Original Article

Fine-needle aspiration cytology as a diagnostic modality for cysticercosis: A clinicocytological study of 137 cases ABSTRACT Background: Cysticercosis, a parasitic tissue infection caused by the larva of Taenia solium, is quite a common disease in our part of the world, but its incidence is often underestimated. Fine-needle aspiration cytology (FNAC) plays an important role in early detection of this disease, especially when the lesion is located in anatomically approachable superficial locations. Aims: The aim was to study role of FNAC in the diagnosis of cysticercosis. Materials and Methods: In this retrospective study, the data of 137 patients with palpable nodules, who were diagnosed as having or suspicious of cysticercosis on FNAC, were retrieved and analyzed. Results: In 129 (94.2%) cases, a definitive diagnosis of cysticercosis was obtained in the form of parts of parasite tegument, hooklets, parenchymatous portion and calcareous corpuscles. In the background, giant cells, mixed inflammatory cells, and epithelioid cells were present. In remaining 8 (5.8%) cases, larval fragments could not be identified on the aspirates, and the diagnosis of parasitic inflammation was suggested on the basis of other cytological findings such as clear fluid aspirate, presence of eosinophils, histiocytes, foreign body giant cells, a typical granular dirty background, etc. Follow-up biopsy in these 8 cases confirmed the diagnosis of cysticercosis in 7 (87.5%) while in 1 (12.5%) case, histopathology was suggestive of parasitic cyst. Conclusion: Fine-needle aspiration cytology in cysticercosis is a low-cost outpatient procedure. The cytological diagnosis is quite straightforward in cases where the actual parasite structures are identified in the smears. In other cases, a cytological diagnosis of suspicious of cysticercosis can be given if the cytological findings suggest the same. Key words: Cysticercosis; fine-needle aspiration cytology; parasite

Introduction Cysticercosis is the parasitic disease caused by the larval stage of Taenia solium (pork tapeworm), the Cysticercus cellulosae. Areas of endemic disease include Central and South America, India, China, Southeast Asia, and sub-Saharan Africa.[1,2] Saran et al.[3] proposed the use of fine-needle aspiration cytology (FNAC) in diagnosing cysticercosis. Currently, other diagnostic tools such as radiologic imaging, serology and immunologic detection are also in use, but the gold standard still remains Access this article online Quick Response Code Website:

the demonstration of the parasitic larva.[4-6] Thus, fine-needle aspiration (FNA) which provides direct and specific diagnosis of cysticercosis remains one of the ideal diagnostic procedure wherever the lesion can be approached easily by FNAC. The diagnosis is further reconfirmed by the histopathological examination of the excised specimen. This study, apart from studying the role of FNAC in the diagnosis of cysticercosis was also aimed at analyzing the incidence, clinical features and cytomorphology of the parasite. In addition, in those cases where the actual parasite could not be demonstrated, other cytological features suggestive of cysticercosis were also looked for.

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Materials and Methods DOI: 10.4103/0970-9371.138665

Fine-needle aspiration cytology is an outpatient procedure. Currently, our center carries out more than 3000 FNACs

Pooja Kala, Pratima Khare Department of Pathology, Dr. Baba Saheb Ambedkar Hospital, Rohini, New Delhi, India Address for correspondence: Dr. Pooja Kala, C/O Dr. Dinesh Mohan Kala, 5-New Road, Opposite Doon Hospital, Dehradun - 248 001, Uttarakhand, India. E-mail: [email protected]

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every year. In this retrospective study, spanning over last 10 years from April 2003 to March 2013, the records of all those patients who were finally diagnosed as cysticercosis on FNAC were retrieved. During this period, more than 25000 FNACs were carried out at our center. There were 137 patients, presenting with palpable nodules at different sites where diagnosis of cysticercosis was established. Subsequent excision biopsy was also evaluated wherever possible. The histopathological sections were reviewed, and findings were correlated with the cytological findings.

Table 1: Age distribution of patients (n = 137)

Results

Table 2: Anatomical distribution of lesions in patients (n = 137)

This study included 137 patients in the age group 2-75 years. There was no sex preponderance and the incidence was almost equal among males and females. Peak incidence was observed in the second and third decades (65.7%). The disease was uncommon in the elderly population [Table 1]. The most common affected site for the lesions was upper extremity, followed by the head and neck in our series. Chest and abdominal wall were also affected in a significant number of cases. Multiple foci were present in 5 patients (3.6%) [Table 2]. Most the patients presented with painless, slow growing nodule with consistency varying from soft to firm. The size of lesion varied from 0.5 to 6 cm in diameter. Associated regional lymphadenopathy was uncommon and present only in 5 cases (3.6%). The duration of disease varied from a week to many years; however, most patients had a history of only a few months (43.8%). The clinical diagnosis at the time of the first examination was not cysticercosis. In 95 cases (69.3%), the aspirate was clear fluid, varying in an amount from a few drops to 15 mL. Cytocentrifuge preparations were made when the amount of fluid was significant. The aspirate was purulent in 23 (16.8%) cases, whereas it was blood mixed in 18 (13.1%) and granular or particulate in 1 case [Table 3]. In 129 cases, actual parasite structures were seen in the smears. In 88 (64.2%) cases, multiple fragments of parasite were present, while in 41 (29.9%) cases, only one fragment was present. In 11 (8%) cases, degenerated forms were also seen. Hooklets were present in 38 (27.7%) cases while suckers were seen only in 3 (2.1%) cases. Calcific corpuscles were observed in 60 (43.8%) cases while 23 (16.8%) cases demonstrated calcification. The microscopic examination of smears revealed the bladder wall in 129 (94.2%) cases. The bladder wall comprised of outer acellular pinkish layer, following which were seen subcuticular or tegumental cells with small pyknotic-looking nuclei set in a loose, fibrillary parenchyma with varying vacoulation [Figures 1

