Diagnostic value of cervical lymph node biopsy: A pathological study of 596 cases

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Journal of Surgical Oncology 42:239-243 (1989)

Diagnostic Value of Cervical Lymph Node Biopsy: A Pathological Study of 596 Cases SAMlR S. AMR, MD, M O H A M M A D F. KAMAL, MD, PhD, AND MUSLEH S. TARAWNEH, From the Department of Pathology, lordan University Hospital, Amman, lordan

MD

During a 10-year period (1976-1985), a total of 596 cervical lymph node biopsies for diagnostic purposes were performed at our institution. Thirtyfive percent of these nodes were involved with malignant lymphoma, and 20.5% showed metastatic deposits. Nondiagnostic reactive hyperplastic changes were noted in 23% of the cases. Several other inflammatory and neoplastic conditions were encountered. Comparison of our data with several series from different countries with review of relevant literature are presented. KEY WORDS:lymph nodes, biopsy, lymphoma, metastatis, lymphoid hyperplasia

INTRODUCTION Enlargement of the peripheral lymph nodes is a common clinical presentation of a variety of pathological conditions, including lymphoreticular malignancies, metastatic malignant processes, reaction to local or systemic inflammatory conditions, and in response to systemic autoimmune diseases and immunization. Cervical lymph nodes are the most frequently enlarged and biopsied of all peripheral lymph nodes affecting patients of different age groups, as judged from several series on peripheral lymphadenopathy in various countries [ 1-51. They have the best diagnostic yield according to large studies on the subject [1,6], and this probably prompts many physicians to biopsy them in search of a diagnosis. In this report, we present our experience with 596 cases of cervical lymphadenopathy and discuss the value of the cervical lymph node biopsy as a diagnostic tool, with comparison of our findings with those reported from other parts of the world. MATERIAL AND METHODS The records of the Laboratory of Surgical Pathology, Jordan University Hospital, for a 10-year period (19761985) were reviewed. All cases of cervical lymph node biopsies were extracted, and data regarding name, age, sex, associated clinical manifestations, results of laboratory and radiological investigations when available, and surgical pathology serial numbers were recorded and tab0 1989 Alan R. Liss, Inc.

ulated. All of these cases had been reviewed, diagnosed, and reported by the authors. At least one histological section stained with hematoxylin and eosin was examined in each case. Additional special stains including Ziehl-Neelsen’s stain for acid-fast bacilli, Gomori’s stain for fungus, reticulin and Periodic acid-Schiff (PAS) stains were obtained when indicated. Careful attention was given to patients who had more than one biopsy, and they were counted only once if the biopsies had the same diagnosis. Patients who underwent cervical lymphadenodectomy as a part of another operation on head and neck organs-such as thyroidectomy , laryngectomy, or radical neck dissection for a known primary malignant neoplasm-were not included in this study.

RESULTS There were 376 male and 220 female patients, and their ages ranged from 6 months to 83 years. Table I lists the cases according to pathological diagnosis and sex of the patients. Table I1 illustrates the age distribution of the most significant pathological conditions. Reactive lymphoid hyperplasia, a nonspecific response to a multitude of antigenic stimuli, accounted for Accepted for publication June 12, 1989 Address reprint requests to Samir S . Amr, M.D., Consultant Pathologist, Dhahran Health Center, ARAMCO, P.O. Box 8341, Dhahran3131 1, Saudi Arabia. Dr. Amr is now at the Dhahran Health Center, Dhahran, Saudi Arabia.

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TABLE 1. Cervical Lymph Node Biopsies, Jordan University HosDital (19761985)

TABLE 111. Follow-Up Diagnosis in 31 Patients With Reactive Lymphoid Hyperplasia*

Pathological condition

Diagnosis

Males (%)

I. Inflammatory conditions Reactive hyperplasia Tuberculous lymphadenitis Sarcoidosis Toxoplasma lymphadenitis Cat scratch lymphadenitis Acute lymphadenitis Necrotizing lymphadenitis

11. Neoplastic conditions Hodgkin’s disease Non-Hodgkin’s lymphoma Leukemic infiltrate Angio-immunoblastic lymphadenopathy Histiocytosis-X Malignant histiocytosis Waldenstrom’s disease Metastatic tumours Total

Females (%) Totals (%)

88 (23.40) 21 (05.60) 5 (01.30) 25 (06.60) 1 (00.30) 0 (00.00) 0 (00.00)

49 (22.30) 137 (23.00) 24 i10.90) 45 (07.50) 6 (02.70) 11 (01.90) 10 (04.55) 35 (05.90) 2 (00.90) 3 (00.50) 4 (01.80) 4 (00.70) 1 (00.45) 1 (00.17)

