Mammographic parasitic calcifications in South West Nigeria: prospective and descriptive study

Introduction Lymphatic filariasis caused by nematode parasite Wuchereria bancrofti and Brugia Malayi is endemic in the tropics. In Nigeria, 25% of the population is infected. Lymph edema and elephantiasis are the predominant manifestations. Its infrequent manifestation is in the breast. This paper discusses the epidemiology, reviews literature, imaging options and mammographic appearances of these parasitic nematodes. Methods This prospective descriptive study reports on 39 cases of parasitic calcifications seen during mammography in the Radiology Department, University College Hospital between 2006 and 2012 in Ibadan, South West Nigeria. Each mammogram was reported by MO and ATS: assigned a final Bi-RADs category. Parasitic calcifications were further evaluated for distribution, and types of calcification. Results A total of 527 women had mammography done between 2006 and 2012. Thirty-nine women (7.4%) had parasitic breast calcifications. The ages of the women ranged between 38-71 years - mean of 52.36±8.72 SD. Twenty-three (59%) were post-menopausal, 16(41%) were pre-menopausal. The majority (31; 79.5%) were screeners while 8(20.5%) were follow up cases. Approximately half (51.3%) of the women had no complaints. Pain (23.1%) was the commonest presentation in the remaining half. Solitary calcifications were predominant (20) while only 3 cases had 10 calcifications. Left sided calcifications (53.8%) were the majority. Calcifications were subcutaneous in 2/3rds of the women (66.7%) while the Yoruba tribe (84.6%) was principal. Conclusion Parasitic breast calcifications can be misdiagnosed on mammography for suspicious micro-calcification. This publication should alert radiologists in a tropical country like Nigeria to increase diagnostic vigilance thereby preventing unnecessary anxiety and invasive work-up procedures.


Introduction
Filariasis is common in most tropical and subtropical countries [1].
In Nigeria, the epidemiology of the disease is complicated because of the multiplicity of the environmental conditions of the different regions [2]. The distribution is more extensive than has been described because of deteriorating drainage systems, large-scale dam and irrigation projects which have created suitable breeding sites for filarial vectors in various parts of Nigeria3. In the past six decades, various levels of endemicity of filariasis have been documented in different parts of Nigeria including Benue, Plateau, Taraba, Oyo, and Bauchi states [2][3][4]. One out of every three sufferers of filariasis in the tropics lives in the Federal Republic of Nigeria [5].
Lymphatic filariasis is caused by the nematode parasite Wuchereria bancrofti and Brugia malayi. Other studies show filariasis due to Mansonella perstans and Mansonella streptocerca infections vastly recorded in different parts of Nigeria [6]. It is endemic throughout the tropics [7]. It is equally distributed in both sexes [8] and affects an estimated 120 million people worldwide7. In Nigeria as much as 25% of the population are infected [9]. The predominant manifestations of the infection are caused by obstruction of the lymphatics which leads to lymphedema, hydrocele and elephantiasis. An infrequent manifestation is lymphatic filariasis involving the female breast [10][11][12][13].
This study of mammographic findings in 39 women in Ibadan South West Nigeria with parasitic calcification of the breast is aimed at increasing the diagnostic vigilance for the parasites thereby preventing misdiagnosis for suspicious micro-calcifications in a country that is endemic for the disease.

Methods
A prospective descriptive study carried out in the Radiology Department of the University College Hospital between 2006 and 2012. Thirty-nine (39) women were involved, out of 527 women who presented for both screening and diagnostic mammography.
Informed consent was obtained from the identified women; after which an assisted questionnaire was administered before a physical examination was performed. Two standard views MLO and CC were obtained utilizing the General Electric senographe 2000 machine.
Additional Spot magnification views were also obtained for evaluation of these calcifications. MO and AA reported these mammograms and assigned a final Bi-RADs category. Details of distribution and types of calcification as well as demographics of the women with the parasitic calcifications were described. Breast ultrasound scan was additionally performed with a linear-array, 10 MHz transducer. The women were predominantly of the Yoruba tribe (84.6%) and domiciled in Ibadan (74.5%). The size of the calcifications ranged between 1-4mm. Whole breast ultrasound was performed on all women but showed no abnormality.

