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Cytopathology including fine-needle aspiration in sub-Saharan Africa: a Cameroon experience.

Around 1986, a general hospital in Calgary (currently Calgary Laboratory Services), Alberta, Canada, began accepting anatomic pathology specimens from a rural, missionary-run hospital in Cameroon (Banso Baptist Hospital, Banso, Cameroon), which has no pathology department or on-site pathologists. Specimen shipments are typically received every 2 to 3 months. Since the implementation of our electronic database in 2003, we have accessioned and reported 978 specimens during a 3-year period. Although these specimens are reported within 2 weeks, approximately 4 months elapse from the time the specimens leave Cameroon to the time the reports reach the treating physicians. These delays may have adverse consequences for some patients.

The benefits of this successful relationship with the Banso Baptist Hospital (BBH) led us to consider whether it would be possible to provide even greater assistance by offering an on-site clinic for fine-needle aspiration (FNA). We undertook this pilot study to assess the feasibility and value of this option.

PATIENTS AND METHODS

This prospective study was conducted for a 5-week period in September and October 2007. Our laboratory in Canada donated many of the materials and the equipment, including a teaching microscope. Space for the FNA clinic was provided by BBH. Banso Baptist Hospital is a 200-bed hospital with surgical, medical, and pediatric wards. The main diagnostic modalities within the hospital are routine laboratory testing, plain x-ray, and portable ultrasonography.

Patients were referred to the FNA clinic by BBH physicians. All patients were interviewed and examined by 1 of the pathologists, and verbal consent was obtained from each patient after discussion of the benefits, limitations, and possible complications of the procedure. When possible, relevant demographic data and clinical findings, including HIV status, were documented for each patient.

Fine-needle aspirations were performed by 2 of the authors (K.G. and M.K.). Palpable superficial lesions were aspirated by using sterile 25-gauge needles and 10-mL disposable syringes. On average, 2 passes were performed per case and direct smears were prepared from the aspirated material. Palpable, intra-abdominal masses were aspirated with a 25-gauge lumbar puncture needle under ultrasound guidance and with the assistance of an ultrasonography technologist. This was done after the exclusion of bleeding tendencies (by using clinical assessment and laboratory testing for bleeding and coagulation times). After the introduction of the needle into the lesion, the stylet was removed and a 10-mL syringe was mounted on the needle. Aspiration was performed as the needle was carefully moved within the lesion. Vacuum was released before the needle was removed. One pass was performed per patient and direct smears were prepared. Patients were observed for at least 4 hours after the procedure. Fluid specimens (urine and serous effusions) were centrifuged and the sediments were used to prepare direct smears. Cervical smears were collected, by using a wooden spatula, after pelvic examination and visual inspection of the cervix. All smears were fixed in alcohol and stained with hematoxylin-eosin. Ziehl-Neelsen (ZN) staining was performed on at least 1 of the smears if tuberculosis was clinically suspected or if granulomatous inflammation was noted on hematoxylineosin staining. All slides were reviewed by both pathologists and a consensus diagnosis was reached for every case. The diagnoses were recorded on the cytology working sheets, documented in the patients' charts, and discussed with the referring physicians.

Quality assurance was conducted through clinical-pathologic correlation conferences and retrospective review of the slides in a proportion of cases. A turnaround-time (TAT) was also logged for each case. After the return to Calgary, cytohistologic correlation was done for 18 cases by using subsequently procured biopsies and resection specimens (Table).

RESULTS

During the 5-week period, 60 patient encounters were recorded. One patient was seen twice for unrelated findings (a clinically benign breast lump and pneumonia associated with pleural effusion). Thirty-three of 59 patients (56%) were females and 26 (44%) were males, with both a mean and median patient age of 38 years. Ten patients (17%) were HIV negative, 16 (27%) were HIV positive, and 33 (56%) had unknown HIV status.