68 (18.10) 66 (17.50) 12 (03.20)

49 (22.30) 117 (19.60) 27 (12.30) 93 (15.60) 4 (01.80) 16 (02.70)

3 (00.80) 1 (00.30) 1 (00.30) 1 (00.30) 84 (22.30)

5 (01.40) 6 (1.00) 2 (00.90) 3 (00.50) 0 (00.00) 1 (00.17) 0 (00.00) I (00.17) 31, (17.70) 123 (20.60)

Non-Hodgkin’s lymphoma Hodgkin’s disease Carcinoma of lung Carcinoma of esophagus Carcinoma of gallbladder Hepatocellular carcinoma Rhabdomyosarcoma, head, and neck Synovial sarcoma, right shoulder Th ymoma Systemic lupus erythematosus Mixed connective tissue disease Behcet’s disease Idiopathic thrombocytopenic purpura Infectious mononucleosis Total

No. of cases

Percent

5 3 6

16.13 9.70 19.35 3.22 3.22 3.22 9.70 3.22 3.22 6.45 3.22 6.45 6.45 6.45 100.00

1 1

1 3 1 1 2 I 2 2 2 31

*Percentages are calculated in relation to total of 31 cases that had follow-up data.

376 (100.00) 220 (100.00) 596 (100.00)

TABLE 11. Cervical Lymph Node Biopsies (1976-1985) Age Distribution* Age group (years)

0-10 11-20 21-30 31-40 41-50 51-60 >60 Grand total

Reactive Hyperplasia

T.B.

Toxoplasma Lymphadenitis

Hodgkin’s disease

Non-Hodgkin’s lymphoma

38 (41.8) 30 (28.3) 32 (30.8) 10 (14.9) 12 (12.1) 11 (14.3) 04 (07.7)

01 (01.1) 10 (09.4) 15 (14.4) 06 (08.9) 07 (07.1) 05 (06.5) 01 (01.9)

05 (05.5) 14 (13.2) 08 (07.7) 04 (06.0) 04 (04.0) 00 (00.0) 00 (00.0)

22 (24.2) 32 (30.2) 22 (21.1) 11 (16.4) 15 (15.1) 11 (14.3) 04 (07.7)

09 (09.9) 10 (09.4) 12 (11.5) 11 (16.4) 20 (20.2) 16 (20.8) 15 (28.8)

137 (23.0)

45 (07.5)

35 (05.9)

117 (19.6)

93 (15.6)

Metastatic tumors

Others

Total

06 (06.6) 05 (04.7) 05 (04.8) 21 (31.4) 33 (33.3) 29 (37.6) 24 (46.1)

10 (10.9) 05 (04.7) 10 (09.6) 04 (06.0) 08 (08.1) 05 (06.5) 04 (07.7)

91 (100.0) 106 (99.9) 104 (99.9) 67 (100.0) 99 (99.9) 77 (100.0) 52 (99.9)

123 (20.6)

46 (07.8)

596 (100.00)

*Numbers in parentheses represent percentage of cases in relation to total cases of an age group. Percentages of grand total are also calculated.

the largest share (23%) of these lymph nodes. Follow-up data was available on 88 cases, and 31 of these were found to have an underlying or associated pathological process identified later on by another biopsy or by other laboratorty means (Table 111).It is of interest to note that 70% of these patients (22 cases) were affected by a malignant tumor. The second most frequent cause 01’ cervical lymphadenopathy is metastatic tumor. Table LV lists, in order of frequency, the primary sites of these neoplasms. Cancer of the lung heads the list followed by nasopharyngeal carcinoma. There are 13 cases in which the primary site is unknown in spite of extensive clinical and radiological work-up. Hodgkin’s disease and non-Hodgkin’s lymphoma rank third and fourth in the order of frequency. However, if both are combined together, lymphomas as a whole rank first in this series. This probably reflects a bias of selection of patients in our hospital, which is a major referral center for neoplastic diseases for the whole country.

About two thirds of cases of Hodgkin’s disease occur in the first three decades of life; two thirds of the patients affected with non-Hodgkin’s lymphomas are above the age of 30 years. Tuberculous lymphadenitis was found in 45 cases; more than half of these patients were in the second and third decades of life. Other granulomatous diseases were encountered, including 11 cases of sarcoidosis and three cases of cat scratch lymphadenitis. Toxoplasma lymphadenitis was present with a fair amount of frequency (5.9%) in this series. Considering the ubiquitous distribution of Toxoplasma gondii throughout the world and the tendency of young children and adolescents to be infected, it is not surprising to encounter this number of patients.

