosis. Moreover the presence of eosinophils should prompt the cytopathologist to search for a parasite.

To conclude, the cytomorphology of cysticercosis and filariasis in breast aspirates is well characterised and can be easily recognised. They are associated with a prominent cellular reaction. It is not possible to correlate the host immune response with the duration or size of the breast lump. However, the presence of palisading histiocytes and eosinophils are features seen consistently with cysticercosis, while epithelioid cell granulomas are more commonly associated with filariasis in the breast. The factors responsible for the initiation of the immune response and the death of the parasite are not well known. However it is probably the initiation of the immune response that causes local symptoms and draws attention to the parasite.

REFERENCES

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