Although variable sites were sampled, most aspirates were from the head and neck region (17/60), 13 of which were enlarged lymph nodes. From the latter, 7 aspirates showed granulomas and/or necrotic material suggestive of tuberculous infection, and the diagnosis was confirmed by Ziehl-Neelsen staining in 6 cases (Table). Two lymph node aspirates led to the diagnosis of non-Hodgkin lymphomas and 1 showed a metastatic, undifferentiated carcinoma consistent with upper aerodigestive primary tumor. One patient was diagnosed with sinus histiocytosis with massive lymphadenopathy (Rosai-Dorfman disease); for 2 patients the etiology of the lymphadenopathy could not be determined and the aspirates were reported as "negative for malignancy." The remaining 4 head and neck aspirates revealed a follicular thyroid neoplasm, a branchial cleft cyst, chronic submandibular sialadenitis, and a parotid gland abscess. Nine HIV-positive patients (60%) underwent FNA for head and neck lesions.

The second most common site sampled for aspirates was the breast (15/60 cases). Of the aspirated masses, 4 (26%) were carcinomas. The benign diagnoses included 3 fibroadenomas, 5 cases of fibrocystic change, 1 galactocele, 1 gestational gigantomastia, and 1 case of gynecomastia.

Six palpable abdominal masses were aspirated, 5 under ultrasound guidance. Of these, 3 were hepatic masses (2 hepatocellular carcinomas and a benign hepatic cyst) and 3 extrahepatic masses (2 large cell lymphomas and an adenocarcinoma of the descending colon). None of the patients suffered procedure-related complications. In addition, intraoperative FNA (bench aspirate) was performed on a cystic ovarian mass, which was diagnosed as a serous adenocarcinoma, and on an intrauterine mass, which was mainly placental tissue.

Of the remaining 6 fine-needle aspirates, 3 were from axillary lymph nodes. Two of the latter were reported as metastatic breast carcinoma and 1 as a low-grade non-Hodgkin lymphoma. One inguinal lymph node aspirate was diagnosed as classical Hodgkin lymphoma. Two superficial soft tissue "tumors" from the upper and lower extremities were reported as possible inflammatory masses with no features of malignancy.

Nongynecologic exfoliative cytology specimens included 4 urine and 2 ascitic fluid samples and 1 pleural effusion and 1 breast nipple discharge sample. All were negative for malignant cells and no acid fast bacilli were detected by Ziehl-Neelsen staining in the serous effusion samples. In addition, touch imprints were prepared from prostatic core biopsies from 2 patients; 1 was diagnosed as an adenocarcinoma and the other yielded negative cytology results.

Five cervicovaginal smears were collected for diagnostic purposes (for visible or palpable abnormalities). Of these, 1 showed invasive squamous cell carcinoma and another showed a small blue cell malignancy consistent with rhabdomysarcoma. Two smears were negative for intraepithelial lesion or malignancy and 1 was considered unsatisfactory (mostly blood).

Nine of 44 FNAs (20%) were initially deemed unsatisfactory and required repeated passes to establish a diagnosis. Ultimately, most of the superficial lesions required 2 passes to procure satisfactory specimens. In all, a definitive diagnosis was rendered on 52 of 60 samples (87%). In addition, a differential diagnosis and management recommendations were provided on 6 specimens. These differential diagnoses allowed for patient triage, although no specific pathologic classification was given. Two specimens were unsatisfactory. Clinical follow-up identified 1 false-negative diagnosis (1.6%) of Kaposi sarcoma, but no confirmatory biopsies were performed, and subsequent cytohistologic correlation revealed 1 false-positive diagnosis (1.6%) of lymphoma (Table). The cost of the procedure was approximately US $10 (5000 CFA [Cooperation financiere en Afrique centrale] francs) per patient with a TAT ranging from less than 24 hours to 7 days, the average TAT being 2.9 days. For cases procured during the last 3 weeks of the study, the TAT dropped to an average of 1.5 days.