DISCUSSION Persistently enlarged lymph nodes in the neck is a common problem confronting physicians and causing much concern and suspicion of malignancy, particularly

Cervical Lymph Node Biopsy 241 from one anatomic site to another [I]. The cervical Organisite No. of cases Percent lymph node biopsy gives the highest diagnostic yield, ranging from 53% to 76.4% [6]. The supraclavicular 35 28.46 Lung lymph nodes have, in particular, the best diagnostic yield 21 17.10 Nasopharynx of all peripheral lymph node biopsies, reaching 85.2% 13 10.57 Unknown 10 8.13 Breast [5] to 90% [6]. In the present study, we had a high 9 7.32 diagnostic yield of 77%. Stomach 9 1.32 Thyroid Biases of selection and referral of patients by treating 4 3.25 Mediastinum, neuroblastoma physicians for biopsy procedure in a tertiary care hospital 3.25 4 Skin, melanoma with active oncological service, like ours, should always 2.44 3 Esophagus 3 2.44 Larynx be considered when interpreting the data of such a study 2 1.62 as this one. Nevertheless, we feel that our results reflect, Tonsil 2 I .62 Neck, rhabdomyosarcoma with few reservations, causes of persistent cervical lym1 Skin, Kaposi’s sarcoma 0.81 phadenopathy in our population. 1 Lip 0.81 Hodgkin’s and non-Hodgkin’s lymphomas rank first 1 Salivary gland 0.81 1 0.81 Pleura in our series, accounting for 35.2% of the cases. This is 1 0.81 Gallbladder a reflection of the high frequency of lymphoreticular 1 0.81 Pancreas malignancies among all cancers in Jordan. Lymphomas 1 0.81 Prostate account for 10.2% of all malignancies in all age groups I 0.81 Ovary in Jordan [13] and 28.7% of all malignant neoplasms in 123 100.OO Total Jordanian children [ 141. Hodgkin’s disease is seen in all age groups, but it is noteworthy that 54 cases, representing 46% of all pawhen they are painless and firm. Many of these nodes tients with Hodgkin’s disease, occur in the first two demay have an apparent underlying cause, which can be cades of life, thus confirming our findings in a previous discovered on careful physical examination or laboratory study on Hodgkin’s disease in Jordanian children [ 151. The mean age of Jordanians affected by non-Hodginvestigations. Nevertheless, the physician will be faced with that enlarged lymph node or group of nodes in the kin’s lymphoma was reported to be 32.4 years, with 22.5% of patients below the age of 10 [16]. In the present neck without apparent or obvious etiology. Greenfield and Jordan [7] presented an algorithm for study, the mean age of our patients is 41 years, and only the clinical investigation of lymphadenopathy in primary 10% of them are within the first decade of life. This is care practice. After exclusion of local lesions or infec- due to the fact that our material is derived solely from tions, toxoplasmosis, cytomegalovirus, and Epstein-Ban cervical lymph nodes, whereas 43.3% of all cases of virus mononucleosis, they suggested that other systemic non-Hodgkin’s lymphomas in Jordanians were found in conditions must be pursued by biopsy of the persistent extranodal sites [ 161, particularly Burkitt’s lymphoma, enlarged lymph nodes. However, other authors, mostly which accounts for 33% of all pediatric lymphomas in head and neck surgeons, warned against untimely lymph Jordan [14], 75% of which are located in the abdomen node biopsy [8], particularly in the elderly patient, who ~ 7 1 . In the United States, lymphomas rank third, after remight have an occult primary tumor in the head and neck area or who had a cursory examination without discov- active hyperplasia and metastatic carcinoma, being diagering the primary site, as vividly illustrated by Martin nosed in 18% of cervical lymph nodes and in 15% of all and Romieu in their classic paper on lumps in the neck peripheral lymph node bioipsies in one large series from [9]. An increase in the incidence of distant metastases in California [I]. Metastatic tumors comprise the second largest group patients who had cervical lymph node biopsy before definitive treatment has been reported [ 101. Gooder and with diagnostic yield. Four organs account for about Palmer [ 111 reported that the incidence of wound sepsis 70% of all metastatic deposits with the lung having the and fungation of tumor through the skin is higher in lead. This is similar to a study from England [2], where patients with head and neck cancer who had undergone carcinomas of the lung represent 30% of all primary such biopsy, with potential compromise of subsequent carcinomas presenting with cervical lymphadenopathy. Thirteen cases (10.5%) of metastatic tumors in our study radical surgical excision. In spite of these reservations, lymph node biopsy re- are of unknown primaries. Silent primary tumors metasmains a time-honored diagnostic technique [5]. The di- tasizing to the cervical lymph nodes represent a diagnosagnostic yield of superficial enlarged lymph node biop- tic dilemma facing the treating physicians, and, in spite sies varies widely from one series to another [I21 and of extensive work-up, there is always a group of cases TABLE LV. Primary Sites of Metastatic Tumors (123 Cases)