Age in years

Number of cases

Percentage of cases

20 43 47 16 09 01 – 01 137

14.6 31.4 34.3 11.7 6.6 0.7 0 0.7 100

1-10 11-20 21-30 31-40 41-50 51-60 61-70 71-80 Total

Anatomical site Scalp Face Periorbital Oral cavity Neck Back Axilla Arm Forearm Chest wall Abdomen Lower extremity (thigh) Lower extremity (lower leg) Breast Multiple sites Total

Number of cases

Percentage

2 10 2 3 18 15 4 29 9 14 14 6 3 3 5 137

1.5 7.3 1.5 2.2 13.1 10.9 2.9 21.2 6.6 10.2 10.2 4.4 2.2 2.2 3.6 100

Table 3: Comparison of gross and cytological findings with those in a previous study FNAC findings Nature of aspirate Clear Purulent Blood mixed Particulate Cytological findings Fragments of larva Hooklets Full parasite Calcareous corpuscle Palisading histiocytes Foreign body giant cells Epithelioid cell granulomas Calcified material Mixed inflammation Acellular cyst wall Complications

Handa et al.[7] (n = 125) (%)

Present study (n = 137) (%)

61 (48.8) 36 (28.8) 9 (7.2) 19 (15.2)

95 (69.3) 23 (16.9) 18 (13.1) 1 (0.7)

57 (45.6) 1 (0.8) 1 (0.8) 3 (2.4) 40 (32.5) 38 (30.4) 6 (4.8) 8 (6.4) 112 (89.6) – 2 (1.6)

129 (94.2) 38 (27.7) 1 (0.7) 60 (43.8) 34 (24.8) 63 (46) 31 (22.6) 23 (16.8) 130 (94.9) 2 (1.5) None

FNAC: Fine-needle aspiration cytology

and 2]. In one of the aspirate, full scolex was seen with attached crown like a row of hooklets, four suckers, followed by the neck

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and then the spiral canal [Figure 3]. Hooklets were refractile and triangular in shape with a pointed end and two blunted [Figure 4]. In 2 cases, acellular parasitic wall with attached giant cells and palisading histiocytes was seen. The inflammatory cells were also seen surrounding and infiltrating parasite fragment [Table 3]. The background of the smears were typically pink granular in 81 (59.1%) cases, clean in 36 (26.3%) cases, necrotic in 18 (13.1%) and reactive in 2 (1.4%) cases. The smears showed a mixed inflammatory infiltrate comprising neutrophils (49.6% cases), lymphocytes (62%), eosinophils (39.4%), plasma cells (40.1%), histiocytes (75.9%), and giant cells (46%). Collections of histiocytes were noted in 34 (24.8%) cases. In 35 (25.5%) cases, well-formed epithelioid cell granulomas were also present. In 48 (35.0%) cases, scattered epithelioid cells were seen. These cases were subjected to Ziehl Neelson staining and the hooklets were found to be acid fast when present, whereas there was no evidence of any acid fast bacilli. Fibroblasts, degenerated inflammatory cells, granulation

tissue fragments were also seen in a small proportion of cases. Scattered bare parasite nuclei and histiocytes with engulfed such nuclei were seen in 8 (5.8%) cases. In 8 (5.8%) cases, parasite was absent. However, suspicion of a parasitic lesion was made in view of a clear fluid aspirate and the presence of eosinophils, neutrophils, palisading histiocytes, and giant cells in a typical pinkish granular background along with calcareous corpuscles. Excision biopsy and subsequent histopathological examination confirmed the diagnosis of cysticercosis in seven of these cases [Figure 5], while in the remaining one case; the histopathology was suggestive of parasitic cyst.

