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(Chest. 2000;117:1004-1011.)
© 2000 American College of Chest Physicians

The Clinical Application and Cost Analysis of Fine-Needle Aspiration Biopsy in the Diagnosis of Mass Lesions in Sarcoidosis*

Rosemary Tambouret, MD; Kim R. Geisinger, MD; Celeste N. Powers, MD, PhD; Kamal K. Khurana, MD; Jan F. Silverman, MD; Ricardo Bardales, MD and Martha B. Pitman, MD

* From the James Homer Wright Laboratories of the General Hospital and the Department of Pathology (Drs. Tambouret and Pitman), Harvard Medical School, Boston, MA; the Department of Pathology (Dr. Geisinger), Wake Forest University School of Medicine, Winston-Salem, NC; the Department of Pathology (Dr. Powers), Medical College of Virginia/Virginia Commonwealth University, Richmond, VA; the Department of Pathology (Dr. Khurana), SUNY Health Science Center, Syracuse, NY; the Department of Pathology (Dr. Silverman), Allegheny University of the Health Science, Allegheny General Hospital, Pittsburgh,

Correspondence to: Rosemary Tambouret, MD, Department of Pathology, Massachusetts General Hospital, 55 Fruit St, Boston, MA 02114; e-mail: rtambouret{at}partners.org


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Sarcoidosis is a prevalent disease of unknown cause characterized by granulomatous inflammation that often creates deep and/or superficial mass lesions. Tissue samples are considered the "gold standard" in diagnosis; however, it is a medically treated disease. We analyzed the utility and relative cost-effectiveness of fine-needle aspiration biopsy (FNAB) in the clinical investigation of patients with both suspected and unsuspected sarcoidosis.

Methods: All FNAB cases with sarcoidosis either as the cytologic diagnosis or mentioned as part of the differential diagnosis were retrospectively reviewed for clinical history, follow-up, cytologic features, and surgical pathology findings. Comparative analysis of cost of FNAB and excisional biopsy were also made.

Results: Thirty-two FNABs in 28 patients included 17 women and 11 men. Anatomic sites included lymph node (n = 17), lung (n = 5), salivary gland (n = 8), and liver (n = 2). Sarcoidosis had already been diagnosed or was a clinical consideration prior to FNAB in 14 cases. Chest radiograph showed abnormal findings in 19 cases. Angiotensin-converting enzyme (ACE) was measured in seven patients and was elevated in four. All aspirates showed granulomatous inflammation; in 22 patients, special stains or cultures for microorganisms were negative. Simultaneous or subsequent excisional biopsies confirmed the FNAB findings in 17 patients. Institutional ratios of excisional biopsy to FNAB in the diagnosis of sarcoidosis ranged from 4 to 19:1. The cost of FNAB was only 12.5 to 50% that of tissue biopsy.

Conclusions: FNAB appears to be underutilized in the diagnosis of sarcoidosis. When used in conjunction with radiologic and laboratory data, FNAB may be a reliable and cost-effective method of diagnosis, especially in patients with an established diagnosis of sarcoidosis.

Key Words: cytology • fine-needle aspiration biopsy • sarcoidosis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Sarcoidosis is a systemic disease of unknown etiology characterized by small well-formed nonnecrotizing granulomas in one or more organs that can cause significant morbidity and even death.1 2 Traditionally, histologic demonstration of granulomas without associated organisms in tissue has been the diagnostic procedure of choice. Although excisionalbiopsy of easily accessible sites is often performed, more invasive procedures such as mediastinoscopy or large-bore percutaneous needle biopsy may be necessary for diagnosis. In view of the relative frequency of sarcoidosis and the often extensive interventional procedures utilized for diagnosis, we reviewed our experience with the use and cost-effectiveness of fine-needle aspiration biopsy (FNAB) as a substitute for excisional biopsy in the clinical investigation and management of patients with both suspected and unsuspected sarcoidosis.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Cytology files were searched for all FNAB cases of granulomatous inflammation in which sarcoidosis was either noted as a cytologic diagnosis or mentioned in the differential diagnosis of the cytopathology report. The organ sampled by FNAB, the cytologic features, especially the presence and character of granulomatous inflammation, and performance of special stains for microorganisms were evaluated. When available, surgical pathology reports and clinical records were reviewed to determine the clinical presentation, extent of disease, and radiologic abnormalities. Laboratory data supportive of the diagnosis of sarcoidosis were noted, such as excisional biopsy, serum angiotensin-converting enzyme (ACE) levels, BAL results, and microbiology culture results.