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ranging from about 4% to 56% in which no primary focus has ever been found [ 181. Martin and Morfit [ 191, in a large study of carcinomas all with metastatic lesions in the neck, found that cervical metastasis was the first symptom in 7.87% of mouth and pharyngeal cancers, 8% of thyroid citncers, and 1% of esophageal cancers. They also noted that in more than 50% of the nasopharyngeal carcinoma, cervical metastasis was the most frequent initial complaint, a figure close to our observation of 2 1 in 39 cases with nasopharyngeal carcinoma diagnosed in our hospital presenting initially with lymph node metastases. Reactive lymphoid hyperplasia, a nonspecific reactive process in which a specific diagnosix cannot be made, accounts for about one fourth of all cases in this series. In the first decade of life, this process is seen in 42% of the biopsies. This high frequency of nondiagnostic hyperplasia in cases of peripheral lymphadenopathy in young patients had been observed hy several authors [20,2 1,221, ranging from 3 1.7% to 52% of biopsied peripheral lymph nodes. This had been attributed to the fact that children manifest more rapid and exaggerated lymphoid hyperplastic response to inflammatory stimuli than adults [23]. The amount of lymphoid tissue is considerable at birth, steadily increases to pulxrty, and then undergoes a relative reduction. In a recent study, 34% of neonates and 58% of infants up to I year of age were found to have palpable lymph nodes at single or multiple sites [24]. Follow-up of 88 of our patients with reactive lymphoid hyperplasia demonstrates that 22 (25%) show a malignant neoplasm, including eight cases of lymphoma and six cases of carcinoma of the lung (Table 111). In a study of 105 adult male patients with nondiagnostic reactive lymph nodes, 53% developed a discase related to the indications for biopsy on follow-up for 5 years or until death in less than 5 years [25]. On the other hand, Kissane and Gephardt [26] followed the outcome of 37 children with nondiagnostic lymph node biopsies, which included 21 cervical lymph nodes, and found that 25 patients (74%) were alive and well 5 to 20 years later. Only three patients developed lymphoreticular malignancy, and another four had thrombocytopenia. Tuberculous lymphadenitis constitutes 7.5% of our cases, a frequency that is substantially lower than rates reported in neighbouring Arab countries, including Iraq (54%) [27], Saudi Arabia (53%) [28], and in African countries, where the frequency varies from 37.6% in Nigeria [3] up to 49.2% in Kenya [4]. This low frequency could be due to bias of seleciion of patients and does not necessarily reflect low frequency of tuberculous lymphadenitis in Jordan. Toxoplasma gondii has a worldwide distribution, with variable prevalence rates [29]. In Jordan, 31% of females

and 28% of males in a series of 917 adults tested for toxoplasma antibodies had a positive reaction with a titre of 1/32 or greater [30]. Involvement of peripheral lymph nodes by this protozoal infection had been observed in several studies on peripheral lymphadenopathy from various countries, with frequency rates ranging from 1.8 in Ireland [31] to 17.39% in India [32]. In a study of 237 histologically diagnosed and serologically verified cases from Finland [33], 85% of the nodes were cervical. The frequency rate of 5.9% in our material is close to the rate reported in a series from Singapore (7.4%) on 203 cervical lymph node biopsies [34]. Sarcoidosis is considered rare in the Middle Eastern Arab countries [35], and few cases have been reported from Saudi Arabia [35] and Iraq [36]. However, in Jordan, this multisystemic granulomatous disease is not as rare as it is thought to be, and there have been more than 20 cases diagnosed and treated in our hospital in the last 10 years. The diagnosis was confirmed in about half of these cases by a cervical lymph node biopsy. Six patients had angioimmunoblastic lymphadenopathy, il lymphoma-like syndrome described first in 1974 by Frizzera et al. [37]. We reported our experience regarding treatment of some of our cases with a conibination of vincristine, adriamycin, and prednisolone elsewhere [38]. In 1972, Kikuchi reported several patients from Japan with necrotizing lymphadenitis associated with histiocytic proliferation simulating lymphoma [39]. Various infectious agents were suspected, including toxoplasma, Epstein-Barr virus, Yersina, and cytomegalovirus, but none was conclusively implicated. This condition was later described in reports from the United States [40], Germany [41], and England [42] occurring in patients of several nationalities. We encountered one case of this entity, which we believe will be recognized more frequently as pathologists are becoming aware of it in recent articles and editorials [43]. Study of lymph node biopsies will continue to pose a challenge to pathologists. There are multiple causes for misdiagnosis, which can be traced to surgical procedure, technical processing of biopsy material, or interpretation of lesions of lymph nodes [44]. The need to have profound knowledge of normal histology of lymph nodes, and particularly their reaction after antigenic stimuli [45], as well as familiarity with the various conditions that can simulate lymphoreticular neoplasms [46,47], has been stressed in the literature. More studies on peripheral lymphadenopathy in general, including various anatomical sites, and lymphadenopathy involving patients of certain age groups, particularly children and adolescents, are needed to understand and to elucidate the causes of lymph node enlargement in various geographic areas of the world.