Discussion
Filariasis is uncommon in developed countries; where it is seen occasionally in travel immigrants from endemic areas of the disease [9,14]. The prevalence of lymphatic filariasis is over 40 million in sub-Saharan African accounting for about 40% of all cases worldwide [15]. It is endemic in the tropics where Nigeria is situated. In Oyo state, four major rivers flow through one of the Page number not for citation purposes 3 local government areas in a north to south direction, the Ogun, Oyan, Ofiki and Opeki and these have been documented as Simulium breeding sites [16]. A detailed history revealed that the women are domiciled in Ogun, Ondo, Lagos and Ibadan which are in the South West geopolitical zone of Nigeria [17]. A history of previous community screening for the disease was elicited with endemicity of filarial disease in the towns of their nativity but no form of treatment for the disease was obtained from the women [3,16].
Though peripheral blood film was negative for microfilaria in these women making clinical diagnosis difficult. However a negative peripheral blood smear does not preclude the diagnosis of filariasis.
This was confirmed in a study conducted by Ogunba [18] in Nigerians infected with loa loa, with up to half of the cases with low peripheral microfilaria levels. Other techniques that may be useful for the diagnosis are tests for antifilarial antibodies/circulating parasitic antigens and polymerase chain reaction (PCR) which is expensive and not frequently performed in Nigeria [15]. No biopsy was performed in the patients.
Fredman and Kalisher [9], reported transmission of filariasis by means of a bite from a mosquito (that has previously bitten an infected host). The mosquito then deposits infective larvae on the skin. The larvae migrate through the puncture wound to reach the subcutaneous vessels where they mature into the adults over a period of 6-months to 2 years. The patient?s infection can remain dormant for decades which are likely in these women. The adult worms mate and produce microfilaria which circulates in the blood stream with a periodicity that generally matches the feeding habits of the mosquito vector [14]. The life cycle is completed when the microfilaria are ingested by the mosquito. W. bancrofti the predominant variant of the two types is more common in Nigeria.

The other variant B. Malayi is responsible for infection in parts of
Asia [14]. The clinical presentation of the infection is due to lymphatic dysfunction, inflammation and obstruction. Later, this region drained by the local lymphatic system is prone to secondary bacteria and superficial fungal infection resulting in further lymphatic damage the so-called granulomatous lymphangitis and may lead to skin changes called elephantiasis [7,9,14].
The breast is a recognized though infrequent site of involvement [14]. In the breast, granulomatous lymphangitis develops in the tissue adjacent to the lymphatic vessel [11] and eventually block the vessels which are soon replaced with fibrous tissue [8] and the patient may present with a palpable breast mass, the filarial granuloma or mass and microcalcifications. In a review of 131 cases of filarial granuloma of the breast [11], it was reported that in most cases, the solitary and superficial filarial nodule was palpable and in more than half the cases the clinical impression was suggestive of a breast tumour, one patient even underwent a simple mastectomy.
However, none of these patients presented with a palpable mass rather, their mammograms demonstrated tortuous, ring?like microcalcifications like the report by Chow et al [14]. On the overall, benign dystrophic calcifications common in the breast can also be differentiated from those of parasitic diseases on the bases of their coarse, dense and irregular appearance [8].
Chen and Xie [10] also warned that foci of calcification of worm are frequent presentation rather than the occasional calcifications of the whole and entire worms. These foci of calcifications could simulate suspicious comedo calcifications and could be wrongly treated as a cancer. In this instance, it is recommended that other stigmata of cancer be considered before a final diagnosis is made. Previously, the full worm calcifications were considered intermediate; which led to localization and excision biopsy [14]. Now with increased awareness of the disease, diagnosis is likely to be more accurate as other ancillary investigative tools could be utilized for final diagnosis. One of the complications of excisional biopsy is the appearance of residual calcifications in follow-up mammograms. The residual micro-calcifications of degenerating and calcifying nematodes may also be confused with malignant calcification [14].
It is therefore important that filarial calcifications are critically assessed, diagnosed accurately and properly categorized to avoid an unnecessary, expensive, invasive procedure like excision biopsy.

Conclusion
This paper illustrates that wormlike calcifications are also visible on mammograms. Radiologists should be aware of the endemic nature of filariasis in the country. As routine mammography becomes available in Nigeria, there is a need for a high level of suspicion for parasitic calcifications in the breast parenchyma in mammographic images so that the infection will not be misdiagnosed for a malignant breast lesion.

Competing interests
We declare that we have no competing interests.

Acknowledgments
We wish to thank all the residents in the department of Radiology, involved in the retrieval of the mammograms for evaluation; radiographers especially Ada Odita and Mrs. Adepoju as well as the dark room technicians for their contributions.