An estimate was made of the number of histologically diagnosed cases of sarcoidosis at four of the five participating institutions. A conservative estimate of the relative cost of FNAB and excisional biopsy was attempted by comparing the allowed Medicare reimbursement and the relative value units (RVUs) per current procedural terminology code for each organ sampled. The RVUs are derived from the medical resource-based relative value scale. The RVU takes into account physician work, practice expenses, and malpractice, and is intended to provide an estimate of the actual cost of the procedure irrespective of geographic factors.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Thirty-two patients were identified in whom granulomatous inflammation was found on FNAB with sarcoidosis mentioned in the cytologic differential diagnosis. Slides for review or a sufficiently detailed microscopic report were available for 28 patients who thus made up the study group.

Patient Characteristics
Thirty-two FNABs were obtained from 28 patients (11 men and 17 women), with ages ranging from 12 to 83 years (average age, 40.8 years). Race, noted in 21 patients, consisted of 12 white and 9 African-American patients.

Seventeen sampled sites were palpable masses, and included the parotid gland (n = 4), submandibular gland (n = 4), and lymph node (LNs) in various sites (n = 9). The remaining 15 sites were deep, nonpalpable masses including thoracic LNs (transbronchial [n = 5], percutaneous [ n = 1]), retroperitoneal LNs (n = 2), and liver (n = 2) and lung masses (n = 5; Table 1 ). Sixteen patients (57.1%) had lesions at multiple sites, although each lesion was not sampled by FNAB in most patients. Of these 16 cases, 11 involved the lung or mediastinal LNs. Of the remaining 12 patients with unifocal disease, 7 had pulmonary or mediastinal lesions. In all, pulmonary/mediastinal disease was present in 64.3% of the patients.


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  		Table 1. FNAB Sites

 
Clinical impressions were recorded in 20 patients and included a history of sarcoidosis (n = 4), a clinical suspicion of sarcoidosis (n = 7), sarcoidosis noted in the pathologic differential diagnosis (n = 3), suspected cirrhosis (n = 1), suspected malignant lung tumor (n = 1), suspected parotid neoplasm (n = 2), and suspected non-Hodgkin’s lymphoma (n = 2; Table 2 ).


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  		Table 2. Clinical Impression or History Prior to FNAB (n = 28)

 
Chest radiograph showed mediastinal or hilar lymphadenopathy in 16 cases and pulmonary infiltrates or masses in 10 cases (Table 3 ), of which 7 were associated with hilar or mediastinal lymphadenopathy. The pulmonary abnormalities were described as an interstitial-reticular pattern in three patients; as a reticulonodular pattern in one patient; as a left lower lobe infiltrate, not otherwise specified, in one patient; and as lung nodule(s) in three patients. The three lung nodules consisted of a 2-cm spiculated mass in the right upper lobe in one patient; as two left lung masses, one in the left lower lobe and one in the lingula in the second patient; and as multiple bilateral lung nodules, not otherwise specified, in the third patient. Of these three, only the patient with the spiculated mass had hilar adenopathy. Finally, in two patients, a radiologic description of the pulmonary abnormalities was not available, although the lung was the site of aspiration in these two cases.


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  		Table 3. Radiologic Findings (n = 28)

 
ACE was measured in the serum of seven patients and was elevated in four patients. BAL was performed in seven cases and showed chronic inflammation in three, no inflammation in one, granulomatous inflammation in one, and nonspecific negative findings in two. Special stains for acid-fast bacilli (AFB) by Ziehl-Neelsen method and for fungi by Gomori methenamine silver method on the BAL material with granulomatous inflammation were negative. One sputum cultured for AFB was negative.