Cervical Lymph Node Biopsy

ACKNOWLEDGMENTS The authors wish to thank Mr. Mumtaz Akhtar for secretarial help and typing of the manuscript. This work was presented at the Seventeenth International Congress of the International Academy of Pathology which was held at Trinity College, Dublin, Ireland, 4-9 September, 1988. REFERENCES 1. Lee Y-T N, Terry R, Lukes RJ: Lymph node biopsy for diagnosis. A statistical study. J Surg Oncol 14:53-60, 1980. 2. Anthony PP, Knowles SAS: Lymphadenopathy as a primary presenting sign: a clinicopathological study of 228 cases. Br J Surg 701412-414, 1983. 3. Attah EB: Peripheral Lymphadenopathy in Nigeria. Trop Geogr Med 26:257-260, 1974. 4. Kasili EG, Shah TS: Lymphoreticular disease in Kenya. Pathological pattern of the superficial lymphadenopathies. Trop Geogr Med 26:242-256, 1974. 5. Sinclair S , Beckman E, Ellman L: Biopsy of enlarged superficial lymph nodes. JAMA 228:602-603, 1974. 6. Doberneck RC: The diagnostic yield of lymph node biopsy. Arch Surg 118:1203-1205, 1983. 7. Greenfield S , Jordan MC: The clinical investigation of lymphadenopathy in primary care practice. JAMA 240: 1388-1393, 1978. 8. Martin H: Untimely lymph node biopsy. Am J Surg 102:17-18, 1961. 9. Martin H, Romieu C: The diagnostic significance of a “lump in the neck.” Postgrad Med 11:491-500, 1952. 10. McGuirt WF, McCabe B F Significance of node biopsy before definitive treatment of cervical metastastic carcinoma. Laryngoscope 88594-597, 1978. 11. Gooder P, Palmer M: Cervical lymph node biopsy-a study of its morbidity. J Laryngol Otol 98:1031-1040, 1984. 12. Margolis IB, Matteucci D, Organ Jr CH: To improve the yield of biopsy of the lymph nodes. Surg Gynecol Obstet 147:376-378, 1978. 13. Khalidi RH: Pattern of cancer incidence in Jordan 1965-1969, with a discussion. Jordan Med J 7:30-40, 1972. 14. Amr SS, Tarawneh MS, Jitawi SA, Oran LW: Malignant neoplasms in Jordanian children. Ann Trop Paediatr 6:161-166, 1986. 15. Tarawneh MS, Madanat F, Abu Khalaf M, Awidi AS, Shamayleh AM, Amr SS, Karyouti RM: Hodgkin’s disease in Jordanian children: A study of 26 cases. Clin Oncol 10:21-25, 1984. 16. Tarawneh MS: Non-Hodgkin’s lymphomas in Jordanians. A histopathological study of 231 cases. Hematol Oncol4:91-99, 1986. 17. Madanat FF, Amr SS, Tarawneh MS, El-Khateeb MS, Marar B: Burkitt’s lymphoma in Jordanian children: epidemiological and clinical study. J Trop Med Hyg 89:189-191, 1986. 18. Acquarelli MJ, Matsunaga RS, Cruze K: Metastatic carcinoma of the neck of unknown primary origin. Laryngoscope 71:962-974, 1961. 19. Martin H, Morfit HM: Cervical lymph node metastasis as the first symptom of carcinoma. Surg Gynecol Obstet 78: 133-159, 1944. 20. Lake AM, Oski, FA: Perhipheral lymphadenopathy in childhood. 10 year experience with excisional biopsy. Am J Dis Child 132: 357-359, 1978. 21. Knight PJ, Mulne AF, Vassy LE: When is lymph node biopsy indicated in children with enlarged peripheral nodes? Pediatrics 69:391-396. 1982.

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