COMMENT

Cytopathology is a simple, relatively affordable, and reliable diagnostic modality that can improve patient care in low-resource countries. (1-8) In this study, we assessed the feasibility of implementing an FNA cytology service in a rural hospital in Cameroon.

Most patients who were referred to our clinic had superficial masses and 28% had enlarged lymph nodes. In the context of high prevalence of HIV and tuberculosis infections, (9) lymphadenopathy is a common clinical finding and a diagnostic challenge for clinicians. (10) The main differential diagnoses include persistent generalized lymphadenopathy, tuberculosis lymphadenitis, lymphoma, and Kaposi sarcoma. (4,11-14) Fine-needle aspiration has been used in the diagnosis of these entities with high accuracy rates. (15-22) Our results demonstrate the value of FNA for triaging patients with lymphadenopathy. A definitive cytologic diagnosis was provided for 90% of the aspirates, thus obviating the need for open biopsies and allowing for immediate treatment (eg, antituberculous drugs) when indicated.

A palpable breast lump is a frequent clinical presentation among female patients at BBH, and most of the patients undergo open biopsies for diagnosis. In this study, breast lesions were the second most common indication for FNA. The procedure proved to be highly effective in distinguishing benign from malignant lesions, and we did not detect any false results by retrospective reviews or by cytohistologic correlation with the subsequently resected specimens. Most of the cancer patients presented at an advanced stage of the disease (Figure 1, a and b), but patients were reluctant to accept radical surgical procedures without a pathologic diagnosis. In fact, 1 of our patients opted to postpone her surgery for 3 months when she learned that she could get a pathologic diagnosis when we arrived in the country. Patients with clinically benign disease, on the other hand, were reassured by the cytologic diagnosis, and the need for the unnecessary open biopsies was eliminated. The cost of the FNA procedure was less than 10% of that of the open procedures. Our observations are similar to those of Spillane and colleagues, (6) who have reported on the role of FNA in reducing the number of breast surgeries and improving the quality of patient care in the rural setting.

Hepatocellular carcinoma is one of the leading cancer types in men and women in sub-Saharan Africa. (23) The utility of FNA in diagnosing this disease had been demonstrated in a study by Ajdukiewicz and coworkers, (24) who also commented on the safety of the procedure. In our study, FNA of intra-abdominal masses was facilitated by the availability of an ultrasonography diagnostic service, and we were able to obtain adequate samples from all 6 masses that we aspirated, with no complications. Although the liver tumors were clinically suspected of being hepatocellular carcinomas, it was important to confirm this diagnosis cytologically and to exclude other treatable conditions such as lymphoma.

Cytology as a screening tool for premalignant lesions of the uterine cervix (Papanicolaou smears) has not been adopted in Cameroon, (25) and cervical cancer is still the leading cancer in women. (23) Other screening methods, such as visual inspection of the cervix with acetic acid, (26) are available at BBH but have not been used on a large scale. Most of the women who were referred to our clinic for a Papanicolau test had visible or palpable cervical lesions, and we used cervical cytology as a diagnostic test. Although the proper collection devices were not available to us, the procedure was worthwhile and allowed for the definitive diagnosis of invasive squamous carcinoma and sarcoma botryoides in 2 patients.

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It is well accepted that having "on-site" pathologists performing the FNA procedures improves the specimen adequacy rate. Such a setting also allows the pathologist to assess the clinical aspects of the disease and enhances the diagnostic accuracy. (22,27) This was a major advantage in our study and compensated for many of the limitations within which we had to operate, and it allowed us to render accurate diagnoses of rare entities without ancillary studies. For instance, it was possible to make the diagnosis of embryonal rhabdomyosarcoma on a cervicovaginal smear (Figure 2, a through c), and the diagnosis of unilateral gestational giagantomastia on a breast FNA, only because we had the opportunity to interview and examine our patients before interpreting the cytology smears. Our patients certainly benefited from the rapid TAT, as many of them did not have to make several journeys before receiving treatment. Repeated travel was not only a financial burden for some patients, but was also stressful for their families. Being on site also allowed us to lend our services in unexpected circumstances, such as providing intraoperative cytologic diagnosis. Perhaps the most beneficial aspect, however, was the daily interaction with clinical colleagues at the patient's bedside, which entailed instant clinicopathologic correlation and ensured patient safety.