Cytologic Findings of Aspirate Samples
FNAB of palpable lesions were obtained with 1- to 1.5-inch, 22- to 27-gauge needles. Longer needles of similar gauge were used for deep lesions accessed under radiologic guidance. At times, thin-needle core biopsies as well as cytology smears were obtained by the radiologist, using a 18- to 22-gauge hollow needle.

Review of the cytologic smears or of the detailed microscopic FNAB report revealed well-formed granulomas in all cases characterized by tightly aggregated groups of at least 10 histiocytes with ovoid to elongate, often twisted nuclei and moderately abundant amphophilic cytoplasm (Fig 1 ). The histiocyte shape varied from epithelioid to spindled. The size of the granulomas varied from small to large, but tended to be uniform in any given case (Fig 2 ). The number of granulomas also varied from few (one to three) to many. Multinucleated giant cells and single epithelioid histiocytes were often present in association with granulomas (Fig 3 ).



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  		Figure 1. Well-formed granuloma without necrosis composed of histiocytes with ovoid to elongate often-twisted nuclei in a FNAB from a cervical LN (Giemsa stain, original x 400).

 


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  		Figure 2. Large granuloma (arrow) in FNAB of salivary gland with salivary gland acini (arrowhead) present in bottom of field (hematoxylin and eosin stain, original x 200).

 


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  		Figure 3. Multinucleated giant cell (arrow) and small granuloma (arrowhead) in FNAB from a cervical LN (Papanicolaou stain, original x 400).

 
Special stains for AFB and fungi were performed in 16 cases on smears and were negative in all 16. Cultures for AFB from three aspirates were negative. Flow cytometry to rule out lymphoma was performed on one FNAB specimen and did not demonstrate a monoclonal lymphoid population.

To our knowledge, no complications resulted due to the FNAB procedure in the 28 patients.

Histologic Findings
Sixteen patients had open biopsies from 22 sites for confirmation. The sites undergoing biopsy included LN (n = 10), liver (n = 3), skin (n = 3), lung (n = 5), and parotid gland (n = 1). All biopsies demonstrated nonnecrotizing granulomatous inflammation. In two instances—a groin LN and the parotid gland—minimal necrosis was present. Tissue from biopsy was cultured in four cases, and all cultures were negative.

Special stains and/or cultures for mycobacteria and for fungi were performed on the FNAB or biopsy material in 22 of the 28 patients (78.6%).

Comparative Cost Analysis
Four of the five institutions supplied estimates of the number of histologically diagnosed sarcoidosis cases for comparison to those diagnosed by FNAB. The ratios of histologic biopsy to FNAB were 19:1, 16:1, 4:1, and 4:1. The comparison of the relative cost (the allowed Medicare reimbursement in dollars and the RVU) of FNAB and excisional biopsy is shown in Table 4 . A biopsy of a superficial LN commanded a Medicare reimbursement of $202 (in the Boston area) with an RVU of 4.73, while FNAB of the same site was reimbursed $85 and had a RVU of 2.35; the surgical biopsy of a superficial LN "cost" 2.4 times the FNAB. The Medicare reimbursement and the RVUs for surgical biopsies of all other sites were considerably higher than FNABs of the same site, with biopsy to FNAB charge ratios varying from 4.6:1 for a liver sample to 8:1 for major salivary gland sampling.


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  		Table 4. Comparative Cost of Surgical Biopsy and FNAB for Diagnosis of Sarcoidosis*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Sarcoidosis is an illness of unknown etiology characterized by nonnecrotizing granulomatous inflammation involving one or more organs. Estimates vary, but between 20 to 40% of patients present with asymptomatic bilateral hilar lymphadenopathy.2 In the remainder, a variety of tissues may be affected and mass lesions may result. Tests formerly believed to be diagnostic of sarcoidosis have proven to be nonspecific. These include serum ACE, which can be elevated in a variety of granulomatous diseases, and BAL fluid analysis.3 The Kveim-Stilzbach skin test, although highly specific, is not standardized and not widely available.