Discussion Cestodes have a lifecycle characterized by two stages- larva and adult, besides an egg phase. The human is a definite host

Figure 1: Aspirate smear showing the fragment of parasite (Giemsa, ×100)

Figure 2: Smear showing bladder wall comprised of -outer acellular pinkish layer, following which were seen subcuticular or tegumental cells with small pyknotic-looking nuclei set in a loose, fibrillary parenchyma with varying vacoulation and occasional calcific corpuscle (Giemsa, ×400)

Figure 3: Aspirate revealing scolex of Cysticercus cellulosae with attached hooklets and suckers (Giemsa, ×100)

Figure 4: Smear showing characteristic hooklets of Cysticercus cellulosae (Giemsa, ×1000)

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and pig is an intermediate host. The larval form of Taenia solium that is, Cysticercus cellulosae is the cause of cysticercosis. The adult form lives in the intestine of human beings. It attaches to the intestinal wall by a scolex and sheds gravid proglottids,[2] which are passed into the soil or water, where the eggs are released. When an intermediate host (i.e., pig and sometimes human) consumes the eggs,[3,5] oncospheres are released. These burrow through the intestinal wall to reach various tissues of the host through hematogenous route, where they develop into encysted cysticerci or bladder worms.[8] The lifecycle completes when undercooked meat is eaten, then the cysticerci are released and attach to the intestinal wall of the definite host (i.e., human) and develop into adult worms.[9] The cysticercus secretes certain substances locally (e.g., paramyosin, taeniastatin), which alter the host immune response. Both cellular as well as humoral immunity are affected. [10] With passage of time, somehow these mechanisms become ineffective, and the inflammatory response leads to degeneration of the parasite, granuloma formation and calcification. The clinical manifestations depend on location and number of lesions at a particular site.[11] The most frequent sites affected are skeletal muscles, subcutaneous tissue, brain, ocular tissue, heart, liver, lungs, and peritoneum.[3,12-14] In our series [Table 2], upper extremity was the most common site to be affected, followed by the head and neck. The unusual finding of multiple foci present in a single individual was present in 5 cases (3.6%). There were three cases (2.2%) of cysticercosis of the oral cavity, which is also an unusual location for cysticercosis. Similar observations about oral cavity region have also been reported by other authors.[15] A comparison about distribution of the site of lesions with a previous large series[7] has been attempted [Table 4]. Demonstration of fragment of larval bladder wall, hooklets and calcareous corpuscles confirms the diagnosis of cysticercosis.[7] In our series, fragments of the larva was seen in 129 cases (94.2%), and hooklets in 38 cases (27.7%), whereas Handa et al.[7] have reported significantly lower percentage of cases with these findings in their series. Similarly, our series had significantly higher percentage of cases with cytological findings of calcareous corpuscle and epithelioid cell granulomas. A comparison about cytological findings of our series with that of Handa et al.[7] have been presented [Table 3]. The presence of scolex in cytology smears is an uncommon finding.[16-18] In our large series also, it was a rare finding and scolex was seen only in 1 case. In the presence of marked necrosis, the diagnosis of cysticercosis on FNAC

Figure 5: Histological section showing Cysticercus cellulosae (H and E, ×100)

Table 4: Anatomical distribution of cases — comparison with a previous study Anatomical region Head and neck Chest wall Upper extremity Abdominal wall Lower extremity Miscellaneous

Handa et al.[7] (n = 125) (%)

Present study (n = 137) (%)

34 (27.2) 22 (17.6) 35 (28) 17 (13.6) 6 (4.8) 11 (8.8)

35 (25.5) 14 (10.2) 38 (27.7) 14 (10.2) 9 (6.6) 27 (19.7)

is difficult. The hooklets and calcareous corpuscles remain the only recognizable parasitic structures in such cases.[7] The local immune response of the host 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. It initially comprises of macrophages and lymphocytes followed by the appearance of palisaded histiocytes. Eosinophils and plasma cells appear still later. Subsequently, neutrophils surround and invade the parasite and lead to its degeneration. Epithelioid cell granulomas can also be present in the later stages. Foreign body giant cells are invariably present in surrounding inflammatory zone.[19] This whole spectrum of inflammatory reaction against the parasite was also observed in our series as well.

Conclusion Fine-needle aspiration cytology helps in early diagnosis of cysticercosis and helps in proper management of the disease. The cytological diagnosis of cysticercosis is quite straight forward in cases where actual parasite structures are identified in the FNA smears. However, in a few cases, none of such features may be present, and the inflammatory infiltrate may also be variable. In such situations, biopsy

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and subsequent histopathological examination helps in pinpointing the diagnosis. It should be kept in mind that cysticercosis is much more common in our part of the world than usually thought. Hence, in all inflammatory/cystic/ inflammatory-cystic lesions, the possibility of cysticercosis should be kept in consideration.

9. 10. 11. 12. 13.

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How to cite this article: Kala P, Khare P. Fine-needle aspiration cytology as a diagnostic modality for cysticercosis: A clinicocytological study of 137 cases. J Cytol 2014;31:68-72. Source of Support: Nil, Conflict of Interest: None declared.

Journal of Cytology / April 2014 / Volume 31 / Issue 2

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Fine-needle aspiration cytology as a diagnostic modality for cysticercosis: A clinicocytological study of 137 cases.

Cysticercosis, a parasitic tissue infection caused by the larva of Taenia solium, is quite a common disease in our part of the world, but its incidenc...
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