The main limitations were the lack of ancillary studies (eg, immunocytochemistry, flow cytometry) and the inability to prepare cell blocks. The effects of those limitations are illustrated in our 2 false results. On retrospective review of the slides of the lymph node aspirate that was misclassified as non-Hodgkin lymphoma, we believe that the "overcall" was in part due to air-drying artifact. This led to a false perception of an increase in number of the large lymphoid cell component. An additional adequate FNA pass, with prompt fixation of the smears, could probably have led to the correct diagnosis, which is likely persistent generalized lymph-adenopathy (Table). Theoretically, this pitfall could also have been avoided if immunophenotyping had been available.

Our false-negative case was associated with an aspirate of an ulcerated leg mass, which was clinically consistent with Kaposi sarcoma (Figure 3, a). We could not make this cytologic diagnosis because of the hypocellularity of the specimen, which was mainly blood elements, and the inability to immunophenotype the few spindle cells that we detected (Figure 3, b). Such difficulties and limitations were previously described by Gamborino et al. (22)

Initially, we also encountered some difficulties in obtaining reliable staining reagents, such as hematoxylin, from within Cameroon. Many of the reagent bottles that were delivered to us were properly sealed and labeled; yet, their contents were not what the label indicated. In addition, the ethyl alcohol that we received had a high water content, which led to a peculiar artifact when the slides were processed and covered (Figure 4). These difficulties adversely affected our turnaround time and inconvenienced some of our patients during the first week of our visit, but we subsequently obtained better quality reagents and our average TAT improved significantly.

In this study, we have demonstrated the feasibility of implementing a diagnostic FNA cytopathology clinic in a rural hospital in Cameroon. The FNA procedure is cost-effective and is applicable to the most frequently encountered superficial and deep lesions. The availability of an on-site pathologist has many advantages but permanent staffing of an FNA clinic remains a challenge. Introducing an elective rotation in pathology of tropical diseases to our residency training curriculum will add to the strength of our program and will enhance the opportunity for providing an on-site cytopathology service for extended periods. We hope that our experience will encourage other institutions and volunteers to pursue similar endeavors and will ultimately motivate medical graduates from the developing countries to dedicate their careers to laboratory medicine.

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The authors wish to thank the staff and patients of Banso Baptist Hospital, the University of Calgary postgraduate medical education office and Pathology Residency Training Program, Calgary Laboratory Services, and the American Society for Clinical Pathology for their support of this project.

References

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(6.) Spillane AJ, Littlejohn D, Wong S, Robertson AO, Crowe PJ. Australia's breast surgery workload is changing: comparison of a metropolitan and a rural hospital. Aust N ZJ Surg. 1999;69(3):178-182.

(7.) National Cancer Institute Fine-Needle Aspiration of Breast Workshop Subcommittees. The uniform approach to breast fine-needle aspiration biopsy. Diagn Cytopathol. 1997;16(4):295-311.

(8.) Oertel YC, Odegbile A. Fine needle aspiration in rural areas. Lancet. 2008; 371(9619):1147-1148.

(9.) Dye C, Harries AD, Maher D, Hosseini SM, Nkhoma W, Salaniponi FM. Tuberculosis. In: Jamison DT, Feachem RG, Makgoba MW, et al. Disease and Mortality in Sub-Saharan Africa. 2nd ed. Washington, DC: The World Bank; 2006:179-193.

(10.) Harries AD. Tuberculosis and human immunodeficiency virus infection in developing countries. Lancet. 1990;335(8686):387-390.

(11.) Sharma SK, Mohan A, Kadhiravan T. HIV-TB co-infection: epidemiology, diagnosis & management. Indian J Med Res. 2005;121(4):550-567.