While bilateral hilar lymphadenopathy, either asymptomatic or associated with erythema nodosum, uveitis, arthralgias, and minor pulmonary symptoms, is clinically evocative of sarcoidosis, leading some authors to suggest elimination of biopsy in clinical stage-1 disease,4 tissue sampling with demonstration of nonnecrotizing granulomas is usually advised to secure the diagnosis. In patients who present with findings uncharacteristic of sarcoidosis, such as isolated superficial and/or deep parenchymal nodules or masses with no history to suggest the diagnosis, tissue diagnosis is necessary. Recent reviews of sarcoidosis advocate tissue biopsy of the most accessible organ, which usually is the skin or bronchus. However, the reviewers do not mention the feasibility of FNAB,1 2 despite a host of publications advocating FNAB of various organs for the diagnosis of sarcoidosis.5 6 7 8 9 10 11 12 13 14 15 16 17 The use of FNAB has also been advised as an adjunct to the diagnosis of childhood sarcoidosis.5 11 To the best of our knowledge, none of the previous studies have performed a comparative cost analysis of FNAB vs histologic sampling in the diagnosis of sarcoidosis.

Most of our specimens were obtained percutaneously either by the clinician, cytopathologist, or radiologist. In five patients, transbronchial FNAB of carinal LNs obtained adequate material for diagnosis by flexible fiberoptic bronchoscope. When radiologic guidance is used for lung or other deep sites, fine-needle core biopsies are often obtained along with FNAB smears. Also, our cases, described radiologically as lung masses prior to FNAB, in reality are better described as "pseudomasses," since they correspond to alveolar infiltrates. Pulmonary nodules are uncommon in sarcoidosis but are known to occur.18

Complications due to FNAB are infrequent.19 20 Aspiration using larger-bore needles and aspiration of deep organs are more likely to produce complications. Hematoma or hemorrhage is probably the most common untoward event.

To be suggestive of sarcoidosis, one must first identify epithelioid granulomas, usually accompanied by multinucleated giant cells. Although requisite for a tissue diagnosis of sarcoidosis, the finding of nonnecrotizing granulomas in tissue whether by FNAB or by incisional biopsy is nonspecific, since granulomatous inflammation is a response to a variety of infections, toxic agents, and neoplasms. In most instances, the pathologist will diagnose nonnecrotizing granulomatous inflammation and then in a note enumerate the differential diagnoses. To put our cases in perspective, we searched the pathology records of Massachusetts General Hospital (MGH) to estimate the frequency with which various malignancies were diagnosed as compared to sarcoidosis for 1993 by surgical pathology and cytopathology: carcinoma (n = 1,774), malignant lymphoma (n = 194), and Hodgkin’s disease (n = 52). During that same year, 31 cases of sarcoidosis were diagnosed and all by surgical pathology. Since only eight of the current FNAB study cases are from MGH, and these were culled from cytology files of > 14 years, one can appreciate the rarity with which the diagnosis of sarcoidosis is suggested by FNAB.

Infectious agents are probably the most common cause of granuloma formation to be ruled out; microorganisms can be demonstrated in sampled tissue on routine stain or by additional stains. Cytologic smears containing granulomas can be decolorized after initial examination and restained with AFB stain for mycobacteria and silver stain for fungal elements. If during an immediate evaluation of the specimen at the time of sampling, granulomatous inflammation is identified, a portion of the aspirated material can be submitted for the appropriate cultures. Studies have shown that special stains are often more effective than cultures in identifying yeast in tissue obtained by open lung biopsy.21 In lung FNABs, fungal culture has been found to be less sensitive than special stains.22 Also, fungal infections often produce necrosis, and fungal elements may be visible on cytologic smears stained with Papanicolaou, hematoxylin and eosin, or Giemsa stains.23 24 Although a small amount of fibrinoid necrosis may be identified in sarcoidosis, a significant amount is uncharacteristic. Two of our cases demonstrated focal noncaseating necrosis on biopsy but not on FNAB.