(12.) Reid AJC, Miller RF, Kocjan GI. Diagnostic utility of fine needle aspiration cytology in HIV-infected patients with lymphadenopathy. Cytopathology. 1998; 9(4):230-239.

(13.) Martin-Bates E, Tanner A, Suvarna S, Glazer G, Coleman DV. Use of fine needle aspiration cytology for investigating lymphadenopathy in HIV positive patients. J Clin Pathol. 1993;46(6):564-566.

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(16.) Pithie AD, Chicksen B. Fine needle extrathoracic lymph-node aspiration in HIV-associated sputum-negative tuberculosis. Lancet. 1992;340(8834-8835): 1504-1505.

(17.) el Hag IA, Chiedozi LC, al Reyees FA, Kollur SM. Fine needle aspiration cytology of head and neck masses: seven years' experience in a secondary care hospital. Acta Cytol. 2003;47(3):387-392.

(18.) Michelow P, Meyers T, Dubb M, Wright C. The utility of fine needle aspiration in HIV positive children. Cytopathology. 2008;19(2):86-93.

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Kelly Guggisberg, MD, FRCPC; Chukwudi Okorie, MD; Moosa Khalil, MBBCh, FRCPC

Accepted for publication June 5, 2009.

From the Department of Pathology and Laboratory Medicine, University of Calgary and Calgary Laboratory Services, Calgary, Alberta, Canada (Drs Guggisberg and Khalil);and the Department of Surgery, Banso Baptist Hospital, Banso, Cameroon (Dr Okorie).

The authors have no relevant financial interest in the products or companies described in this article.

Presented in part at the symposium on Pathology in Developing Countries at the annual meeting of the Canadian Association of Pathologists, Ottawa, Ontario, Canada, July 14, 2008.

Reprints: Moosa Khalil, MBBCh, FRCPC, Department of Pathology and Laboratory Medicine, Foothills Medical Centre, C1125, 1403 29 St NW, Calgary, AB T2N 2T9, Canada (e-mail: moosa.khalil@cls.ab.ca).
Summary of Cytohistologic and Clinical Correlation for 25 Patients

Case Age, HIV
No. y/Sex Status Clinical Presentation and Site

1 23/M Bilateral, painful, firm, markedly enlarged
 cervical nodes, 8 months' duration
2 4/F ? Bilateral, enlarged cervical nodes, 3
 months' duration
3 57/M Neg Parotid mass/lymph node, previous diagnosis
 of "diffuse lymphocytic lymphoma"
4 28/M Pos Large right supraclavicular node
5 38/M Pos Cervical adenopathy, cough for 6 weeks
6 42/M Neg Cervical adenopathy, fever and weight loss
7 30/M Pos Cervical lymphadenopathy, left
 supraclavicular
8 37/F Pos Enlarged, painless right cervical lymph
 nodes, severe anemia
9 38/M Pos Cervical lymphadenopathy
10 22/F ? Large, cystic right breast mass, 1 year's
 duration after child birth
11 56/F ? Breast mass, 8 cm, fixed
12 50/F ? Right breast mass, fungating
13 43/M Pos Nontender, hypogastric abdominal mass,
 fever, and abdominal pain
14 34/F ? Intrauterine mass, vaginal bleeding
15 63/F ? Cystic ovarian masses, clinically
 endometrioma
16 62/M Neg RLQ/abdominal wall mass, peripheral
 neuropathy
17 51/M Neg LUQ abdominal mass and
 discomfort, anemia
18 11/M ? Painful, deep, ill-defined, forearm soft
 tissue mass, 5 years' duration
19 37/M Pos Left leg, ulcerated anterior soft tissue
 mass
20 34/F ? Vaginal bleeding, palpable cervical mass
21 18/F ? Vaginal bleeding, enlarged uterus,
 grapelike cervical polyps
22 63/M ? Prostatic core biopsy, PSA = 10.5 ng/mL
 initially and normal PSA levels on
 repeated test
23 70/M ? Prostate/rectal mass
24 66/M ? Polyuria, polydipsia
25 55/M ? Chronic retention

Case
No. Procedure Cytologic Diagnosis

1 Lymph node FNA Rosai-Dorfman disease
2 Lymph node FNA TB lymphadenitis
3 Lymph node FNA Large cell lymphoma
4 Lymph node FNA TB lymphadenitis
5 Lymph node FNA TB lymphadenitis
6 Lymph node FNA TB lymphadenitis
7 Lymph node FNA TB lymphadenitis
8 Lymph node FNA Non-Hodgkin lymphoma
9 Lymph node FNA TB lymphadenitis
10 Breast FNA Benign cystic mass consistent
 with galactocele
11 Breast FNA High-grade mammary carcinoma
12 Breast FNA Mammary carcinoma, high grade
13 Ultrasound-guided FNA Large cell lymphoma
14 FNA (intraoperative bench Gestational sac
 aspirate)
15 Intraoperative FNA Adenocarcinoma, high grade,
 bilateral
16 FNA of abdominal wall mass Large cell lymphoma
17 Ultrasound-guided Adenocarcinoma
 FNA consistent with colon
 primary tumor
18 Soft tissue mass FNA Nondiagnostic FNA of soft
 tissue showing no features
 of malignancy
19 Soft tissue FNA Inflamed granulation tissue,
 negative for malignancy;
 biopsy recommended
20 Cervicovaginal smear Invasive squamous cell
 carcinoma of the uterine
 cervix
21 Cervical smear Rhabdomyosarcoma (sarcoma
 botryoides)
22 TP of core biopsy Hypocellular material with no
 evidence of malignancy
23 TP of core biopsy Adenocarcinoma
24 Catheterized, urine Bacterial overgrowth;
 suspect urinary tract
 infection; recommend culture
 and sensitivity testing
25 Voided urine Negative for malignant cells

Case Histologic Diagnosis and
No. Follow-up Clinical Progress

1 Sinus histiocytosis with massive lymphadenopathy
 (Rosai-Dorfman disease)
2 TB lymphadenitis confirmed on tissue biopsy
3 No biopsy but excellent clinical response to chemotherapy
4 Acid fast bacilli identified in a smear by ZN staining
5 Acid fast bacilli identified in a smear by ZN staining
6 Acid fast bacilli identified in a smear by ZN staining
7 TB lymphadenitis
8 Reactive hyperplasia of lymph node
9 Acid fast bacilli identified in a smear by ZN staining
10 Galactocele
11 Invasive papillary carcinoma grade 3/3
12 Metaplastic breast carcinoma
13 No biopsy but good clinical response to chemotherapy and
 subtotal resolution of mass on US
14 Placental tissue
15 Serous adenocarcinoma
16 Diffuse large B cell lymphoma with plasmablastic features
17 Poorly differentiated
 colonic adenocarcinoma
18 Fibroadipose tissue with nonspecific chronic inflammation,
 negative for malignancy
19 Clinically consistent with Kaposi sarcoma but no tissue
 biopsy was done
20 Invasive squamous cell carcinoma of the uterine cervix
21 Embryonal rhabdomyosarcoma of uterine cervix
22 Prostatic core biopsy, negative for malignancy
23 Prostatic adenocarcinoma Gleason score 4 + 4
24 Nodular prostatic hyperplasia
25 Nodular prostatic hyperplasia

Abbreviations: FNA, fine-needle aspiration; LUQ, left upper
quadrant; Neg, negative; Pos, positive; PSA, prostate-specific
antigen; RLQ, right lower quadrant; TB, tuberculosis; TP, touch
preparation; US, ultrasonography; ZN, Ziehl-Neelsen; ?, unknown.
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Author:Guggisberg, Kelly; Okorie, Chukwudi; Khalil, Moosa
Publication:Archives of Pathology & Laboratory Medicine
Date:Feb 1, 2011
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