Unlike fungal infection, culture is often more sensitive than special stains for mycobacteria,25 26 27 except in the study by Renshaw21 on open lung biopsies, in which only half of the six cases positive for AFB by acid-fast stain had positive cultures. Although mycobacterial infection is also often associated with necrosis, this is not always so. In a review of 39 cases of tuberculosis, Bailey et al25 identified 18 cases in which epithelioid granulomas predominated on FNAB with scant necrosis; of these, fluorescent auramine-rhodamine stain identified 5 cases showing mycobacteria, while culture identified 12. Lapuerta et al26 found in a comparative study of HIV and non-HIV-associated tuberculosis, that in both groups necrosis was present in a minority of cases and that culture was more sensitive than special stain. Khan et al27 describe a group of 12 patients with strongly positive tuberculin skin tests and isolated mediastinal adenopathy, most often right-sided paratracheal, who underwent FNAB. Only eight specimens were diagnostic for mycobacteria, but the findings in the falsely negative cases were not detailed. Again cultures were more sensitive than special stains for detecting mycobacteria. If suspicion is high, but smears and cultures are negative, polymerase chain reaction will permit diagnosis of mycobacteria.28

Cat-scratch disease will also produce granulomatous inflammation, but the granulomas are suppurative in nature.29

From the information available to us, only 22 of 28 patients had special stains or cultures applied to their material. At times, if little material is obtained by FNAB, the pathologist may forego performing special stains, with the thought that the diagnostic possibilities have been narrowed and the clinician will obtain additional material. Although the six cases without studies to rule out microorganisms were suboptimally evaluated, in certain instances the findings are clinically useful. An illustrative example among our cases was that of a 35-year-old woman who presented to her internist in September 1996 with a small nodule behind the left ear and a diffuse reticulonodular infiltrate on the chest radiograph. CT scan of the head showed bilateral abnormalities of the parotid glands. An FNAB of the palpable mass showed nonnecrotizing granulomas. Insufficient material was deemed present to perform special stains. The pathologist indicated that the differential diagnosis included sarcoidosis, mycobacterial or fungal infection, and, although unlikely, lymphoma. The patient was found subsequently to be nonreactive to a panel of skin tests (purified protein derivative, Candida, Trichophyton, and mumps). Titers of serum antibodies to cryptococcal antigen and coccidiomycosis antigen were within the normal range. The patient was seen by a pulmonologist in March 1997, at which time the chest radiograph showed improvement without therapy, which was thought to argue in favor of sarcoidosis, so no attempt was made to obtain additional material for culture. By June 1997, the clinical picture was compatible with a spontaneous remission of sarcoidosis, and the patient continues to remain well as of May 1999.

Although exceedingly rare, another situation of which to be aware is the presence of sarcoid-like granulomas without evidence of intracellular bacilli in regional LNs draining organs affected by Whipple’s disease.30 31

Granulomatous inflammation can be found adjacent to a malignant tumor, most commonly in Hodgkin’s disease, malignant lymphoma, and seminoma.32 33 One report gives the following frequencies of sarcoid-like reactions in patients with malignant tumors: 4% for solid tumors, 7% for non-Hodgkin’s lymphoma, and 14% for Hodgkin’s disease.34 We searched the computerized MGH pathology files for nonnecrotizing or sarcoid-like granulomas associated with malignancy in the same tissue and found such responses in only five primary lung tumors, two metastatic tumors to the lung (malignant fibrous histiocytoma and melanoma), one squamous cell carcinoma metastatic to LN, and two cases of Hodgkin’s disease in LN and spleen. Thus, at one of the our institutions, granulomatous response to tumor appears to be uncommon. However, an FNAB of a mass harboring malignancy and granulomas would be problematic. Careful evaluation of all cells on the smears in which granulomas have been identified is mandatory, for any suggestion of cytologic atypia must be further explored as illustrated by the six cases reported by Khurana et al,35 in which cytologic evidence of granulomatous inflammation accompanied a malignancy. In order to avoid misdiagnosis of a malignant lymphoma at MGH, a portion of all FNAB specimens with a significant lymphoid component is submitted for flow cytometry. Unless a careful search is made when confronted with granulomatous inflammation, one may overlook Reed-Sternberg cells, as was reported by Kardos et al.36 Hodgkin’s disease cannot be diagnosed by flow cytometry, and if Reed-Sternberg cells are not identified, the diagnosis can only be suspected by accompanying atypical mononuclear cells and a background of a mixed inflammatory infiltrate containing eosinophils.

In other cases, regional LNs draining a malignancy or even LNs draining a different anatomic region than that harboring the malignancy can show a sarcoid-like granulomatous response.37 The frequency of such a response is unknown, but a search of the MGH pathology records found that of 150 cases of nonnecrotizing granulomas, only 3 cases of sarcoid-like granulomas in LNs removed at the time of surgery for malignancy (lung, stomach, and vagina). In a review of FNAB of granulomatous disease, Klemi and Joensuu17 identified 5 cases of unifocal sarcoid-like reaction in LNs of patients with a history of malignancy out of a total of 21 cases. When confronted with a mass lesion and regional lymphadenopathy, a prudent approach would be nonetheless to sample both sites. An example of this problem occurred in one of our patients, a 37-year-old woman who presented with a 2-cm spiculated lesion of the right upper lobe of the lung and bilateral mediastinal lymphadenopathy. Initially, carcinoma was strongly suspected; however, LNs obtained at mediastinoscopy showed only nonnecrotizing granulomas. Knowing that LNs draining a malignancy can demonstrate a sarcoid-like response, a subsequent FNAB was performed on the spiculated lung mass, but this too revealed only granulomatous inflammation. Thus, this patient’s illness was believed to be compatible with sarcoidosis. At the time of her last chest radiograph, 1.5 years after the above procedures, bilateral ill-defined nodular opacities of the lungs with mediastinal and hilar lymphadenopathy are still present consistent with sarcoidosis.

Once the pathologist has identified the lesion as nonnecrotizing granulomatous inflammation and ideally has eliminated conventional infectious agents or malignancy from the differential diagnosis by negative special stains and/or cultures and flow cytometry, the clinician needs to exclude other possible etiologies.

A detailed occupational, environmental, and medical history including medications is necessary. As already mentioned, serologic and skin tests for mycobacterial and fungal disease can be performed. Beryllium can cause granulomatous inflammation indistinguishable from sarcoidosis, but a history of exposure, even minor, should be elicited and the beryllium lymphocyte proliferation test should be positive.3 Wegener’s granulomatosis tends to have significant necrosis and no well-formed granulomas, with only single epithelioid histiocytes, multinucleated giant cells, neutrophils, and lymphocytes. An antineutrophil cytoplasmic antibody test will almost always be diagnostic.38 39 40 Exceptionally, primary biliary cirrhosis may involve the lung.41 On rare occasions, sarcoid may clinically involve only the liver, simulating primary biliary cirrhosis.42

Finally, savings can be realized by use of FNAB in contrast to open biopsy, as demonstrated by our cost analysis using RVU for various organs. We calculated that a $13,000 savings would have been possible had all our cases been diagnosed by FNAB only. The same conclusion was reached in a recent study by Rimm et al43 of cytopathology cases seen over 20 years at the Medical College of Virginia. Despite the potential savings, clinicians at our institutions continue to perform far more open biopsies for sarcoidosis rather than FNAB. At MGH, we identified 31 cases of sarcoidosis diagnosed by incisional biopsy in 1993 alone. Although clinicians may be concerned that a cytologic diagnosis of a nonnecrotizing granulomatous process with a differential diagnosis of sarcoidosis would necessitate an additional procedure to secure the diagnosis, we contend that open biopsy is fraught with the same problems that plague the FNAB diagnosis of sarcoidosis: the nonspecificity of the granulomatous process with the challenge of finding the causative or associated serious disease. We believe that FNAB for mass lesions of sarcoidosis should be more extensively utilized based on our multi-institutional study, which demonstrates that it is a cost-effective diagnostic procedure, especially for the maintenance of patients with an established diagnosis.


   Acknowledgements
 
The authors would like to express their gratitude to Dr. W. Stephen Black-Schaffer for his assistance with the financial data.


   Footnotes
 
Abbreviations: ACE = angiotensin-converting enzyme; AFB = acid-fast bacilli; FNAB = fine-needle aspiration biopsy; LN = lymph node; MGH = Massachusetts General Hospital; RVU = relative value unit

PA; and the University of Arkansas for Medical Sciences (Dr. Bardales), Little Rock, AR.

Presented in abstract form at the Annual Meeting of the American Society of Cytopathology, Boston, MA, November 4–8, 1997.

Received for publication March 5, 1999. Accepted for publication October 18, 1999.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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